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QuinoaImprovement and Sustainable

Production

QuinoaImprovement and Sustainable

Production

Edited by

Kevin Murphy and Janet Matanguihan

Copyright © 2015 by Wiley-Blackwell. All rights reserved

Published by John Wiley & Sons, Inc., Hoboken, NewJerseyPublished simultaneously in Canada

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Quinoa : improvement and sustainable production /edited by Kevin Murphy and Glafera Janet Matanguihan.

pages cmIncludes bibliographical references and index.ISBN 978-1-118-62805-8 (cloth)1. Quinoa. 2. Crop improvement. 3. Sustainable

agriculture. I. Murphy, Kevin (Kevin Matthew), 1972-editor. II. Matanguihan, Glafera Janet, editor.

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2015006917

Printed in the United States of America

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Contents

List of Contributors ix

Preface xi

1 Quinoa: An Incan Crop to FaceGlobal Changes in Agriculture 1Juan Antonio González, Sayed S. S.Eisa, Sayed A. E. S. Hussin, andFernando Eduardo Prado

Introduction 1A Brief History of Quinoa Cultivation 2Nutritional Value of Quinoa Seed 2Botanical and Genetic Characteristics of

the Quinoa Plant 5Quinoa and Environmental Stresses:

Drought and Salinity 7Conclusion 12References 12

2 History of Quinoa: Its Origin,Domestication, Diversification,and Cultivation with ParticularReference to the ChileanContext 19Enrique A. Martınez, Francisco F.Fuentes, and Didier Bazile

Quinoa Origins in the Central Andes 19Ancient Expansion to Southern Latitudes

in Chile 20Reintroduction of Quinoa in Arid Chile

after Local Extinction 20

Final Remarks 23References 23

3 Agroecological and AgronomicCultural Practices of Quinoa inSouth America 25Magali Garcia, Bruno Condori, andCarmen Del Castillo

Introduction 25Andean Domestication 26Botanical and Taxonomical Description 27Genetic Background and Research on

Quinoa Genetics 28Ecology and Phytogeography 30Cultivation and Agronomic Practices

in South America 30Quinoa Production 31

Soil conditions 31Climate 32

Drought resistance 32Temperature and photoperiod 33Hail 34

Cultivation 34Sowing 34Fertilization of quinoa 36Cultural practices 37Crop water requirements and

irrigation 37Biotic threats: pests and diseases 38Seed harvest and postharvest

technology 39References 41

v

vi Contents

4 Trends in Quinoa Yield over theSouthern Bolivian Altiplano:Lessons from Climate andLand-Use Projections 47Serge Rambal, Jean-Pierre Ratte,Florent Mouillot, and Thierry Winkel

Summary 47Introduction 48Materials and Methods 49

The study area 49Recent past and present climate 49Source of climate scenarios 50Simulating the yield index at local

or plot scale 50The soil water balance model 50Scenarios of land-use/land-cover

changes 51Scaling local yield index up to the region 51

Results 52Drought history over the area 52Climate projections and soil drought

limitation 52Time variation of yield at local or

plot scale 54Model results at landscape level 56

Discussion 57Acknowledgments 60References 60

5 The Potential of Using NaturalEnemies and ChemicalCompounds in Quinoa forBiological Control of InsectPests 63Mariana Valoy, Carmen Reguilón,and Griselda Podazza

Introduction 63Insects in Quinoa 64

Insect pests of quinoa 65Beneficial insects in quinoa 65Chemical responses of quinoa

to insect herbivory 72Quinoa secondary metabolites 74

Potential of Biological Control in Quinoa 76

Potential for Ecological Management ofQuinoa 77

References 80

6 Quinoa Breeding 87Luz Gomez-Pando

History – Domestication Process 87Collection of Genetic Resources 88Goals and Methods of Quinoa Breeding 92

Requirement of the farmers 92Requirements of the industry and

consumers 95Methods in genetic improvement 96

Quinoa Breeding Methods 98Selection 98Participatory plant breeding (PPB) 98Introduction of foreign germplasm 99Hybridization 99Interspecific and intergeneric crosses 102Backcross method 102Using heterosis in quinoa 102Mutagenesis 103Marker-assisted selection (MAS) 103

Conclusion 103References 103

7 Quinoa Cytogenetics, MolecularGenetics, and Diversity 109Janet B. Matanguihan, Peter J.Maughan, Eric N. Jellen, and BozenaKolano

Introduction 109Cytogenetics and Genome Structure of

Chenopodium Quinoa 109Crossability of Quinoa and Allied

Tetraploid Taxa 111DNA Sequence Evidence for Quinoa’s

Genomic Origins 112Quinoa Genetic Markers and Linkage

Maps 113Quinoa Diversity 115

Phenotypic diversity 115Genetic diversity 117

Summary 118References 120

Contents vii

8 Ex Situ Conservation of Quinoa:The Bolivian Experience 125Wilfredo Rojas and Milton Pinto

Introduction 125Centers of Origin and Diversity

of Quinoa 126Geographical Distribution of Quinoa 127Genebanks of the Andean Region 128Bolivian Collection of Quinoa

Germplasm 130History and management of the

quinoa germplasm 130Current status of quinoa germplasm 132

Steps for Ex Situ Management andConservation of Quinoa 132Collection of quinoa germplasm 133Technical procedure for quinoa

germplasm collection 133History and evolution of quinoa

germplasm collections 134Distribution of quinoa germplasm

collection 136Preliminary multiplication of quinoa

germplasm 136Storage and conservation of quinoa

germplasm 138Short- and medium-term storage

(1 to 20 years) 138Long-term storage (80 to 100 years) 138Characterization and evaluation

of the quinoa germplasm 140Stages of germplasm characterization

and evaluation 140Agromorphological variables 141Agro-food and nutritional value

variables 143Molecular characterization 144Multiplication and regeneration

of quinoa germplasm 144Monitoring of seed quantity and

percentage of seedgermination 145

Technical procedure for multiplicationand/or regeneration 145

Regeneration schedule 146Documentation and information

on quinoa germplasm 147

Utilization of quinoa germplasm 148Conclusions 155References 158

9 Quinoa Breeding in Africa:History, Goals, and Progress 161Moses F.A. Maliro and Veronica Guwela

Introduction 161Origin of quinoa 161Introducing quinoa in Africa 161Ecological adaptation of quinoa 163

Goals of Quinoa Breeding in Africa 164Quinoa studies under Malawi

conditions 164Quinoa studies in Kenya 166

Challenges and Considerations forFuture Research 169Plant lodging 169Acceptability 169Agronomic practices 170Rain-fed versus irrigated cropping

systems 170Conclusion 170References 170

10 Quinoa Cultivation forTemperate North America:Considerations and Areasfor Investigation 173Adam J. Peterson and Kevin M. Murphy

Introduction 173Tolerance to Abiotic Stresses 173

Heat tolerance 173Drought tolerance 174Cold tolerance 175Salinity tolerance 176

Production Aspects 177Variety selection 177Fertilization 178Planting/spacing 179Maturity and harvesting 181

Challenges to Quinoa Production 182Waterlogging and preharvest sprouting 182Disease 183Insect pests 184

viii Contents

Weed control 185Saponins 186

Alternative Uses of Quinoa 186Forage 186Feed 187

Conclusion 187Acknowledgments 188References 188

11 Nutritional Properties of Quinoa 193Geyang Wu

Introduction 193Protein 193Carbohydrates 196

Starch 196Sugar 198Dietary fiber 198

Lipids 199Vitamins 200Minerals 201Anti-Nutritional Factors of Quinoa 202Bioactive Compounds 204

Phenolic compounds 204Phenolic acid 204Flavonoids 204Carotenoids 205

Summary 205References 205

12 Quinoa’s Calling 211Sergio Núnez de Arco

Introduction 211A Snapshot of the Economics of a

Smallholder Farmer in Bolivia andthe International Market 212

The Quinoa Market: Supply andDemand 213

Bolivia, Peru, and Ecuadorincrease quinoa acreage 213

Evolution of quinoa,(Figs. 12.7–12.10and Fig. 12.3) acreage inBolivia 213

The US quinoa market and evolutionof prices 215

Quinoa in the eye of a market storm 215The quinoa grower rises out

of poverty 217Current Production Practices, Increased

Acreage, and Thoughts onSustainability 221

Living Well, Reversed Migration, andCultural Identity 224

Opportunities for the Bolivian Farmer 225

Index 227

List of Contributors

Sergio Núñez de ArcoAndean Naturals, Inc.,Foster City, CA, USA

Didier BazileUPR47, GREEN, Centre de CoopérationInternationale en Recherche Agronomiquepour le DéveloppementCampus International de BaillarguetMontpellier, France

Carmen Del CastilloFaculty of AgronomyUniversidad Mayor de San AndresLa Paz, Bolivia

Bruno CondoriConsultative Group on InternationalAgricultural Research – International PotatoCenter, La Paz, Bolivia

Sayed S.S. EisaAgricultural Botany Department, Faculty ofAgriculture, Ain Shams University, Cairo, Egypt

Francisco F. FuentesFacultad de Agronomía e Ingeniería Forestal,Pontificia Universidad Católica de Chile, Casilla306–22, Santiago, Chile

Magali GarciaFaculty of Agronomy,Universidad Mayor de San AndresLa Paz, Bolivia

Juan Antonio GonzálezInstituto de Ecologia – Area de BotánicaFundación Miguel Lillo TucumánTucumán, Argentina

Veronica GuwelaInternational Crops Research Institute for theSemi-Arid Tropics, Lilongwe, Malawi

Sayed Abd Elmonim Sayed HussinAgricultural Botany Department, Faculty ofAgriculture, Ain Shams UniversityCairo, Egypt

Eric N. JellenPlant and Wildlife SciencesBrigham Young UniversityProvo, UT, USA

Bozena KolanoDepartment of Plant Anatomy and CytologyUniversity of Silesia, Poland

Moses F.A. MaliroDepartment of Crop and Soil Sciences, BundaCollege Campus, Lilongwe University ofAgriculture and Natural ResourcesLilongwe, Malawi

Enrique A. MartínezCentro de Estudios Avanzados en Zonas ÁridasLa Serena and Facultad de Ciencias del MarUniversidad Católica del NorteCoquimbo, Chile

ix

x List of Contributors

Janet B. MatanguihanDepartment of Crop and Soil SciencesWashington State UniversityPullman, WA, USA

Peter J. MaughanPlant and Wildlife SciencesBrigham Young UniversityProvo, UT, USA

Florent MouillotIRD, UMR 5175 CEFEMontpellier, France

Kevin M. MurphyDepartment of Crop and Soil SciencesWashington State UniversityPullman, WA, USA

Luz Gomez-PandoUniversidad Nacional Agraria La MolinaAgronomy FacultyLima, Peru

Adam J. PetersonDepartment of Crop and Soil SciencesWashington State UniversityPullman, WA, USA

Milton PintoPROINPA Foundation538 Americo Vespucio St., P.O. Box 1078,La Paz, Bolivia

Griselda PodazzaInstituto de Ecología, Fundación Miguel LilloTucumán, Argentina

Fernando Eduardo PradoFacultad de Ciencias Naturales e IMLFisiología VegetalTucumán, Argentina

Serge RambalCNRS, UMR 5175 CEFEMontpellier, FranceDepartamento de BiologiaUniversidade Federal de LavrasLavras, MG, Brazil

Jean-Pierre RatteCNRS, UMR 5175 CEFEMontpellier, France

Carmen ReguilónInstituto de Entomología, Fundación MiguelLillo Tucumán, Argentina

Wilfredo RojasPROINPA FoundationAv. Elias Meneces km 4El Paso, Cochabamba, Bolivia

Mariana ValoyInstituto de Ecología, Fundación Miguel LilloTucumán, Argentina

Thierry WinkelIRD, UMR 5175 CEFEMontpellier, France

Geyang WuSchool of Food ScienceWashington State UniversityPullman, WA, USA

Preface

The seeds of this book took root in the summerof 2010, during the first year of our multilocationquinoa trials across three major climatic regionsof Washington State. We began growing andevaluating quinoa thanks to generous fundingfrom the Organic Farming Research Foundation,and growers around the state looked on with keeninterest. In that first year we tested 44 varieties ofquinoa sourced from almost as many diverse geo-graphical locations and we were mildly surprisedwhen only 12 of these actually produced seed inour northern latitude. That first year we wereintroduced to many of the ongoing challenges wecontinue to face 5 years later, including suscepti-bility to preharvest sprouting and downy mildew,photoperiod insensitivity, pollen sterilizationresulting from high summer temperatures withlittle to no rainfall or supplemental irrigation,and the negative effects of aphid and lyguspredation. We quickly realized that if quinoa wereto become a successfully grown crop in the PacificNorthwest region of the United States, it wouldrequire a concerted effort of a transdisciplinarycadre of scientists with a range of expertise,a forward-thinking and risk-taking group ofinnovative farmers, and a strong supporting castof distributors, processors, and consumers. Fromthat first year, with only one junior faculty and oneundergraduate research intern collaborating withthree farmers, the quinoa group at WashingtonState University has grown into diverse team ofover 10 faculty and 10 graduate students, eachaddressing a key component of quinoa breeding,agronomy, sociology, entomology, or food science.This book is intended to lay the groundwork forthe latest quinoa research worldwide and to assistfaculty and students new to the crop to gain a

foothold of understanding into quinoa genomicsand breeding, global agronomy and production,and marketing.

In August 2013, Washington State Univer-sity hosted the International Quinoa ResearchSymposium (IQRS). One hundred and sixtyenthusiastic participants from 24 countriesdescended on Pullman, Washington and sharedknowledge, questions, obstacles, observations,and ideas on the path forward during an intense,vibrant and thought-provoking 3 days of talks,field visits, poster sessions, and quinoa vodkainfused social exploration. Many of the co-authorsof the various chapters in this book were atten-dees and/or presenters at the IQRS, and thesymposium provided a safe forum for the opendiscussion of ideas that have found their way intothe chapters of this book. Symposium attendeeswho have contributed to this book include DidierBazille, Juan Antonio Gonzalez, Luz GomezPando, Rick Jellen, Moses Maliro, EnriqueMartinez (in absentia), Jeff Maughan, SergioNúñez de Arco, Adam Peterson, Wilfredo Rojas,Geyang Wu, and co-editors Janet Matanguihanand Kevin Murphy.

Keynote speakers at the IQRS includedSven-Erik Jacobsen, renowned quinoa researcherfrom University of Copenhagen, Tania San-tivanez from the United Nations Food andAgriculture Organization, and John McCamant,a long-time quinoa farmer and researcher fromWhite Mountain Farms in Colorado, USA. Otheresteemed presenters not mentioned includedDaniel Bertero from the University of BuenosAires, Argentina, Morgan Gardner of WashingtonState University, Frank Morton of Wild GardenSeeds in Oregon, and Hassan Munir of the

xi

xii Preface

University of Agriculture Faisalabad, Pakistan,as well as numerous poster presentations. Finally,the highlight of the symposium for many atten-dees was the eloquent thoughts delivered by agroup of five Bolivian farmers, who traveled tothe United States for the first time to join in theinternational discussion on the many social andpolitical aspects of quinoa cultivation.

This book reflects the many presentations anddiscussions that took place at the IQRS, and isintended to provide the reader with a compre-hensive base knowledge of the current body ofknowledge of the ever-expanding, global scientificresearch of quinoa. In Chapter 1, Gonzalez et al.provide a solid overview of quinoa as an Incancrop, primarily in Peru and Bolivia, now facing adiversity of global challenges. Chapter 2 followsup on this introduction by discussing the origin,domestication, diversification, and cultivation ofquinoa from a Chilean perspective.

Chapter 3 by Garcia et al. encapsulates many ofthe wide-ranging agronomic and agroecologicalcultural practices of quinoa throughout the majorgrowing regions of South America as a whole.This broad chapter provides a botanical andtaxonomical description of quinoa, ecology andphytogeography of quinoa, and many tangibleproduction practices across a wide range ofclimates, soils, and growing conditions that canbe emulated in nontraditional growing regionsaround the world. Rambal et al. follow this witha description of the historical trends in quinoayield in the southern Bolivian altiplano, includingimportant lessons from climate and land-use pro-jections in Chapter 4. Valoy et al. then discuss inChapter 5 the potential of using natural enemiesand chemical compounds in quinoa for biologicalcontrol of pests. This chapter follows up on theagroecological themes discussed in Chapter 3, andcompiles and elucidates a vast array of knowledgegained through previous research in this realmof quinoa science, and provides the thoughtfulreader many potential ideas for new research inthis direction.

In Chapter 6, Peruvian plant breederGomez-Pando describes the historical andmodern context of quinoa breeding in the Andeanregions. Beginning with the effect of farmer

selection on seed color, dormancy, seed sizeand seed coat thickness, salt and drought toler-ance, and adaptation to multiple and countlessmicroclimates, Gomez-Pando then moves on tohighlight the rise of modern quinoa breedingin the 1960s, the collection of quinoa geneticresources and in situ conservation, and the goalsand methodology employed by current quinoabreeders.

Matanguihan et al. follow this with an in-depthdiscussion on the cytogenetics, genomic structure,and diversity of quinoa in Chapter 7. Informa-tion on close genetic relatives of Chenopodiumquinoa are discussed, along with DNA-basedmolecular genetic tools and linkage maps whichcan facilitate and accelerate the transfer of exoticgenes into C. quinoa. Also included in Chapter 7is a review of phenotypic and genetic diversitystudies which show that the genetic variability ofquinoa has a spatial structure and distribution.The congruence between genetic differentiationand ecogeography suggests that quinoa all overthe southern Andes may be undergoing similarprocesses of genetic differentiation. Not surpris-ingly, human activities, specifically seed exchangeroutes, have significantly affected the geneticstructure of quinoa.

In Chapter 8, Rojas and Pinto discuss theex-situ conservation of quinoa genetic resourcesfrom a Bolivian perspective. According to Rojasand Pinto, the Bolivian quinoa germplasm col-lection has the greatest diversity in the world,and this diversity represents the cultural impor-tance of quinoa in Bolivian customs, indigenousconsumption, and production. Chapter 8 alsoprovides insight into the center of origin anddiversity of quinoa, the geographical distributionof quinoa, and steps needed for the ex situmanagement and conservation of quinoa.

Chapters 9 and 10 discuss quinoa cultivation ntwo continents, Africa and North America, thatare considered nontraditional quinoa productionenvironments. In Chapter 9, Maliro and Guweladescribe the necessity of stabilizing food securityand alleviating malnutrition in Africa, and thepotential for quinoa as a novel crop to make apositive contribution to these efforts. The goals ofquinoa breeding in Africa and information from

Preface xiii

recent quinoa trials in Malawi and Kenya arediscussed in an effort to address the challengesand considerations for future quinoa researchin Africa. Key among these considerations isthe acceptability of quinoa into African diets.In Chapter 10, Peterson and Murphy discussquinoa introduction to the United States as a cropapproximately 30 years ago, and the key breeding,research, and production events in the timeperiod after its introduction. Recent research atWashington State University is highlighted inthis chapter.

In Chapter 11, Wu describes the nutritionalproperties of quinoa that have played an impor-tant role in bringing the crop to worldwideattention. Finally, in a refreshing departure fromthe scientific writing in the previous chapters,Nuñez de Arco provides an insider’s view into themarketing of quinoa in Chapter 12. Of particularinterest are the personal descriptions and snap-shots of the lives of smallholder farmers, of whichan estimated 35,000 produce quinoa in Bolivia,who discuss their philosophy of marketing quinoa

under the current fluctuations in the supply anddemand of this increasingly popular crop.

This book is a reflection of the increasingimportance of quinoa in the global market. Theroster of contributors – from South America,Europe, Africa and North America – also reflectsthe expansion of quinoa from its origins to newproduction areas in the world. It was a pleasureto work with colleagues from countries who havegrown quinoa for centuries, and with colleaguesfrom countries which are growing quinoa for thefirst time. We are indebted to these authors fortheir willingness to share their expertise and fortheir cooperation in the process of shaping thisbook. It is our hope that this book will contributeto quinoa knowledge to benefit growers, students,researchers, and professionals from universitiesand institutes involved in the improvement ofquinoa and its sustainable production.

Kevin M. MurphyJanet B. Matanguihan

Chapter 1

Quinoa: An Incan Crop to Face GlobalChanges in Agriculture

Juan Antonio González1, Sayed S. S. Eisa2, Sayed A. E. S. Hussin2,

and Fernando Eduardo Prado3

1Instituto de Ecologia – Area de Botánica, Fundación Miguel Lillo, Tucumán, Argentina2Agricultural Botany Department, Faculty of Agriculture, Ain Shams University (ASU), Cairo, Egypt3Facultad de Ciencias Naturales e IML, Fisiología Vegetal, Miguel Lillo 205, 4000 Tucumán, Argentina

INTRODUCTION

Environmental changes have always occurred inthe past but in the last decades these have escalatedto critical levels, presenting environmental riskto people, especially in terms of food supply, as itaffects crop yield, production, and quality. Rapidpopulation growth leads to increase in demandfor land and thus to accelerated degradation anddestruction of the environment (Alexandratos2005; IPCC 2007). Probably the most importantchange driven by human activity is the increasingaccumulation of greenhouse gases such as carbondioxide (CO2), among others (Wallington et al.2004; Montzka et al. 2011). Greenhouse gasescan absorb and emit infrared radiation, and thus aglobal earth warming occurs, otherwise known asthe greenhouse effect. Many scientists agree thateven a small increase in the global temperaturewould lead to significant climate and weatherchanges, affecting cloud cover, precipitation, windpatterns, the frequency and severity of storms,and the duration of seasons (Solomon et al. 2009).This scenario will lead to scarce natural resourcesand the reduction of food production.

Quinoa: Improvement and Sustainable Production, First Edition. Edited by Kevin Murphy and Janet Matanguihan.© 2015 John Wiley & Sons, Inc. Published 2015 by John Wiley & Sons, Inc.

The net consequences of global warming oncrop physiology and yield are not yet fully under-stood, but there are some evidences indicatingthat decrease in yield may be the main response(Parry et al. 2005). Another deleterious effectof global warming is the increase in diseases,especially those caused by fungi and bacteria, asa consequence of higher humidity (Chakrabortyet al. 2000; Hunter 2001). As most crops world-wide are well adapted to previous weatherconditions, many of these crops will becomeless productive and may even disappear in afuture of increasing climate change. It is thereforenecessary to explore plant species as alternativecrops or develop new crops to grow underthese changing weather patterns. In this sense,it is very important to take into account plantspecies that grow in different altitudinal levelsor those that have thrived in mountain regionsfor millennia. Mountain plants, especially thoseadapted and cultivated in different altitudinallevels, may be very important because of thegenetic richness that enabled those adaptations.

Quinoa (Chenopodium quinoa Willd.), a nativegrain to the Andean highlands in South America,could be an excellent alternative crop in manyregions of the world. Quinoa has been grown

1

2 Quinoa: Improvement and Sustainable Production

in the Andes about 5,000–7,000 years ago andhas been cultivated in different ecological zonesfrom sea level in the northwest region of Chile toaltitudes over 4,000 m above sea level (masl) in theBolivian Altiplano (Fuentes et al. 2009). Owingto this plasticity, quinoa has been introduced tohigher latitudes as a new or alternative crop, withreports indicating an acceptable adaptation ofthis species in the United States, Canada, andEurope (Johnson and Ward 1993; Jacobsen 1997)and recently in Morocco (Jellen et al. 2005), India(Bhargava et al. 2006, 2007), and Italy (Pulventoet al. 2010).

A BRIEF HISTORY OF QUINOACULTIVATION

Archeological studies provide evidence on theconsumption of quinoa as human food thousandsof years before the first Spanish conquerorsarrived in America. Uhle (1919), taking intoaccount evidences from Ayacucho (Perú), saidthat quinoa domestication began almost 5,000years BC. According to Nuñez (1974), quinoa wasutilized in the north region of Chile at least 3,000years BC. Many chronicles and archeologicalstudies provide evidence that quinoa was usedby indigenous people for centuries in Colombia,Ecuador, Perú, Bolivia, Chile, and the Argen-tinean northwest. During pre-Columbian times,quinoa seed served as a staple food in the Incandiet, leading the Incas to call it the “mothergrain” and considered it as a gift of the sun god,“Inti.” It is believed that the Incas consideredquinoa to be a sacred plant. Religious festivalsincluding an offering of quinoa in a fountain ofgold to the Inti god were held. The Inca Emperorused a special gold tool to make the first furrowof each year’s quinoa planting. In Cuzco, ancientIncas worshipped entombed quinoa seeds asthe progenitors of the city. The first Spanishconqueror who mentioned quinoa was Pedrode Valdivia. In 1551, he wrote to Carlos I, theSpanish Emperor, about the presence of somecrops in the neighboring area of Concepción,Chile and specifically mentioned “…maize,potatoes and quinuas… ” (Tapia 2009). On the

other hand, in the Comentarios Reales de los Incas,a book written by Inca Garcilaso de la Vega andpublished in 1609 in Lisbon, Portugal, Garcilasomentioned “quinoa” as one of the first crops inthe Inca Empire (de la Vega 1966). Garcilasomentioned that there was an intent to exportquinoa to Spain but the seeds were nonviable.Other authors had also mentioned the existenceof quinoa in Pasto and Quito, Ecuador (Cieza deLeón 1560), in Collaguas, Bolivia (Ulloa Mogol-lón 1586), Chiloé island in Chile (Cortés Hogea1558), and in the Argentinean Northwest andCordoba province, Argentina (de Sotelo 1583).During the Spanish conquest of South Americain the sixteenth century, quinoa was scornedas a “food for Indians” and the conquerorsdestroyed fields of quinoa, actively suppressing its“non-Christian” production and consumption.The Incan peoples under the yoke of Spanishoppression were forbidden to grow it on painof death and were forced to grow corn instead.According to Tapia (2009), after the Spanishconquest, the quinoa crop was preserved byAndean peoples in “aynokas” (communal lands)for centuries. This cropping practice also allowedthe conservation of quinoa germplasm in situ(Tapia 2009). Today, quinoa is cultivated in morethan 50 countries beyond the Andes. As a result,the cloud of ambiguity that has enveloped thiscrop for more than four centuries is beginning todisappear (National Research Council 1989).

NUTRITIONAL VALUE OF QUINOA SEED

There is extensive literature on the chemicalcomposition of quinoa seed (González et al. 1989;Ando et al. 2002; Repo-Carrasco et al. 2003; Abu-goch 2009), which cover all nutritional aspectssuch as chemical characterization of proteins(Brinegar and Goundan 1993; Hevia et al. 2001),fatty acid composition of the seed oil (Wood et al.1993; Ando et al. 2002), mineral content (Koziol1992; Konishi et al. 2004; Prado et al. 2010), andnutritional value (Prakash et al. 1993; Ranhotraet al. 1993; Ruales and Nair 1992).

The lipid content of quinoa seed is higher thanthat in common cereals (Repo-Carrasco-Valencia

Quinoa: An Incan Crop to Face Global Changes in Agriculture 3

2011) and is mainly located in the embryo. Theoil of quinoa seed is rich in polyunsaturated fattyacids (linoleic and linolenic) and in oleic acid.Its level of unsaturated fatty acids in relation tohuman nutrition is better than those in othercereals (Alvarez-Jubete et al. 2009). According tothe Food and Agricultural Organization (FAO)recommendations on fats and fatty acids in humannutrition (FAO/WHO 2010), infant food shouldcontain 3–4.5% energy in the form of linoleicacid (LA) and 0.4–0.6% in the form of linolenicacid (ALA), which corresponds to LA/ALAratio (n-6/n-3 ratio) between 5 (minimum) and11.2 (maximum). The LA/ALA ratio of quinoaoil is 6.2 (Alvarez-Jubete et al. 2009) and thusfalls within the FAO/WHO (2010) recommendedvalues. Furthermore, a diet with a high n-6/n-3ratio promotes the pathogenesis of many degen-erative diseases such as cardiovascular disease,cancer, osteoporosis, as well as inflammatory andautoimmune diseases (Simopoulos 2001). Themain carbohydrate in quinoa seed is the starchwhere soluble sugars, that is, sucrose, glucose,and fructose are present at low levels (Gonzálezet al. 1989). Quinoa starch is located mainly inthe perisperm and it occurs both as small indi-vidual granules and larger compound granulescomposed of hundreds of individual granules(Prado et al. 1996). The individual granules arepolygonal with a diameter of 1.0–2.5 μm and thecompound granules are oval, with a diameter of6.4–32 μm (Atwell et al. 1983). Quinoa starch isrich in amylopectin and gelatinizes at relativelylow temperatures (57–71∘C). Moreover, it hasexcellent freeze-thaw stability attributed to itsrich amylopectin content (Ahamed et al. 1996).In comparison with common cereals, quinoa isan excellent source of γ-tocopherol (vitamin E),containing about 5 mg/100 g DM (Ruales andNair 1993). The content of γ-tocopherol is of par-ticular biological relevance because of its potentialanticarcinogenic and anti-inflammatory activities(Jiang et al. 2001). Quinoa also contains significantamounts of riboflavin, thiamine, and, especially,vitamin C that is uncommon in cereals (Koziol1992; Ruales and Nair 1993; Repo-Carrasco et al.2003). Recently, it has been demonstrated thatquinoa seed also contains high levels of folate

(Schoenlechner et al. 2010). The folate contentfound in quinoa is 132.7 mg/100 g DM, about10-fold higher than that in wheat seed. Quinoabran contains a higher amount of folate thanflour fraction (Repo-Carrasco-Valencia 2011).Furthermore, quinoa seed does not contain aller-genic compounds such as gluten or prolamine orenzyme (protease and amylase) inhibitors presentin most common cereals (Zuidmeer et al. 2008)or trypsin and chymotrypsin inhibitors present insoybean seeds (Galvez Ranilla et al. 2009).

Despite its healthy nutritional composi-tion, several cultivars of quinoa contain bittersaponins, glycosylated secondary metabolitesin the seed coat that act as antinutrients anddeterrents of seed predators such as birds andinsects (Solíz-Guerrero et al. 2002). Saponinsare concentrated in external layers of the seed(Prado et al. 1996) and include a complex mixtureof triterpene glycosides that are derivatives ofoleanolic acid, hederagenin, phytolaccagenicacid, serjanic acid, and 3β,23,30-trihydroxyolean-12-en-28-oic acid, which bear hydroxyl andcarboxylate groups at C-3 and C-28, respectively(Kuljanabhagavad et al. 2008). Presently, at least16 different saponins have been detected inquinoa seeds (Woldemichael and Wink 2001).Saponins are reported to be toxic for cold-bloodedanimals and have been used as fish poison bySouth American inhabitants (Zhu et al. 2002).They have some adverse physiological effects,as they are membranolytic against cells of thesmall intestine and possess hemolytic activity(Woldemichael and Wink 2001). Moreover,saponins form complexes with iron and mayreduce its absorption.

Although saponins have negative effects, theyalso have positive effects such as reducing serumcholesterol levels, possessing anti-inflammatory,antitumor, and antioxidant activities, andenhancing drug absorption through the mucosalmembrane. Saponins also exhibit insecticidal,antibiotic, antiviral, and fungicidal properties(Kuljanabhagavad and Wink 2009). Furthermore,saponins act as immunological and absorptionadjuvant to enhance antigen-specific antibodyand mucosal response (Estrada et al. 1998).


Saponin content varies among genotypes,ranging between 0.2 and 0.4 g/kg DM (sweetgenotypes) and 4.7 and 11.3 g/kg DM (bit-ter genotypes). Therefore, selection of sweetgenotypes with very low saponin content inthe seeds is one of the main breeding goals inquinoa. However, selection for sweet genotypesis retarded by cross-pollination (Mastebroeket al. 2000). The tissue containing saponins is ofmaternal origin, and the saponin content of theseed reflects the genotype of the plant from whichthe grain is harvested (Ward 2001). Accordingto Gandarillas (1979), the saponin content traitis controlled by two alleles at a single locus,with the bitter allele (high saponin) dominantto the sweet allele (low saponin). More recently,researchers have observed that saponin content inquinoa seed is a continuously distributed variableand is therefore more likely to be polygenicallycontrolled and quantitatively inherited (Galweyet al. 1990; Jacobsen et al. 1996).

Quinoa seeds must be freed of seed coatsaponins before consumption. Saponins canbe easily eliminated by water washing or abra-sive dehulling. There was no difference in theremoval of saponins observed between the twomethods (Ridout et al. 1991), although the lattermethod has the advantage of not generatingwastewater. However, some nutrients can be lostwhen the abrasive dehulling method is used(Repo-Carrasco-Valencia 2011).

Among the nutritional attributes of quinoaseed, prominent is its high-quality protein thatis gluten-free and has an exceptional amino acidbalance. The presence of essential amino acidssuch as methionine, threonine, lysine, and trypto-phan are very important because they are limitingamino acids in most cereal grains (Gorinsteinet al. 2002). The high level of tryptophan foundin the seed of the Bolivian cultivar “Sajama” isnoteworthy (Comai et al. 2007). Protein quality isdetermined by its biological value (BV), which isan indicator of protein intake by relating nitrogenuptake to nitrogen excretion. The highest valuesof BV correspond to whole egg (93.7%) and cowmilk (84.5%) (Friedman 1996). The protein ofquinoa seed has a BV of 83%, which is higherthan that of fish (76%), beef (74.3%), soybean

(72.8%), wheat (64%), rice (64%), and corn(60%) protein (Abugoch 2009).

According to the FAO/WHO nutritionalrequirements for 10- to 12-year-old children,quinoa protein possesses adequate levels ofphenylalanine, tyrosine, histidine, isoleucine,threonine, and valine (FAO/WHO 1990). Con-sequently, there is no need to combine quinoaseed with other protein sources to supply humanrequirements for essential amino acids. Thisnutritional aspect of quinoa is very significant as itcan provide a new protein source for a good diet.Quinoa may also be an important alternative cropfor mountainous regions of the world, where manypeople live. In these regions, there are severe con-straints in obtaining good quality food and quinoawill be able to supply the nutrient requirementsthat other crops cannot, especially for children.

The nutritional composition of quinoa seed isdetermined by both the genotype and the envi-ronment. The metabolism of nitrogen-containingcompounds, that is, proteins and amino acids, maybe strongly affected by environmental conditions(Triboi et al. 2003). In a recent ecophysiologicalstudy carried out on 10 quinoa cultivars from theBolivian highland region (Patacamaya site, 3,600masl) and northwest Argentinean lowland region(Encalilla site, 2,000 masl), González et al. (2011)demonstrated that in six cultivars (Amilda, Kan-colla, Chucapaka, Ratuqui, Robura, and Sayaña)the protein content showed an increment in thelowland growing site when compared with seedsfrom the highland site. In contrast, four cultivars(CICA, Kamiri, Sajama, and Samaranti) showeda decreased content (Table 1.1). Similarly, it hasalso been demonstrated that both the content andthe composition of quinoa saponins are affectedby environmental conditions. Both droughtand salinity decreased the content and profile ofsaponins of quinoa cultivars (Solíz-Guerrero et al.2002; Dini et al. 2005; Gómez-Caravaca et al.2012). In effect, many metabolic and physiologicalaspects of crops are affected by agroecologicalconditions (Triboi et al. 2003). Soil type andclimatic conditions also play a crucial role in thesuccess of crops. These are important results andshould be taken into account when choosing acommercial cultivar.


Table 1.1 Protein content (g/100 g DW) of quinoa seeds cultivated in twoagroecological sites (Patacamaya, 3,600 masl and Encalilla, 2,000 masl).

Patacamaya Encalilla

Cultivar (g/100 g DW)Difference

(%)

Amilda 11.41 12.5 8.7Kancolla 14.44 15.17 4.8Chucapaka 11.67 14.34 18.6CICA 15.46 13.46 −14.9Kamiri 13.98 13.12 −6.6Ratuqui 10.38 15.53 33.2Robura 9.62 10.43 7.8Sajama 12 9.15 −31.1Samaranti 12.26 9.34 −31.3Sayaña 11.36 13.85 18.0

Quinoa may be considered as a potentialalternative crop in many regions of the worlddue to the nutritional quality of its seed and itsgood potential for adaptation (González et al.1989, 2012; Dini et al. 2005; Comai et al. 2007;Thanapornpoonpong et al. 2008). Probably allthese aspects were taken into account by theFAO when it included quinoa in the list of mostpromising crops for world food security andhuman nutrition in the twenty-first century (FAO2006). The National Aeronautics and SpaceAdministration (NASA) also included quinoawithin the Controlled Ecological Life SupportSystem (CELSS) to augment the inadequateprotein intake of astronauts in long-durationspace travel (Schlick and Bubnehiem 1993).

BOTANICAL AND GENETICCHARACTERISTICS OF THE QUINOAPLANT

Quinoa is an annual Amaranthaceae. This Andeangrain is an important crop of the Andean regionin South America from Colombia (2∘N) to centralChile (40∘S) (Risi and Galwey 1984; Jacobsen2003). Despite its wide latitudinal distribution,quinoa also has a broad altitudinal distribution.Quinoa may be cultivated at sea level, middlemountain (between 2,000 and 3,000 masl), andhigh mountain (above 3,000 masl). In relationto this altitudinal and latitudinal distribution

pattern, Tapia (2009) distinguished at least fiveecotypes of quinoa: (i) Valley quinoa, which arelate-ripening, with plant heights 150–200 cm ormore, and growing at 2,000 and 3,000 masl; (ii)Altiplano quinoa, which can withstand severefrost and low precipitation, growing aroundTiticaca Lake in Bolivia and Perú; (iii) Salarquinoa, which can tolerate salty soils with highpH values, growing on the plains of the BolivianAltiplano such as Uyuni and Coipasa; (iv) Sealevel quinoa, generally small plants (near 100 cm)with a few stems and bitter grains, found in thesouth of Chile; and (v) Subtropical quinoa, whichhave small white or yellow grains, growing in theinter-Andean valleys of Bolivia. Royal Quinoa(Quinoa Real) is probably the most recognizedquinoa cultivar in the international market. It isa bitter variety and is only produced in Bolivia,particularly in the districts of Oruro and Potosí,around the salt flats of Uyuni and Coipasa. Themicroclimatic conditions and physicochemicalproperties of the soil offer the appropriate habitatfor the production of this type of quinoa (Rojaset al. 2010). Morphophenological characteristicsof quinoa show that there is a huge diversity invarieties or local ecotypes (del Castillo et al. 2007).Therefore, available commercial quinoas exhibitwide genetic diversity, showing great variability inplant color, inflorescence and seeds, inflorescencetype, protein, saponin and betacyanine contents,and calcium oxalate crystals in leaves. Thisextreme variability may reflect wide adaptation to


different agroecological conditions such as soil,rainfall, nutrients, temperature, altitude, drought,salinity, and UV-B radiation.

Quinoa is a dicotyledonous annual herba-ceous plant usually erect, with a height of about100–300 cm, depending on environmental con-ditions and genotype. Leaves are generally lobed,pubescent, powdery, rarely smooth, and alterna-tively inserted on a woody central stem. The plantmay be branched or unbranched, depending onvariety and sowing density. Stem color may begreen, red, or purple. The leafy flower cluster(a panicle with groups of flowers in glomerulus)arises predominantly from the top of the plantand may also arise from the leaf junction (axil) onthe stem. Flowers are sessile, of the same color asthe sepals, and may be hermaphrodite, pistillate,or male sterile. The stamens have short filamentsbearing basifixed anthers; the style has two orthree feathery stigma. The fruit occurs in anindehiscent achene, protected by the perigonium.The seeds are usually somewhat flat, measure1–2.6 mm, and approximately 250–500 seedscomprise 1 g. The seeds also exhibit a great varietyof colors – white, yellow, red, purple, brown, andblack, among others. Seed embryo can be up to60% of the seed weight and forms a ring aroundthe endosperm. The taproot (20–50 cm long) isprofusely branched and forms a dense web ofrootlets that penetrate to about the same depthas the plant height (National Research Council1989).

The vegetative period of quinoa is related tophotoperiod sensitivity and varies between 120and 240 days. Some varieties, such as CO-407from Chile, have a vegetative period between110 and 120 days, but others, such as the CICAvariety, have more than 200 days. On the otherhand, C. quinoa is a C3 species confirmed byanatomical studies and carbon isotope discrim-ination (González et al. 2011). The δ13C valuesof leaves of 10 varieties of quinoa ranged from aminimum of −27.3‰ to a maximum of −25.2‰(Table 1.2). Typical values of δ13C in C3 speciescan ranges from −35 to −20‰ (Ehleringer andOsmond 1989).

C. quinoa is an allotetraploid (2n= 4x= 36) andexhibits disomic inheritance for most qualitative

Table 1.2 Carbon isotope composition δ13C of 10varieties of quinoa.

Cultivar δ13C

Amilda −25.6Chucapaca −26.3CICA −26.6Kancolla −27.3Kamiri −26.7Ratuqui −26.4Sayaña −26.3Robura −25.7Sajama −25.2Samaranti −25.6

traits (Simmonds 1971; Risi and Galwey 1989;Ward 2001; Maughan et al. 2004). The speciesclosest to cultivated quinoa are Chenopodiumhircinum and Chenopodium berlandieri, whosebasic chromosome number (2n= 4x= 36) isthe same as that of the cultivated types, andChenopodium petiolare and Chenopodium pallidi-caule, which have 2n= 2x= 18 chromosomes(Fuentes et al. 2009). Quinoa species includesboth domesticated cultivars (subsp. quinoa) andfree-living, weedy forms (subsp. milleanum ormelanospermum) (Wilson 1981, 1988). Domes-ticated and weedy quinoa populations aresympatric, and share a fundamentally autogamousreproductive system as well as a wide range ofvariation in leaf and grain size and color (delCastillo et al. 2007). Wild and domesticated pop-ulations of quinoa exist under cultivation, whichindicates that domesticated quinoas are generallyaccompanied by wild populations in their variousdistribution areas. Thus, natural hybridizationbetween wild and domesticated populationsprobably occurs easily (Fuentes et al. 2009). Thehighest variation in cultivated quinoa is foundnear Titicaca Lake, between Cuzco (Peru) andLake Poopó (Bolivia), and this is where scientistsbelieve the crop was first domesticated (Heiserand Nelson 1974). The main varieties knownin this region are Kancolla, Cheweca, Witulla,Tahuaco, Camacani, Yocara, Wilacayuni, Blancade Juli, Amarilla de Maranganí, Pacus, Rosadade Junín, Blanca de Junín, Hualhuas, Huancayo,Mantaro, Huacariz, Huacataz, Acostambo, BlancaAyacuchana, and Nariño in Peru and Sajama,


Real Blanca, Chucapaca, Kamiri, Huaranga,Pasancalla, Pandela, Tupiza. Jachapucu, WilaCoymini, Kellu, Uthusaya, Chullpi, Kaslali,and Chillpi in Bolivia (Hernández Bermejo andLeón 1994). Throughout the Andean region,there are several genebanks where over 2,500quinoa accessions are preserved in cold-storagerooms: in Peru, at the experimental stations ofCamacani and Illpa (Puno), K’ayra and Andenes(Cuzco), Canaan (Ayacucho), Mantaro y SantaAna (Huancayo), Baños del Inca (Cajamarca); inBolivia, at the Patacamaya station of the IBTA;and in Ecuador, at the Santa Catalina station ofINIAP.

QUINOA AND ENVIRONMENTALSTRESSES: DROUGHT AND SALINITY

Soil salinization is one of the major environmen-tal issue affecting crop production, especiallyin marginal landscapes or areas with limitedresources (Munns and Tester 2008; Rengasamy2010; Munns 2011; Hussin et al. 2013). Theintensive use of valuable natural resources suchas land and water, along with high soil evapo-transpiration and inefficient irrigation systemsassociated with poor water and soil management,inevitably accelerate secondary salinization thatusually results in the loss of productive areas(Munns 2005; Hussin et al. 2013). Nearly 20%of the world’s cultivated areas and about half ofthe world’s irrigated lands are salt affected (FAO2008). Out of the current 230 Mha of irrigatedland, 45 Mha are salt-affected soils (19.5%), andof the almost 1,500 Mha dry agricultural land,32 Mha are salt affected to varying degrees byhuman-induced processes (Munns and Tester2008). Salinization of irrigated lands causes a lossof US$12 billion of the annual global income(Ghassemi et al. 1995).

In this context, enhancing salt tolerance of theconventional crops has proved to be somewhatelusive in terms of genetic manipulation to allowgreater yields in salt-affected soils and marginalareas (Flowers 2004). The results, althoughpromising, remain insignificant so far (Läuchliand Grattan 2007). An alternative approach is

the use of naturally occurring xero-halophyte forcrop production, “cash crop halophytes,” as theyalready have the required level of salt tolerance(Lieth et al. 1999). The sustainable utilizationof halophytes as cash crops may significantlycontribute toward food, feed, fuel, wood, fiber,chemical production, and environmental quality(dune stabilization, combating desertification,bioremediation, or CO2 sequestration) in manycountries (Geissler et al. 2010; Hussin et al. 2013).Hence, research has focused more and more onthe identification and selection of plant speciessuch as C. quinoa that are naturally tolerant todrought and salinity.

Quinoa is one of the few crops, if not theonly crop, able to grow in the most extremeenvironmental conditions (Jacobsen et al. 2003).In effect, quinoa can be cultivated from sea levelto 4,000 masl, even in the Bolivian Altiplano withan extreme altitude of 4,200 masl. Quinoa is alsoremarkably adaptable to different agroecologicalzones. It adapts to hot, dry climates, can grow inareas of varying relative humidity, ranging from40% to 88%, and can withstand temperaturesfrom −4 to 38∘C. Quinoa can grow in marginalsoils lacking in nutrients, in soils with a widerange of pH from acid to basic (Boero et al. 1999),and even tolerates soil infertility (Sanchez et al.2003). It also has excellent tolerance to extremefrost (Halloy and González 1993; Jacobsen et al.2005, 2007), long drought periods (Vacher 1998;González et al. 2009a; Jacobsen et al. 2009),salinity (González and Prado 1992; Prado et al.2000; Rosa et al. 2009; Ruffino et al. 2010; Hariadiet al. 2011), and high solar radiation (Palenqueet al. 1997; Sircelj et al. 2002; Hilal et al. 2004;González et al. 2009b). It has high water useefficiency (WUE) shown by its tolerance orresistance to lack of soil moisture and producesacceptable yields with rainfall of 100–200 mm(Garcia et al. 2003, 2007; Bertero et al. 2004).Quinoa resists up to 3 months of drought at thebeginning of its growth cycle. To make up forthis part of its growth cycle, the stalk becomesfibrous and roots strengthen. When rains come, itrecovers physiological activity (National ResearchCouncil 1989). Some varieties can grow in saltconcentrations similar to those found in seawater


(40 dS/m) and even higher, well above thethreshold for any known crop species (Hariadiet al. 2011; Razzaghi et al. 2011).

Salt tolerance is a complex trait and attributedto a plethora of interconnected morphologi-cal, physiological, biochemical, and molecularmechanisms. These mechanisms are linked tothe major constraints of salinity on plant growth(i.e., osmotic effects, restriction of CO2 gasexchange, ion toxicity, and nutritional imbalance)and operate in coordination to alleviate both thecellular hyperosmolarity and ion disequilibrium(Koyro 2006; Flowers and Colmer 2008; Geissleret al. 2009). The primary deleterious effectof soil salinity on plant growth is due to anosmotic effect, resulting from the lower soil waterpotential (Ψ), defined as the work water can doas it moves from its present state to the referencestate. The reference state is the energy of a poolof pure water at an elevation defined to be zero(Munns 2002; Koyro et al. 2012). A low valueof (Ψ) interferes with plant ability to take upwater from the soil and, hence, causes a growthreduction, along with a range of physiologicaland biochemical changes similar to those causedby water deficit (Larcher 2001; Schulze et al.2002; Munns 2005). To endure osmotic con-straint, salt-tolerant plants are more restrictivewith water loss via transpiration by a sensitivestomatal closure response. Inevitably, this leadsto a decrease in the apparent photosynthetic ratedue to a restricted availability of CO2 for thecarboxylation reaction (stomatal limitation ofphotosynthesis) (Huchzermeyer and Koyro 2005;Flexas et al. 2007; Dasgupta et al. 2011; Benzartiet al. 2012), thereby suppressing plant growthand productivity (D’Souza and Devaraj 2010;Gorai et al. 2011; Tarchoune et al. 2012; Yan et al.2013).

According to several studies, quinoa toleranceto drought and salinity stresses is dependenton its vegetative stage (Bosque Sanchez et al.2003; Garcia et al. 2003; Jacobsen et al. 2003).At the cotyledonary stage, the high adaptabilityof quinoa to soil salinity is related to metabolicadjustment. In studies carried out with seedlingsof the Sajama cultivar, it was demonstrated thatsalinity tolerance depends on improved metabolic

control of ion absorption and osmotic adjustmentthrough osmolyte accumulation derived from asalt-induced altered carbohydrate metabolism(Rosa et al. 2009; Ruffino et al. 2010), whereasin early maturing stage, it is also related tostructural and physiological adaptations. In thisway, quinoa avoids the negative effects of droughtthrough the development of a deep and dense rootsystem, reduction of the leaf area, leaf dropping,special vesicular glands (salt bladders), smalland thick-walled cells adapted to losses of waterwithout loss of turgor even at severe water losses,and stomatal closure (Jensen et al. 2000; Adolfet al. 2013).

Although quinoa was classified as a highlysalt-tolerant species (Jacobsen 2003; Hariadi et al.2011; Razzaghi et al. 2011; Eisa et al. 2012; Adolfet al. 2013), many quinoa cultivars show distinctvariability in their germination and growthresponses to salinity. More than 200 quinoa acces-sions have been tested under saline conditionsand found to be different in their responses tosalinity. Differences were observed at germinationstage and also later during the vegetative growthstage (Adolf et al. 2012). Moreover, salt toleranceat germination is not necessarily correlated withthe degree of tolerance at later developmentalstages. Eisa et al. (2012) found that the growthof the Peruvian quinoa cultivar “Hualhuas” wasslightly stimulated in response to a low salinitylevel (20% seawater salinity). The same trend ofsalt-induced growth stimulation has been recentlyobserved for the cultivar “CICA” (Fig. 1.1). Theoverall growth of CICA plants based on freshweight (FW) gain was significantly increased∼85% compared with control plants grownunder non-saline conditions. This increase wasmainly a result of increased shoot FW rather thanroot FW (Fig. 1.1). Similar salt-induced stimu-lation of growth has also been reported for otherPeruvian and Bolivian quinoa cultivars (Wilsonet al. 2002; Koyro and Eisa 2008; Hariadi et al.2011). Furthermore, the Andean hybrid grownat salinity level of 11 dS/m showed increases inboth leaf area and dry mass when comparing withplants grow at control salinity level of 3 dS/m.As shown in Fig. 1.1, salinity tolerance thresholdfor CICA variety was at 200 mM NaCl, whereas


Ctr. 100 200NaCI concentration (mM)

300 400 5000

50

100

150

200

b

a

bc

cded

e

Fre

sh w

eigh

t (g)

R S AI JI In Poly. (Growth)

Fig. 1.1 Development and growth responses of differentorgans (expressed as fresh weights) of C. quinoa cv. CICAgrown at different NaCl concentrations. The dotted line marksthe C50 value. Each column represents the mean value ofthree replicates and the bars represent standard deviations.Columns with the same letter are not significantly different at P≤0.05, Duncan test. (R) root, (S) stem, (Al) adult leaf, (Jl) juvenileleaf, and (In) inflorescence.

C50 was slightly above 40% seawater salinity. Thesalinity tolerance threshold is the salt level thatleads to the initial significant reduction in themaximum expected yield (Shannon and Grieve1999), whereas C50 is the water salinity leading to50% growth reduction in the maximum expectedyield. In contrast, salinity levels above thresholdvalue (supraoptimal condition) severely inhibitplant growth in many quinoa cultivars (Hariadiet al. 2011; Eisa et al. 2012). Seawater salinity level(500 mM NaCl) led to a significant reduction(∼66%) in the FW of CICA plants relative tothe control (Fig. 1.1). Inhibition of the initiationof new leaves and the formation of small leaves,some with symptoms of nutrient disorders,might contribute to the low FW observed at thissalinity level. Interestingly, the plants displayedconspicuous growth and continued to grow evenat seawater salinity levels (Fig. 1.1). Together,these results indicate that the CICA cultivar ishighly salt tolerant and productive, capable ofgrowing even under sea water salinity levels.

Salinity stress results in a decrease of pho-tosynthesis in a wide variety of plant species

(Sudhir and Murthy 2004). However, manyhalophyte species show higher level of photo-synthesis under conditions of elevated salinity(Andersone et al. 2012), depending on the levelof salt tolerance of the species and/or genotypes(Brock et al. 2007). Quinoa cultivars also showdifferent photosynthetic responses, depending onparental origin. Recently, Adolf et al. (2012) foundsignificant differences in both photosyntheticCO2 assimilation and stomatal conductance whentwo varieties of quinoa when grown under salineconditions. “Utusaya,” originating from the salarregion of Bolivia, maintained a relatively highstomatal conductance, with only 25% reductionin net CO2 assimilation when compared with theuntreated control plants. In contrast, the cultivar“Titicaca” that has been bred in Denmarkshowed a higher decrease in stomatal conductanceand also a 67% reduction in CO2 assimilation.Interestingly, in the Utusaya variety, both thestomatal conductance and the photosynthesis ratewere generally low under non-saline conditions,whereas these did not decrease in the Titicacavariety. Thus, it may be assumed that in salineenvironments, the Utusaya variety has a genet-ically improved osmoregulator mechanism tocounteract the deleterious osmotic effects of saltand has less need to reduce water loss by tran-spiration (Adolf et al. 2013). A similar trait wasobserved between the CICA (less salt tolerant)and the Hualhuas (more salt tolerant) cultivarsgrown under increasing saline levels. The CO2assimilation (net photosynthetic rate, PN) of theCICA cultivar steadily and significantly declinedwith increasing water salinity, reaching only 1.5%of the control values at seawater salinity treatment(Table 1.3). This result was consistent withobservations on the effect of salinity on photosyn-thesis in many salt-tolerant species (Ashraf 1999;Bayuelo-Jiménez et al., 2003; Qiu et al. 2003;Koyro 2006). In a previous study, however, Eisaet al. (2012) showed that the photosynthetic activ-ity of the Hualhuas cultivar was less affected withsalt-induced reduction of about 72% at seawatersalinity level. Furthermore, the photosyntheticresponses of the cultivars CICA and Hualhuascorrespond with the assumptions of Kao et al.(2006) and Moradi and Ismail (2007), who assume


that relatively higher salt-tolerant species wouldhave less reduced net photosynthesis. On theother hand, the reduction of PN observed inCICA coincided with the progressive decreaseof stomatal conductance (CS), suggesting thatsalinity impacted the photosynthesis of CICAplants, at least partly, by an enhanced stomatalclosure. Positive correlations between PN and CShave been found in C. quinoa, Hualhaus cultivar(Eisa et al. 2012), Atriplex prostrata (Wang et al.1997), Atriplex nummularia and Atriplex hastata(Dunn and Neales 1993), Atriplex centralasiatica(Qiu et al. 2003), and Avicennia marina (Ball andFarquhar 1984).

According to Moradi and Ismail (2007) andCentritto et al. (2003), reduction of stomatalconductance is a significant way to decreasewater loss from the leaves via transpiration andcould be considered as an adaptive feature forsalt tolerance. In CICA plants, the salt-inducedreduction of CS gives a strong inhibition of thetranspiration rate (E), which reaches a minimumvalue at the highest salinity treatment (Table 1.3).This would contribute to conservation of waterand also maintain a positive water balance. In fact,lower values of E represent an additional adaptivemechanism for coping with high salinity levels,as it could reduce salt loading into leaves andhence prolong the leaf lifespan by maintaining asubtoxic level of salt (Everard et al. 1994; Koyro2006).

The coordinated regulation of CO2/H2O gasexchange is considered a key determinant forplant growth and biomass production under salineconditions (Romero-Aranda et al. 2001; Lu et al.

2002; Gulzar et al. 2003, 2005). In Hualhuas, Eisaet al. (2012) found that salt-induced reductionof transpiration rate was proportionally largerthan the photosynthetic rate, leading to improvedphotosynthetic water use efficiency (PWUE).However, this is not the case for CICA, as thesalt-induced reduction of photosynthetic rate wasproportionally larger than that of the transpira-tion rate, resulting in a marked decline of PWUE(Table 1.3). According to Naidoo and Mundree(1993) and Koyro (2000), increasing PWUEis an important adaptive feature for long-termsurvival of plants and would be an advantagein saline environments. This may explain therelatively lower salt tolerance of CICA comparedto Hualhaus. Interestingly, salt-induced reductionof PN in CICA showed a positive correlation withCS, but not with intercellular CO2 concentration(Ci) (Table 1.3), suggesting that Ci is not thelimiting factor for photosynthesis reduction inCICA under saline conditions.

Non-stomatal inhibition of photosynthesis insalt-stressed plants, particularly under severestress conditions, has also been reported forseveral other crop species such as Gossypiumhirsutum and Phaseolus vulgaris (Brugnoli andLauteri 1991), Oryza sativa (Dionisio-Sese andTobita 2000), Helianthus annuus (Steduto et al.2000), and Beta vulgaris (Dadkhah 2011), amongothers. This inhibition of photosynthetic capacityhas been attributed to an inhibited coupling factoractivity (Tezara et al. 2008), reduced carboxy-lation efficiency (Wise et al. 1992; Jia and Gray2004), reduced amount and/or activity of crucialphotosynthetic enzymes such as Rubisco (Parry

Table 1.3 Effect of elevated water salinity on the net photosynthesis rate (PN), transpiration rate (E), Stomatal conductance (Cs),ratio of the internal to the external CO2 concentration (Ci/Ca), and photosynthetic water use efficiency (PWUE) of C. quinoa cv.CICA. All of these values are at the light saturation point of photosynthesis.

Treatments PN (μmol m−2 s−1) E (mmol/m2s) Cs (mmol H2O/m2s) Ci/Ca PWUE (%)

Control 16.615a ± 1.011 2.733a ± 0.234 0.164a ± 0.018 0.491a ± 0.022 0.625a ± 0.019100 mM 12.310b ± 0.122 2.417a ± 0.045 0.140b ± 0.003 0.588b ± 0.006 0.510bc ± 0.006200 mM 10.907c ± 0.119 1.998b ± 0.019 0.111c ± 0.002 0.550b ± 0.010 0.546b ± 0.007300 mM 8.088d ± 0.398 1.232c ± 0.148 0.064d ± 0.008 0.577b ± 0.018 0.446c ± 0.034400 mM 1.105e ± 0.240 0.357d ± 0.032 0.017e ± 0.002 0.747c ± 0.029 0.256d ± 0.034500 mM 0.237e ± 0.048 0.280d ± 0.009 0.012e ± 0.000 0.882e ± 0.015 0.171e ± 0.018

Means within a column followed by the same letter are not significantly different at P ≤ 0.05, as determined by Duncan test. Eachmean represents three replicates.


et al. 2002), reduced ribulose-1,5-bisphosphate(RuBP) regeneration (Giménez et al. 1992;Gunasekera and Berkowitz 1993), and reductionof the contents of photosynthetic pigments(Seemann and Critchley 1985; Hajar et al. 1996;Koyro 2006).

Salinity and drought may also impair pho-tosynthesis by disturbing the photochemicalreactions in the chloroplast (Tezara et al. 2005;Hura et al. 2007). Furthermore, as an indirectconsequence of stomatal closure induced by saltand/or drought stress, restriction in intercellularCO2 concentration should increase suscepti-bility to photochemical damages as excessivelight energy at PSII level increases when CO2assimilation rates are low (Silva et al. 2010). Thiseffect, however, seems to be species specific.For example, sorghum (Sorghum bicolor) plantssubjected to salt stress showed a strong distur-bance of photochemical activity (Netondo et al.2004), whereas cowpea (Vigna unguiculata) plantssubjected to progressive drought displayed slightchanges in the PSII activity (Souza et al. 2004).Moreover, it has been demonstrated that stomatalclosure reduces the CO2/O2 ratio in leaves andinhibits the fixation of CO2, which induces anincreased ROS generation via enhanced leakageof electrons to oxygen (Foyer and Noctor 2000).Therefore, in salt-treated plants, a low rate ofCO2 assimilation can result in oxidative stress.

Salt-induced leaf succulence and reductionin chlorophyll content has also been observed inquinoa plants in response to high water salinity(Eisa et al. unpublished results). With quinoabeing a salt-tolerant species, it is conceivable thatin salt-stressed plants the stomatal closure allowsthe leaves to either develop an additional scav-enging mechanism in their light reaction centersor utilize the excessive energy for ion excretionor sequestration. This condition may lead to areduction of the flow of electrons through thephotosystems (reduction of the apparent quantumefficiency) (Table 1.3). Furthermore, the presenceof a dense layer of bladder hairs filled with salt onthe surface of leaves can form a strong reflectivelight (Fig. 1.2). Thus, this light-reflecting layeris thought to protect the photosystems fromoverreduction and photoinhibition under stress

BH

EC

Fig. 1.2 Representative SEM micrographs of the juvenile leafsurface showing the various stages of bladder hairs develop-ment. BH, bladder hair and EC, epidermal cells.

400 800

PAR (μmol/m2 s)

1200 1600 2000

–5

0

5

10

15

20

25Ctr. 300 mM 500 mM

Pho

tosy

nthe

tic r

ate

(μm

ol/m

2 s)

Fig. 1.3 Light response curves of C. quinoa, CICA cultivar, atdifferent NaCl concentrations. Values are the mean of threeindependent measurements.

conditions (Freitas and Breckle 1992; Agarie et al.2007; Orsini et al. 2011).

Light saturation point (Ls) gradually decreasedwith increasing water salinity, as shown in thecultivar CICA, commensurate with the reduc-tion in photosynthetic capacity (Fig. 1.3). Thismight partially be due to salt-induced reduc-tion in chlorophyll concentration per unit area


Table 1.4 Calculated photosynthetic efficiency (Φc), dark respiration (Dr), light compensation point (Lc), and light saturationpoint (Ls) of C. quinoa cv. CICA plants grown under various NaCl salinities.

Treatments Φc[μmol CO2 μmol−1 Quantum] Dr[μmol m−2 s−1] Lc[μmol m−2 s−1] Ls[μmol m−2 s−1]

Control 300 mM 0.062 0.052 −3.343 −2.627 49.945 46.172 872.297 652.115500 mM 0.034 −1.756 45.722 506.239

The calculation was done using SigmaPlot software.

(Eisa et al. 2012). As a consequence, the calcu-lated CO2 compensation point (Lc) decreasedin response to water salinity. Furthermore,the calculated dark respiration (Dr) decreasedmarkedly with elevated water salinity, being min-imal at 500 mM NaCl (Table 1.4). Salt-inducedreduction in respiration rates might be due tothe fact that the maintenance respiration ofrapidly growing control plants is generally muchhigher than that of the more slowly growingplants grown under high saline stress (Koyro andHuchzermeyer 1999).

CONCLUSION

New goals and insights into food productionand market development are needed in light ofdwindling fresh water resources and the rapidloss of arable land due to soil salinization. Domes-tication of native halophytes and increasing thesalt tolerance of glycophytic crops through thegenetic engineering could achieve these goals, butresearch on these processes is still in the earlystages. Realistically, success in both approacheswill require considerable investment of timeand resources (Rozema and Schat 2013). Giventhis scenario, C. quinoa appears to be a reliablenew crop option to sustain the food supply fora rapidly growing world population. Its hightolerance to salinity and drought, together withits excellent nutritional quality, makes it anideal crop to contribute to food security for thetwenty-first century.

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Chapter 2

History of Quinoa: Its Origin,Domestication, Diversification, and

Cultivation with Particular Reference to theChilean Context

Enrique A. Martínez1, Francisco F. Fuentes2, and Didier Bazile3

1Centro de Estudios Avanzados en Zonas Áridas, La Serena and Facultad de Ciencias del Mar, Universidad Católica delNorte, Coquimbo, Chile

2Facultad de Agronomía e Ingeniería Forestal, Pontificia Universidad Católica de Chile, Casilla 306-22, Santiago, Chile3UPR47, GREEN, CIRAD (Centre de Coopération Internationale en Recherche Agronomique pour le Développement),

TA C-47/F, Campus International de Baillarguet, 34398 Montpellier, Cedex 5, France

QUINOA ORIGINS IN THE CENTRAL ANDES

Quinoa, a tetraploid crop plant, was described forthe first time in 1797 by the German botanist andpharmacist Carl Ludwig Willdenow. It has beencultivated for the past 8,000 years in the SouthAmerican Andes. It is hypothesized that theclosest ancestors of quinoa could be the speciesChenopodium berlandieri var. nuttalliae, distributedin North America, or a complex of species grow-ing in the southern hemisphere, includingChenopodium pallidicaule Aellen (Kañahua),Chenopodium petiolare Kunth, Chenopodiumcarnasolum Moq., and the tetraploïd species,Chenopodium hircinum Schard or Chenopodiumquinoa var. melanospermum. All these species arefrom the Andes (Wilson and Heiser 1979; Heiserand Nelson 1974; Mujica and Jacobsen 2000;Fuentes et al. 2009a). The areas cultivated withquinoa in South America goes from 2∘ Northlatitude in Colombia to 47∘ South latitude inChile, and from 4,000 m in the high Andes to the


sea level in southern latitudes. Particular adapta-tions of this species to certain geographical areasalong the Andes gave rise to five major ecotypesassociated with subcenters of diversity, differingin branching morphology and adaptations torainfall regimes with precipitation of 2000 mmper year to strong drought stress of 150 mm peryear. These ecotypes are the (i) Inter Andeanvalleys quinoa (in Colombia, Ecuador, and Peru);(ii) Highlands quinoa (in Peru and Bolivia);(iii) Yungas quinoa (in Bolivian subtropical for-est); (iv) “Salares” quinoa in salt flats (in Bolivia,northern Chile, and Argentina); and (v) Coastalquinoa, from lowlands or from sea level (in centraland southern Chile). The expansion routes fromthe Titicaca Lake were summarized by Fuenteset al. (2012) and supported with genetic data asrevealed with the use of molecular markers.

The domestication process must have includedall factors of the domestication syndrome, includ-ing larger fruit size, higher and uniform yields,reduced branching and bigger inflorescence,

19


reduced seed dormancy, and less auto dehiscenceor seed fall. The quinoa landraces had alsoadapted to different soils, climates, and partic-ularly day-lengths as day-lengths grow longerin the spring and summer seasons toward thesouthern latitudes.

ANCIENT EXPANSION TO SOUTHERNLATITUDES IN CHILE

Quinoa cultivation in Chile is centered primarilyon two of the five main ecotypes, namely thesalt flat (“salares”) and the coastal ecotypes.The “salares” ecotype is distributed in theTarapacá and Antofagasta regions (18–25∘S) innorthern Chile, with elevations over 3,000 m high(Fig. 2.1). In these regions, highland indigenouscommunities (Aymara and Quechua people)traditionally cultivate these quinoas in salinesoils, with precipitation fluctuating between100 and 200 mm per year falling during thesouthern hemisphere summer, from Decemberto February (Lanino 2006). These ecotypes areclosely related to the quinoa Bolivian varietiesthat are also of the “salares” ecotype, probablybecause these are also cultivated by the Aymaraand Quechua communities on both sides ofthe current Chile–Bolivia border. On the otherhand, there is evidence for the introduction ofsome quinoa genetic materials from the PeruvianAndean zone to the Antofagasta region. Despitethis evidence, the dominant morphology of mostof the quinoa studied so far in Chile is of the “saltflat” ecotype (Fuentes et al. 2009b).

In central Chile (Fig. 2.1) and even at themore southern latitudes (43∘S) (O’Higgins toLakes’ political regions), the cultivated quinoaare different landraces of the coastal ecotype.Areas of quinoa cultivation are rain-fed andhave variable altitudes between sea level and1,000 m height. A remarkable difference is thatcompared to the extremely dry conditions wherethe “salares” quinoa is grown in northern Chile,rainfall in the central and southern zones ofChile occurs during the southern hemispherewinter (June–August), with rainfall fluctuations

between 500 and 2,000 mm per year. This rainfallincreases steadily across 34–40∘S.

When the two ecotypes, “salares” and coastalecotypes cultivated in Chile, are compared, thereis a recognized and remarkable difference interms of their adaptation to altitude, tolerance todrought and salinity, and day-length sensitivity(Bertero et al. 1999; Bertero 2001). In addition,the genetic backgrounds of the two main ecotypescultivated in Chile are also very different. Inter-estingly, even within the southern coastal quinoa,the genetic backgrounds are extremely diverse(Fuentes et al. 2012).

Only one hybrid has been produced andrecorded in the Chilean national system ofprotection for new varieties. The hybrid “LaRegalona” (Von Baer et al. 2009) has been bredfor higher yields and wide adaptation and is ableto grow under day-lengths in latitudes close to theequator to latitudes as far as the polar latitudes upto 40∘ (S or N).

The expansion pattern of quinoa in Chileimplies that it underwent a micro-evolutionaryprocess, supported by a high genetic diversitythat made it possible for ancient peoples to selectquinoa adapted to contrasting and extendedagroecological gradients (Fuentes et al. 2012).The quinoa adaptation process in Chile occurredat least since the past 3,000 years, as revealedby recent dating of seeds found in El Plomohill in Santiago, at central Chile (Planella et al.2011). Seed exchanges occurred throughoutChile even when ancient peoples from the north(Aymara, Quechua, Atacameños or Licanantay,Coyas, Diaguitas), from the center (Picunches,Pehuenches), and from the south (Mapuches,Huilliches) spoke different languages. The peoplefrom the south even gave quinoa another name,dawue (Sapúlveda et al. 2003).

REINTRODUCTION OF QUINOA IN ARIDCHILE AFTER LOCAL EXTINCTION

Quinoa cultivation probably disappeared veryearly in the first two regions colonized by theSpanish conquerors some 400 years ago, in theSantiago and the Coquimbo regions, at 33 and

History of Quinoa: Its Origin, Domestication, Diversification, and Cultivation 21

PeruBolivia

Chile

EcuadorColombia

Argentina

25°S25°S

50°S50°S

0°0°

(a)

(c)

(b)

(d)

Pacific Ocean

Fig. 2.1 Position of Chile in South America (right upper corner) where a long Atacama Desert (a) isolates the country fromsouthern Peru and Bolivia. Quinoa is cultivated in places as the eastern Altiplano (b) at 4,000 m high (“salares” ecotypes), in thecenter (c) and south (d) of the country (“coastal” ecotypes) at sea level or piedmont (1,000 masl).

30∘S, respectively. The recent ongoing effortsto reintroduce quinoa in the arid region ofCoquimbo are supported by the scientific com-munity. In 2003, a new research center, Centro deEstudios Avanzados en Zonas Áridas (CEAZA),started its activities in this northern zone of Chile.One of the objectives of the research conducted inthis region is to relate climate change and naturaland human-induced activities on natural andcultivated lands and coastal waters. In this region(29–32∘S), the climate is mediterranean-deserticand semi-desertic with a marked seasonality, withrainfall occurring in winter and 8–10 dry monthsper year (Novoa and López 2001). The weatherinformation available indicates that averagerainfall in La Serena (30∘S) has dropped about100 mm (50%) in the past century (Martínezet al. 2009a), placing it among those regions withthe greatest decrease in precipitation worldwide(http://www.ipcc.ch/pub/tpbiodiv_s.pdf ).

These changes in precipitation coincided withincreases of 0.6∘C in the earth’s temperature dur-ing the past century (http://www.ipcc.ch/pub/un/ipccwg1s.pdf ).

The environmental conditions in the Co-quimbo region are transitional between theMediterranean climate and the Atacama Desert.Its main transversal (East-West) valleys (Elqui,Limarí, and Choapa) present an increasingpluviometry from the North to the South, withapproximately 60 mm per year rainfall in theElqui Valley to 300 mm per year in the Choapavalley (Favier et al. 2009). Farmers lost incomefrom grain crops such as wheat due to low yields.Farmers who had more income started farmingfruit plantations for export and have been usingdrip irrigation (Jorquera 2001). Even thoughquinoa had been cultivated as early as 3000 B.P.in the arid region of Coquimbo (Planella et al.2011), it probably disappeared very early during

http://www.ipcc.ch/pub/tpbiodiv_s.pdf

http://www.ipcc.ch/pub/un/ipccwg1s.pdf

http://www.ipcc.ch/pub/un/ipccwg1s.pdf


the Spanish conquest when the conquistadoresintroduced wheat and other European crops. Thecity of La Serena was the second city founded inChile, after Santiago, and farmers around bothcities have forgotten even the word “quinoa.”The social memory loss of quinoa has driven thiscrop to near extinction in Chile, with less than300 quinoa farmers represented in the nationalagronomic statistics (INE 2007). In fact, allancestral seeds have been lost from the arid regionof Coquimbo. When this fact was known, CEAZAstarted to acquire quinoa seeds through field col-lections in the rest of the country, from farmersin the Andes highlands, who cultivate quinoaat 4,000 m high, and also from other sources insouthern latitudes at sea level (34–40∘S). Thefirst efforts focused on evaluation of the seedscollected for their adaptation to the arid region,particularly to determine if quinoa could becultivated under the current low precipitation.The tests were also conducted to determine ifquinoa could replace the wheat crop in areasfrom which it has already disappeared due tothe increasing drought trend. The first resultsindicated that seeds from the center and southof Chile gave higher yields than those collectedfrom the Andes highlands if sown in the springseason (Martínez et al. 2007, 2009b). Later on,results showed that extremely low irrigation wasadequate for the quinoa to produce seeds butunder experimental conditions, where all waterapplied was from artificial irrigation (Martínezet al. 2009a). Such experiments showed thatquinoa could grow and produce seeds underextremely low levels of irrigation, equivalent to50 mm of rainfall, but applied at very precisemoments of the cycle (growth, flowering, andrain filling). However, precipitation at criticalgrowth stages cannot be assured for farmerswho depend solely on rainfall. Even thoughrainfall could reach 100 mm per year, there areyears when majority of the rainfall comes in aspan of a few days, as in the case in 2012, when90% of the rainfall came in a single autumn day.Thus, experimental results can only predict theeconomic profit and yields from the arid region ofChile if artificial irrigation is provided. However,

for other southern and more rainy regions ofthe country, quinoa undoubtedly can be a goodrain-fed crop for the future.

Quinoa’s tolerance to abiotic stresses is one ofthe reasons why the Food and Agriculture Orga-nization (FAO) of the United Nations declared2013 as the International Year of Quinoa and topromote it as one of the crops that alleviate worldhunger and poverty. Other reasons to promotequinoa are related to its outstanding capacity towithstand other stressful conditions such as frostand salinity in soils and irrigation water. Ourexperience in reintroducing quinoa in the aridregion of Chile confirmed that germinating seedshave a high tolerance to salinity. Experimentalresults also showed that genetic mechanismsare triggered in response to salinity: either saltsare rejected from plant tissues or higher saltconcentrations can be tolerated inside the cellvacuoles (Orsini et al. 2011; Ruiz-Carrasco et al.2011). Both studies also revealed that quinoasfrom central Chile and those from the high Andesdo have landraces highly tolerant to salt stress.However, those landraces from the more southernlatitudes (39∘S) are less tolerant to salt stress, asshown by the study of Delatorre-Herrera andPinto (2009).

The nutritional value of quinoa is anotheraspect invoked by FAO to promote its worldcultivation and consumption. The presence ofthe 20 amino acids in quinoa seed, and twicethe quantity of proteins than that of manycereals, in addition to minerals, vitamins, goodquality oils and antioxidants, and good qualitystarch, make quinoa seed of high nutritionaland functional value (Galwey 1992; Schlick andBubenheim 1996; Vega-Gálvez et al. 2010). Allthese nutritional properties have been confirmedfor landraces of quinoa from the three ancestralproduction zones in Chile (Miranda et al. 2011,2012a, 2012b). Isoflavones, important for improv-ing milk during breast milk production, havealso been found in Chilean quinoa (Lutz et al.2013). Other flavonoids, probably from its seedcoat saponins, seem to be involved in antibacterialactivity (Miranda et al. 2013).

History of Quinoa: Its Origin, Domestication, Diversification, and Cultivation 23

FINAL REMARKS

The ancestral progenitors of quinoa mighthave originated in North America, but quinoaproduction and the culture that developedalongside its cultivation and consumption isknown to be shared among the ancient peoplesof South America. In ancient times, quinoa wasgrown from the southern part of South Americafrom the highlands of what is now Bolivia, to thefurthest austral latitudes and lowlands of Chileand Argentina, where the agrocultural tradition ofquinoa almost disappeared. This long latitudinalgradient implies at least 3,000 years of quinoaacclimation to new lands, new climates, andlonger day-lengths. Interestingly, the nutritionalquality and stress-tolerant properties of quinoadid not change. Efforts to reintroduce quinoato the arid regions of Chile have shown thatcertain quinoa landraces could produce seed evenunder extremely low irrigation levels, but it hasto be applied at precise points during the growthcycle. At present, there is a wide range of quinoalandraces that can be adapted to new areas in theworld. Stress-tolerant quinoa can be grown inmarginal areas or under harsher environmentswhere the more traditional crops cannot begrown. Moreover, quinoa seed is extremelynutritious and can fulfill the need and demands ofa growing world population for high-quality food.

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Chapter 3

Agroecological and Agronomic CulturalPractices of Quinoa in South America

Magali Garcia1, Bruno Condori2, and Carmen Del Castillo1

1Faculty of Agronomy, Universidad Mayor de San Andres, La Paz, Bolivia2Consultative Group on International Agricultural Research – International Potato Center, La Paz, Bolivia

INTRODUCTION

The Food and Agriculture Organization (FAO)of the United Nations identified quinoa as apotential crop to combat global malnutrition.Quinua or quinoa (Chenopodium quinoa Willd.) isan underutilized crop with enormous potential,mainly due to its nutritional and physiologicalproperties. The crop produces small grains andhas several intrinsic qualities for developingsuperior varieties, including a major gene pool,that is, more than 6,000 varieties and several wildrelatives with outstanding characteristics such asearliness, color, and grain size. Quinoa also has alarge genetic variability and plasticity, resistanceto biotic and abiotic factors, and ability to adaptto adverse soil and climatic conditions in placeswhere most agriculture is marginal. Moreover,quinoa is efficient in its use of production inputs,and thus can be grown through a large range ofproduction environments, from the equator tohigh latitudes, and from sea level to 4,000 m.It has the ability to produce grains even underhighly saline soils. It is a functional and idealfood for human nutrition due to its nutritionalprofile, as represented by the quality and quantityof its essential amino acid composition. Unlikemany other regional products, quinoa grain can


be stored in natural conditions, constituting areserve that can be consumed even after severalmonths or in seasons with food scarcity. Thisproperty increases the value of quinoa in supportof human nutrition. The diversity of its uses andits importance, both cultural and nutritional,make it a principal crop in South America.

Together with potato, quinoa was the staplefood of the indigenous population (Hellin andHigman 2003). Among the food grains cultivatedin the South American highlands, quinoa ranksas a very significant crop in terms of quality andnutritional value. At the time of the Spanishconquest of the Inca Empire in 1532, quinoa,potatoes, and maize were the principal staplefoods in Andean South America, with quinoacultivation extending slightly beyond the regionoccupied by the Incas (Galwey 1993; Cusack1984; Risi and Galwey 1984). Following theconquest, quinoa cultivation declined drasticallyand was displaced by crops preferred by the“conquistadores.” Furthermore, quinoa was notadopted as a crop by European settlers in SouthAmerica or in Europe, as were other New Worldcrops such as maize and potatoes. It was not untilthe last decades of the twentieth century thatinterest in quinoa rose again. The crisis in foodsecurity worldwide made it imperative to look

25


for crop alternatives. Quinoa, with its excellentnutritional profile and genetic diversity, makes itan ideal crop to be developed further.

ANDEAN DOMESTICATION

Quinoa has been cultivated in the Bolivian andPeruvian Andean region for ∼7,000 years byindigenous population groups (e.g., the Aymaraand the Quechua in Bolivia) (Garcia 2003).Several names were given to the crop, such as“mother cereal” in Quechua, or the internation-ally known names “Inca-rice,” “Inca-wheat,” or“Han” (China). People of the Chibcha (Bogota)culture called quinoa “suba” (Valencia-Chamorro2004), the Tiahuanacotas (Bolivia) called it“jupha,” the inhabitants of the Atacama desert(currently in Chile) knew it by the name “dahue,”and in Ecuador, it was called “quimián” (PulgarVidal 1954). Tapia (1979) wrote that the names“quinua” and “quinoa” were used in Bolivia,Peru, Ecuador, Argentina, and Chile.

The monikers “Grain of the Incas” or“Inca-rice,” though internationally known, ismisleading since archaeological evidence showsthat the Andean quinoa was domesticated beforethe Incas (Heisser and Nelson 1974; Jacobsen2003). Through migration and growing trade,the crop spread throughout the Andean regions.Pre-Inca native populations practiced intensiveagriculture, using irrigation, composting, rota-tions, and construction of terraces to conserve soilfertility in the mountains and increase agriculturalproduction, especially in the areas surroundingLake Titicaca. When the Incas established theirkingdom in Cuzco (1100–1533 AC), they quicklyrecognized the extraordinary agricultural andnutritional qualities of quinoa and gave thequechua name “chisiya mama” or “mother grain”and introduced the grain in religious activities.Quinoa served very well as concentrated food forthe Incan army during the marches of conquest.Thus, through the extension of the Inca kingdom,quinoa was also systematically distributed fromChile to Colombia. The variation in quinoa seedsize and the wide range of seed color, from blackto yellow, pink, and white, is a clear indication

that the ancient Andean farmer successfully bredquinoa.

The botany of quinoa was first described byWilldenow in 1778. It was recognized as native toSouth America, with the center of origin locatedin the Andes of Bolivia and Peru (Cardenas1944). The distribution range is fairly widegeographically but restricted to the Andes. Thegreatest diversity of ecotypes can be found inthe Andes, both cultivated and wild relatives.Social, cultural, and economic importance wasalso given to quinoa by peoples of the Andesregion (Gandarillas 1979b).

Bonifacio (2001), Del Castillo et al. (2008),and the FAO (2011) identify four main groups ofquinoa according to the agroecological conditionsof the areas where it is grown: valleys, high plains,salt flats, and sea level. These ecotypes havedifferent and specific botanical agronomic andadaptive characteristics. Most probably, it tookdecades for the actual varieties to be developedfrom the wild forms, though certain wild formsof quinoa are still consumed as vegetable in localcommunities in the Andes (Mujica et al. 2001a).Although its production declined significantlyduring the Spanish conquest, the popularity ofquinoa rose again in the past century and is widelyconsumed at present.

The area where quinoa was domesticated ishardly suitable for agriculture. The Andes, andmore the higher planes, are exposed to harshclimatic and soil conditions. Water shortage is amajor problem due to the combined effect of lowrainfall, high rate of evapotranspiration, and thelow water retention capacity of the soils. Plants areexposed to extremely high rates of solar radiationand large daily thermal amplitudes. During spellsof dry periods, farmers frequently deal with yieldreductions that lead to cumulative shortages ofhuman food and animal feed (Garcia et al. 2003;Jensen et al. 2000). In addition, plant growth isexceedingly hampered by frost in the southernpart of Peru and Bolivia and by high soil salinity,especially in the salt deserts of the southern partof Bolivia (Jacobsen et al. 2003).

As quinoa and other robust agricultural cropshave been domesticated in the harsh environmentof the Andes, with its highly variable conditions,

Agroecological and Agronomic Cultural Practices of Quinoa in South America 27

(a) (b) (c)

Fig. 3.1 (a–c) Examples of quinoa plants in farmer’s field showing the vast diversity of colors and the forms of pani-cles (Province of Omasuyos, bordered to the south and west by Lake Titicaca, Bolivia) (Del Castillo and Winkel, IRD – CLIFA,2002–2008). (See color insert for representation of this figure.)

these crops are characterized by exceptional envi-ronmental adaptation, specifically to mountainand arid conditions with tolerance to drought(Jensen et al. 2000; Garcia et al. 2003, 2007;Jacobsen et al. 2001, 2003, 2003b, 2003c; Boiset al. 2006;Geerts et al. 2008b), frost (Jacobsenet al. 2005, 2007), saline soils (Koyro and Eisa2008; Rosa et al. 2009; Ruffino et al. 2010; Jacob-sen and Mujica 2003; Hariadi et al. 2011; Bosque1998), large ranges in daily temperature, andother abiotic and biotic factors (Jacobsen et al.2003, 2003b; Bertero et al. 2004). These Andeancrops have yielded products of high nutritionalvalue for millennia (Gonzalez et al. 1989, 2009,2010; Grau 1997; Gross et al. 1989; Hermannand Heller 1997; Repo-Carrasco et al. 2003;Jacobsen and Mujica 2003) and are consumed bythe indigenous population.

BOTANICAL AND TAXONOMICALDESCRIPTION

Quinoa is commonly known as a pseudo-cereal,as its characteristics are very different from thoseof the true cereals. First, it is dicotyledonous andnot a member of the Poaceae (grasses) family asare the monocotyledonous cereals. Moreover,quinoa and other specimens such as the amaranthdo not contain gluten, which most typical cerealsdo. The crop has enormous intraspecies vari-ability and plasticity, enabling it to grow under

extremely diverse agronomic conditions. Owingto its physiological efficiency, it is classified asa C3 plant. The Andean quinoa (Fig. 3.1) has aheight of 0.5–2 m, with grains of approximately2-mm diameter. Its roots, often with numerousramifications, can reach up to 1.80 m in depthin times of severe drought in sandy soils. Dif-ferent genotypes exist with and without shootramifications and intermediate forms. The crophas efficient mechanisms against various abioticstresses such as hail, frost, and drought. Mostphenotypic differences are reported in relationwith variety and agroclimatic conditions.

Leaves are polymorphic on the same plant andalso differ much in form and color (green, red,purple) among varieties (Mujica et al. 2001a).They are amphistomatal, with the youngerleaves often covered by Ca-oxalate glands on theupper leaf surface. Flower buds are organizedin typical inflorescences with a central axis andsecondary and tertiary axes. They can be of thelax form (amaranthiform) or the compact form(glomerous). Flowers are incomplete and auto-gamous or allogamous. Both hermaphrodite andunisexual female flowers are present (Bhargavaet al. 2006). The percentage of allogamy differsbetween varieties and goes from nearly from 0%to 80%. Asynchronous flowering is typical ofthe crop. Flowering occurs over a total of 12–15days, although individual flowers remain openonly during 5–7 days, with maximal openingbetween 10 AM and 2 PM (Erquinigo 1970).


Fruits are grain shaped and contain approxi-mately15% moisture at harvest (Gallardo 1997).The pseudo-grains (dicotyledonous embryo,episperm and perisperm) are embedded in aperigonium (modified leaf structure) that has tobe removed during postharvest processing. Ingeneral, large and sweet grains that are white incolor are preferred in the international market,although recently, colored grains are becomingpopular in exotic markets (Geerts et al. 2008b).

Initially, the crop was classified within theChenopodiaceae family (Cronquist 1981), butphylogenic revision has merged the Amaran-thaceae and Chenopodiaceae in the family of theAmaranthaceae (Angiosperm Phylogeny Group2003), and the crop is now a member of thesubfamily Chenopodioidae. It is a member ofthe family of the Amaranths (Amaranthus spp.)and of the Himalayan grain chenopods such asthe domesticated forms of Chenopodium albumL. (Partap and Kapoor 1985a, 1985b). Severalcrops such as sugar beet, beetroot, mangold,spinach and other goosefoot weeds also belongto the family. The genus Chenopodium alsoincludes several grain crops in South Americasuch as C. quinoa Willd. and Chenopodium pal-lidicaule Aellen, vegetables in Mexico such asChenopodium nuttalliae Safford and Chenopodiumambrosioides L., and vegetables or medicinal

plants in South America such as Chenopodiumcarnosolum Moq. and C. ambrosioides (FAO 2011).

GENETIC BACKGROUND AND RESEARCHON QUINOA GENETICS

The Andean region is the center of origin ofquinoa, more specifically the Bolivian and Peru-vian Andes (Bonifacio 2003). In terms of itsgenetic variability, quinoa can be considered asan oligocentric species with its center of originaround Lake Titicaca (Mujica et al. 2001a). Incomparison with the wild types (C. album, C.carnosolum, Chenopodium hircinum, Chenopodiummurale, Chenopodium petiolare), the flower budsof quinoa are more condensed, plant and grainsize larger, and the level of pigmentation higher(Mujica et al. 2001a). Ancient peoples haveselected genotypes on the basis of their use andresistance to adverse biotic and abiotic factors.Over the decades, these genotypes have beendeveloped to the currently known ecotypes(Table 3.1 and Fig. 3.2). Nowadays, traditionalwild types are still locally conserved for medicinalpurposes or as security crop in case of naturaldisasters (Geerts et al. 2008b). In addition, wildquinoa plants, widely distributed in the SouthAmerican Andes, have valuable genes that can be

Table 3.1 Different ecotypes of quinoa, their local names, and theirproperty or principal use.

Ecotype Property or principal use

Chullpi SoupPasankalla Roasted (toasted)Coytos FlowerReales Grain or “pissara”Utusaya Good performance under saline conditionsWitullas andAchachinos

Good performance under coldtemperatures and frost

Kcancollas Good performance under droughtconditions

Quellus (yellowforms)

High yield

Chewecas Good performance under excess waterAyaras High nutritional valueRatuquis Short cycle

Source: Mujica et al. 2001a.


(a) (b) (c)

Fig. 3.2 (a–c) Close-up view of quinoa grains (Del Castillo and Winkel, IRD – CLIFA, 2002–2008).

exploited in the future to increase crop resistanceto climate hazards and adaptation, thus main-taining high production rates. Some populationsare characterized by tolerance and resistance toinsects and diseases, frost, and drought. Theyalso possess favorable traits in terms of nutritionalvalue and the duration of the productive cycle,which also add commercial value to the crop(Rojas et al. 2008; Del Castillo et al. 2007).

At present, the large genetic diversity ofquinoa is conserved in germplasm banks (Bonifa-cio 2003) such as the Bolivian quinoa germplasmbank (PROINPA Foundation 2003a), whichis currently under the management of theNational Institute for Agricultural and ForestryResearch (INIAF). There are several otherquinoa germplasm banks, such as those managedby the Centro Internacional de la Papa (CIP),the Institute of Plant Genetics and Crop PlantResearch (IPK, Germany), the US Departmentof Agriculture (USDA), and the Faculty ofAgronomy of UMSA in La Paz. As reportedin 2010 (FAO 2011), the Bolivian germplasmbank holds 3,121 accessions, including wild-typevariations, though this number continues toincrease due to on-going germplasm collectiontrips. In Peru, the Germplasm Bank at theIllpa Experimental Station in Puno holds 536quinoa accessions, whereas the gene bank at theUniversity of La Molina holds about 2,000 acces-sions (Bravo and Catacora 2010). In Ecuador, theNational Institute of Agricultural Research has608 accessions (Peralta 2009).

In general, ecotypes of the north and centralAndes have small to medium grains comparedto the larger grains of the southern ecotypes of

the salt flats of Bolivia (PROINPA Foundation2003d). A large genetic diversity is also tradi-tionally preserved for auto-consumption in localcultivation systems called “aynokas” (Mujica et al.2001c). “Aynokas” are agricultural productionunits formed by a division of communal areas toensure agricultural and ecological sustainabilityand necessary crop rotation (Aguilar and Jacobsen2003). Unfortunately, due to market pressure,several farming systems in the Altiplano haveshifted to more commercial quinoa varieties andeven different crops altogether, thus reducing theuse of local varieties (Geerts et al. 2008b).

Owing to the large differences in agroecolog-ical environments and the wide distribution ofquinoa in the Andes, three main classes of quinoaecotypes can be distinguished. The valley eco-types have small grain size, tall plants, and highresistance to mildew. The ecotypes around LakeTiticaca also have small grains, medium resis-tance to mildew, intermediate growth cycles, andlow saponin content. In the Southern Altiplano,the ecotypes have higher saponin content, largegrains, and low resistance to mildew. The variousecotypes with local names and the propertiesfor which they are cultivated are presented inTable 3.1.

Quinoa is a diploid allotetraploid (2n= 4x= 36),with 36 somatic chromosomes. The basic numberof chromosomes of the Chenopodium genus isnine (Mujica et al. 2001a). There has beenconsiderable research on the floral biology ofquinoa, such as the proportion of auto-pollinationand cross-pollination. This type of research hasbrought about important advances in hybridiza-tion, selection, and genetic improvement of


quinoa varieties (Mujica et al. 2001a). Breedingprograms are generally directed toward develop-ing cultivars with higher yields, high protein, andlow saponin contents (Bhargava et al. 2006), whileincreasing or maintaining resistance against bioticand abiotic factors, such as downy mildew anddrought (Bonifacio 2003).

ECOLOGY AND PHYTOGEOGRAPHY

The geographical distribution of quinoa extendsfrom 5∘ North Latitude in southern Colombiato 43∘ South Latitude in the Tenth Region ofChile and the Argentinean Andes. The altitudinaldistribution ranges from sea level to 4,000 masl.Quinoa is planted mainly in the highlands sharedby Chile, Peru, and Bolivia. There are coastalquinoa, valley quinoa, and highlands quinoa.The Bolivian Altiplano, with a cultivated areaof more than 100,000 ha, has the world’s largestconcentrated area of quinoa production. A largepart of this extension is located in the south of thecountry, close to the salt flats. The second largestproducer is Peru with a cultivated area of around55,000 ha, concentrated mainly in southernPuno producing more than 41,000 tons per year.In Ecuador, 1,700 ha are dedicated to quinoaproduction in the provinces of Carchi, Imbabura,Pichincha, Cotopaxi, Chimborazo, Loja, Lata-cunga, Ambato, and Cuenca. In Colombia, some700 ha are grown with quinoa, nearly all in thesouth of Nariño, in the municipality of Sapuyes.The north of Chile and the Argentine highlandsare also working to increase quinoa production.

In South America, different quinoa varietiesare distributed according to eco-geographiczones. For example, one of the most popularvarieties is the variety “Real” (PROINPA Foun-dation 2003a) cultivated mainly in the largestproduction area in the Andes, at the south of theBolivian Altiplano. It is grown under conditionsof intensive drought and frost to which it isextremely resistant. In this area, annual rainfallvaries from exceptionally dry in the extremesouth to dry in the intersalar region, from 150to 340 mm precipitation, respectively (Geertset al. 2006b). Farm households rely mostly on

quinoa production (Laguna 2000). The “Real”variety is in demand due to its large white grains.Nevertheless, it has not been grown successfullyoutside its center of origin apparently due to thefact that its flowering is closely linked with lighthours at high altitude and high solar radiationintensity that is absent in other latitudes andaltitudes. To the north of the Bolivian Altiplano,specific varieties more adapted to their localenvironments are grown, generally with small andmedium grains (PROINPA Foundation 2002),but which are completely unable to thrive in thesalt flats of Bolivia. In general, native varietieshave a moderate yield but are more resistant toabiotic factors and have a higher-than-averagenutritional quality if cultivated close to theircenter of origin.

The crop cycle varies largely from 120 to 240days, depending on the varieties and on the zoneof production and the attendant environmentalconditions. In general, varieties grown in colderenvironments have longer crop cycles, whereasshorter cycle varieties are grown in the valleysand lowlands. Sanchez (2012), using a basetemperature of 1∘C for the crop, found in theBolivian Highlands at a thermal time of 1,500heat units, which was fairly constant from Northto South. Apart from this study, there have beenno more studies on the quantity of heat that thecrop needs to complete its growing cycle. Thereare indications that climate change impacts aresomewhat shortening the crops cycles, especiallyin the highlands. Despite this possible climateeffect, research institutions at present are notworking toward the release of early varieties.

The most important phenological stages thatare morphoanatomically significant accordingto Espindola (1980, 1992) and Mujica et al.(2001b) are presented in Table 3.2 with their keyproperties (Geerts et al. 2008b).

CULTIVATION AND AGRONOMICPRACTICES IN SOUTH AMERICA

In general, the production systems of quinoain South America can be grouped into thesystems of the southern highlands, the systems


Table 3.2 Phenological stages of quinoa.

Phenological Start (between x–x daysstage Characteristics after sowing)

0 Germination Seed swelling and bursting 3–51 Cotyledonous phase Plant emergence 3–10 days after sowing2 Two real leaves Initiation of the vegetative

period; a rapid rootdevelopment is noticed

10–20

3 Five alternate leaves Early vegetative stage; sensitiveto competition by weeds

35–45

4 Thirteen alternate leaves Important root ramificationspresent

45–50

5 Preflowering (flower buddevelopment)

Varieties with lax and compactflower buds can bedistinguished

55–70

6 Flowering Flowering starts on top of theflower bud and continues to thebottom; sensitive stage for hail,frost, drought, and diseases

90–130 (50% of flowers)

7 Early grain filling (milky) Grains are still malleable andmoist (50% moisture content orMC); sensitive stage for hail,frost, drought, and diseases

100–130

8 Late grain filling (pasty) The specific color of the varietyis obtained and grains are muchdrier (25% MC)

130–160

9 Physiological maturity Hard and dry grains areobtained (15% MC)

160–180

Source: Adapted from Espindola 1992; Mujica et al. 2001b.

of the central and northern Altiplano, and thoseof the valleys in Ecuador and Colombia. Roughly,the northern and central Altiplano includesthe North Altiplano of Bolivia and the Punoregion in Peru. The so-called intersalar regionis agroclimatologically classified as SouthernAltiplano (Geerts et al. 2006b).

In the Southern Altiplano, quinoa is commonlycultivated mainly as a monoculture. In this sys-tem, fields are left fallow for one to three croppingcycles or even longer, before being cultivatedagain. In the rest of the Altiplano or Highlands,the crop is in rotation with potato or beans (Mujicaet al. 2001b). In the Andean valleys of Ecuadorand Colombia, quinoa is always cultivated aspart of a rotation system after maize and potato(Peralta 2009). Nutritional conditions are gener-ally favorable for subsequent quinoa cultivationafter a potato crop (Mujica et al. 2001b).

Traditional cultivation includes the incorpora-tion of some organic fertilizer, if available, suchas sheep and/or llama dung. The dung is appliedat sowing, after the first weeding and thinning,and at flowering. Mycorrhizal association hasbeen reported in quinoa, which suggests possiblemaximization of nutrients (Mujica 1994).

QUINOA PRODUCTION

Soil conditions

Quinoa can grow in soils with a textural classranging from sandy to clay, although soils withgood drainage are better for the crop. Quinoa canalso tolerate a wide range of soil pH (Mujica et al.2001b), from acid soils (pH 4.5; e.g., Cajamarcaregion in Peru) to more alkaline soils (pH 9; e.g.,salt depressions of Bolivia) with optimum growthin soils with almost neutral pH. The quinoa


plant has high requirements for nitrogen (N) andcalcium (Ca), moderate for phosphorous (P), andminimal for potassium (K) (Mujica et al. 2001a).

Quinoa is a facultative halophyte (Bosque et al.2006; Jacobsen and Mujica 2003) and can growin extreme saline conditions, such as soils withelectrical conductivity that can be as high as52 dS/m (Jacobsen et al. 2001). Adjustment ofleaf water potential by the accumulation of saltions in tissues enables the plant to maintain cellturgor and transpiration under saline conditionsin the salt flats of the Altiplano. Potentially,quinoa could play an important role in cleaningsalt-contaminated soils (Jacobsen et al. 2003).Gonzalez and Prado (1992) reported that germi-nation is retarded due to increased soil salinity,but even at very high salinity, seeds can remaindormant and viable. Nevertheless, tolerance orsensitivity to soil salinity is dependent on thevariety (Schabes and Sigstad 2005).

CLIMATE

Drought resistance

Owing to its phenological plasticity and resistanceto climate constraints, quinoa is exceptionallyadapted to the different arid climates of theAndean region (Mujica et al. 2001b). In theAndean Altiplano, droughts can occur at the endand beginning of the rainy season due to a decreasein the length of the rainy seasons. Droughts canalso occur within the growing period becauserainfall in the Altiplano is likely to occur indelimited episodes of rain, separated by dryperiods (Garreaud et al. 2003; Garcia et al. 2007).Intraseasonal dry spells are by far as important tocrop yield as interseasonal differences, especiallywhen the dry spells occur during critical growthstages such as anthesis (Fox and Rockström 2000).Generally, quinoa is a remarkable crop in thatit can still produce grains even under droughtconditions (Garcia et al. 2003). Quinoa is veryefficient in water use, despite being a C3 plantspecies. Several mechanisms related to droughtresistance are present in quinoa, includingdrought escape, tolerance, and avoidance (Jensen

et al. 2000). Many of these mechanisms also serveto make quinoa tolerant or escape the effects ofother abiotic stresses such as frost. However, whendrought occurs during sensitive phenologicalstages, such as emergence, flowering, and milkygrain, yields can be severely reduced.

Drought escape appears as a lengthening ofthe growth cycle in response to droughts duringearly vegetative stages and as an early maturingprocess in response to drought stress during thelater growth stages (Jacobsen and Mujica 1999;Garcia 2003;Geerts et al. 2006a). Early maturingis an important escape mechanism in the Andeanareas with frequent droughts at the beginningand end of the growing season (Jacobsen et al.2003). Quinoa tolerates drought mainly throughtissue elasticity and low osmotic potential, whichis a measure of solutes in the plant. Proline mightact as a main regulating agent for the osmoticbalance in quinoa as it does in cotton (Paridaet al. 2007). In turgid tissues, proline is knownto oxidate quickly, whereas under water-deficitconditions, proline oxidation is inhibited. Indeed,Aguilar et al. (2003) reported that proline contentwas highest in varieties from eco-geographiclocations with distinctly unfavorable droughtconditions and large differences in day and nighttemperatures.

The quinoa plant also avoids the negativeeffects of drought through a high root/shootratio (Bosque et al. 2003; Sanchez et al. 2003),reduction in the leaf area by leaf dropping,dynamic stomatal behavior, and the presence ofspecial vesicular glands of Ca-oxalate, which aresmall and thick-walled cells that preserve cellturgor even during severe water losses (Jensenet al., 2000). The Ca-oxalate glands are a veryspecific drought resistance mechanism for quinoa.Ca-oxalate crystals are hygroscopic and have atwo-way function for drought stress mitigation.First, they are assumed to increase albedo anddecrease the direct radiation on the leaves.Second, they are assumed to control excessivetranspiration by humidification of the stomatalguard cells (Mujica et al. 2001a). Asynchronousflowering within the flower bud is another mecha-nism to spread the risk and is induced by droughtand several other abiotic stresses.


Although quinoa possesses a wide variety ofdrought resistance mechanisms, water stressstill decreases grain yields quite often (Bilbaoet al. 2006; Bosque et al. 2003), except whendroughts occur during the initial growth phasesafter successful emergence that induce a certainhardening (Huiza 1994; Bosque et al. 2000;Garcia 2003; Geerts et al. 2006a).

Temperature and photoperiod

In general, the adequate mean temperature forquinoa growth is 15–20∘C, but it can grow atmean temperatures ranging from 10 to 25∘C.Extremely high temperatures can cause flowerabortion (Jacobsen et al. 2003). Apart fromdrought, frost is one of the major growth limitingfactors in the Altiplano (Carrasco et al. 1997;Hijmans 1999; François et al. 1999). Frost canreduce yield due to cell destruction and even plantdeath (Fig. 3.3). Quinoa is one of the few cropsthat can tolerate frost to a certain extent, but thisdepends largely on the duration of the frost, thequinoa variety, the phenological stage of the plantwhen frost occurs, the relative humidity, and themicro-location of the fields (e.g., hill slopes havelower risk of frost compared to valleys).

Jacobsen et al. (2005) studied the influence offrost events of different duration and intensityin various phenological stages and for differentcultivars of quinoa. They found that quinoa ismost susceptible to frost from the flower bud

formation stage onward but less susceptibleduring the vegetative stages (Bois et al. 2006).A temperature of −4∘C lasting for four hoursduring the flowering stage caused seed reductionup to 66%, while quinoa in the vegetative periodwas considerably damaged when exposed totemperatures of −8∘C which last for 2–4 h.

Recently, Jacobsen et al. (2007) reported thatthe main survival mechanism against frost inquinoa is a moderate supercooling that avoids iceformation. Supercooling is the cooling of liquidbelow its normal freezing point without crystal-lization of the liquid. The high level of solublesugars in quinoa reported in their study may causea reduction in freezing temperature and the meanlethal temperature. Proline content and the con-tent of soluble sugars such as sucrose may serve asindicators of frost tolerance in different varieties.

Quinoa also tolerates a broad range of radiationintensities, from radiation at sea-level up tointensive radiation at high altitudes. Genotypeshave been classified as short day, long day, andindifferent, in relation to photoperiod sensitivity(Bertero 2003). Bertero (2001, 2003) and Berteroet al. (1999a, 1999b, 2000) conducted extensiveresearch on photoperiod and temperature sensi-tivity of quinoa development in South America.Varieties originating from Colombia to SouthernChile were used in the study, and all cultivarshad a facultative short day response in termsof duration of emergence to flowering. It wasdemonstrated that the duration of all phases of

(a) (b)

Fig. 3.3 (a,b) Frost damage in quinoa (−5∘C at 60 days after sowing).


development is sensitive to photoperiod (Bertero2003). In the same way that water stress duringcertain phenological stages influences the dura-tion of subsequent phenological stages (Garcia2003), the duration of the photoperiod duringcertain phases also influences subsequent phasesand is called delayed response (Bertero 2003). Themean incident radiation affects the phyllochronin quinoa, with higher incident radiation causinglarger phyllochrons. However, cultivars withthe highest photoperiod sensitivity and largestphyllochron were insensitive to radiation (Bertero2001).

Temperature sensitivity was highest in quinoacultivars originating from cold and dry climatesbut lower in cultivars from warmer and humid cli-mates (Bertero et al. 2000), an observation that canpossibly explain why varieties from the highlandsare more affected by global warming. The highersensitivity of cultivars from regions with frequentlate season drought and frost predisposes them fora faster seed filling when photoperiods are short-ening and unfavorable conditions are approaching(Bertero 2003).

Hail

Hail, and sometimes snow, are sporadic and quitelocalized in the Andes (Jacobsen et al. 2003) butmay still cause substantial yield losses in quinoa,especially when flower buds are already present(Fig. 3.4, unpublished data). As is the case forother abiotic stresses, susceptibility to hail islargely dependent on the variety.

CULTIVATION

In the Andes, quinoa is mainly grown during theaustral summer months (September to May),although the sowing times markedly differ and insome equatorial areas cultivation may go beyondthat period. Similarly, the production techniquesare in accordance to the local ecosystem, and sodiffer from one system to another. In the areassurrounding the southern salt flats, traditionalcultivation includes field preparation carried outfrom March to May on virgin fields or fields

Fig. 3.4 Quinoa after hail damage (Del Castillo and Winkel,IRD – CLIFA, 2002–2008).

that are fallow to capture moisture from the laterains and some winter snows and store it for thefollowing season. Much of the intensity of fieldcultivation (plowing, breaking, harrowing, andleveling) depends on the years a field has beenfallow, the soil texture, and the availability of atractor.

In the northern Altiplano of Bolivia and Peru,field preparation is done either shortly afterharvest of the previous crop or before sowingafter the first rains. In Ecuador and Colombia, thecultivation period could range from November toFebruary, after the onset of the rainy season.

Sowing

Quinoa production in areas close to its cen-ter of origin goes from fully traditional tosemi-mechanized to fully mechanized. Fieldpreparation and sowing is carried out either byhand or tractor (Fig. 3.5). In general, it has to bestressed that mechanization often causes excessive


(a) (b)

Fig. 3.5 (a) Traditional quinoa farming with little soil surface opening and large spaces between plants (SUMAMAD-UMSAteam). (b) Mechanized fields (Winkel 2013 ©IRD).

eolic erosion and fertility loss due to increasedsoil denitrification, especially in the southernhighlands.

The average sowing date of quinoa in the Andeslies mostly between September and November,although in some minor areas close to the equator,the sowing date could extend until February. Thedifferences in sowing dates are due to crop cyclelengths of individual varieties and local climaticconditions. The sowing date also depends mainlyon availability of initial soil moisture. Sowingis one of the most important activities becausethe emergence of seedlings, which impacts plantdensity and final yields, depends on this stage.Sowing is a key practice for the success or failureof the quinoa crop and requires quite some expe-rience. Quinoa seeds are sown at different times,depending on the place to be sown, the varietaltraits, and soil moisture. These are also importantfactors in determining the sowing method to beused, whether manual or mechanical. Superficialsowing poses the risk of seed dehydration orburning by solar radiation, whereas deep sowingcan prevent germination due to restricted growth(Rodriguez and Raffaillac 2003).

The sowing method most often used in thesouthern highlands near the salt flats of Bolivia isthe manual method, which is to dig sowing pitsat an average distance of 1 m. Using a “taquiza”

(a local specialized tool), holes are dug until moistsoil is reached. Several seeds are then depositedin the hole and immediately covered with soil toa depth ranging from 4 to 10 cm. Sowing densityis generally from 8 to 15 kg/ha, with lower seeddensities when high-quality, certified seeds areused (Mujica et al. 2001b; Aguilar and Jacobsen2003; Yucra and Garcia 2007). Shortly aftersowing, pits are often covered with grasses orsmall shrubs to prevent burning of seeds due toextreme solar radiation.

Previously, the cultivation of quinoa in thesouthern highlands near the salt flats of Boliviarelied exclusively on the manual sowing method asdescribed. The production system also includes astrong linkage with the llama husbandry becauseof the positive effect of the animal dung to cropproductivity. At present, though, the productionsystem is shifting toward a more mechanizedmethod (Cossio 2008). Owing to the higherdemand for quinoa, the agricultural frontier hasbeen extended. More virgin land on the flats isbeing plowed, drastically reducing the naturalvegetation and giving rise to some environmentalproblems (Jacobsen 2011).

In contrast, sowing in the north Altiplano ofBolivia and south of Peru is generally by furrow,with a distance of 0.4–0.8 m in the furrows oron the ridges. Less common sowing methods are


by transplanting (inter-Andean valleys) to avoidintensive weeding later on or by broadcasting theseeds. In the inter-Andean valleys of Ecuador andColombia, the traditional cultivation techniqueconsists of sowing under dry conditions inrotation with potato or on strips in maize crops,with little soil preparation and using only theresidual organic fertilizers from the precedingcrop. Sowing density varies between 15 and 20 kgseeds/ha. Regardless of the area where quinoais cultivated, traditional Andean growers alwayslook to reduce the risk, and sow several ecotypesat different times and in different locations.

Fertilization of quinoa

One of the problems in quinoa cultivation is thelocal belief that as it is an indigenous crop, it isunnecessary to provide a large quantity of exter-nal inputs. Actual field application by farmers isnot a priority, although animal dung is applied toquinoa fields or pits, when available.

Research on quinoa fertilization has beenlimited. Schulte auf’m Erley et al. (2005)reported that quinoa responds strongly tonitrogen fertilization, producing up to 3.5 t/hawith a fertilization rate of 120 kg N/ha withoutreduction in nitrogen use efficiency. Harvestindexes were not affected by nitrogen applicationbut grain nitrogen content increased significantly.Murillo (1995) investigated the application of80 kg N/ha for quinoa in Bolivia at sowing,without additional P or K application. Yieldand grain quality increased significantly. More-over, they reported the necessity of additionalirrigation to facilitate nitrogen absorption whenrainfall is inadequate. Berti et al. (1997) applied0–225 kg N/ha to quinoa sown at sea level inChile and found the highest yields (3,555 kg/ha)at the highest fertilizer levels. The yield responseto increasing N fertilization was quadratic inshape, and a slight decrease in nitrogen use effi-ciency was noted up to 225 kg N/ha. Moreover,the harvest index was significantly lower for treat-ments with high N fertilizer application. In otherChilean experiments, yields up to 5 t/ha werereported for quinoa fertilized with N combinedwith drip irrigation (De la Torre-Herrera 2003).

To ensure an adequate nutrient supply forcrops, growers must strive to maintain a goodbalance of nutrients in the soil (Miranda 2012).The loss of nutrients has to be minimized, whilemaximizing efficiency in their addition as theirremoval during harvest is unavoidable. The higherand better the quality of yield is, the greater theremoval of soil nutrients. Therefore, to increasequinoa yields in a sustainable way, it is extremelyimportant to consider application of fertilizers,particularly as quinoa is well known for the highquality of its protein, suggesting a strong nitrogendemand from the soil. Without fertilizers, therecould be permanent soil nitrogen and nutrientdepletion, rapidly degrading an already poor soil.

As the organic market is the largest nichemarket for quinoa, most fertilization researchhad been conducted on the application and useefficiency of manure in fields. The application oforganic fertilizers, especially manure, at inappro-priate times and quantities will not necessarilyimprove soil characteristics but may even havenegative effects on the soils, especially over theshort-term period. The actual incorporation ofmanure into the soil in farmers’ fields ranges onlyfrom 4 to 10 t/ha. Small quantities of manureincorporated within the production systems willincrease field labor but with negligible effect onyield. With such results, farmers get discouragedand forgo manure application. To have a signifi-cant effect, manure should be applied at higherrates, up to 20–30 t/ha, to guarantee adequaterevenue from crop harvest and commercialization,in addition to maintaining good soil structure(Miranda 2012). An adequate soil and waterbalance, as well as water availability during criticalperiods, is essential to reap benefits from soilfertilization, especially manure application.

The timing of fertilization is also impor-tant when working solely with organic fertilizers.There is limited effect on crop yield when manureis applied during sowing because the nitrogenwill be liberated approximately 50–60 days afterapplication, especially in the highlands of theAndes. The low air and soil temperatures preventthe rapid decomposition of manure and resultin a slow release of nutrients. The best time toapply manure is around 2 months before sowing,


or at least 45 days, to adequately age the manure.Working with compost, Miranda et al. (2012)demonstrated a reduction in the time needed formanure to be decomposed and showed the bene-fits to the crop because of the accelerated ageing ofmanure.

In general, in the northern Andes, wherequinoa is sown after potatoes, organic mattercontent and nutrients is favorable for quinoa. Insome cases, the slow decomposition of manure,coupled with previous application of nutrientsfor the potato crop, almost fulfill the nutrientrequirements of quinoa. Afterward, the crop onlyneeds supplemental fertilization.

However, when planted after a grain crop (cornor wheat on the coast and barley or oats in themountains), it is necessary to use organic matter ina ratio of at least 3 t/ha. The average fertilizationrequired is in the formula 80-40-00, equivalent to174 kg/ha of 46% urea, 88 kg/ha of 46% triplecalcium, and zero potassium. Potassium is freelyavailable in the soils of the Andes and in SouthAmerica in general, as there are large quantitiesof potassium-retaining clays in the soils.

On the coast, soil nutrients are scarce as theamount of organic matter is extremely low andsoils are very sandy. In general, the formularecommended for fertilization is 240-200-80,equivalent to 523 kg/ha of 46% urea, 435 kg/haof superphosphate, 46% calcium triple, and134 kg/ha of 60% potassium chloride. In addi-tion, application of manure, compost, humus, ororganic matter is recommended, when available.

Cultural practices

Cultivation is limited to one or two hoeings,with an occasional hilling-up, particularly in theinter-Andean valleys. Hoeing is done duringthe first phenological phases, whereas hilling-upis specific for furrow-sown quinoa and is alsoused for additional fertilization just before budformation to optimize yields. When there isexcessive vegetative growth, hilling-up can benecessary to avoid plant lodging due to heavycanopy. Also, thinning of plants is necessary toprevent intraspecific competition. If sown in

rows, quinoa plants should be spaced around10 cm apart (Aguilar and Jacobsen 2003).

Early weeding (±30 days after sowing) is impor-tant in quinoa fields in the Altiplano as plantscompete with each other for scarce nutrients(De Barros Santos et al. 2003; Bhargava et al.2006). Additional weeding is generally carriedout around flowering (±90 days after sowing).Chemical weed control is not recommended soas to preserve field biota. In the case of organicquinoa, chemical weed control is prohibited.

Crop water requirements and irrigation

Quinoa is known largely for its drought resis-tance (Jensen et al. 2000; Geerts et al. 2008a).Therefore, it is traditionally cultivated underrain-fed conditions, even in semi-arid and veryarid locations. However, this high drought resis-tance is often translated in low yields, becausequinoa sacrifices yield for survival and adap-tation. Under this consideration, Geerts et al.(2008a, 2008b) studied the impact of additionalwater on quinoa production and found deficitirrigation (DI) to be highly beneficial in variousexperimental locations. DI is already practiced inthe re-introduction of quinoa in the arid regionsof Chile (Martínez et al. 2009). On the otherhand, quinoa is rarely grown under full irrigation,probably because it is not traditional and becauseit does not respond well to high irrigation due tothe increased risk of downy mildew.

Analysis of water requirements showed howmuch water quinoa requires for “optimal” pro-duction (Garcia et al. 2003). The analysis alsodetermined which stages in quinoa productioncould be more efficient regarding water con-sumption and transformation into yield. The ideawas to apply DI with the aim of concentratingirrigation during the most sensitive crop stages,while maximizing water use efficiency (WUE).The results were quite significant, showing thatregardless of the cropping location, the mostsensitive stages for successful or at least mediumyields were crop establishment (emergence) andflowering. Moreover, an adequate balance betweenevapotranspiration before and after anthesis, witha larger proportion of water consumed after


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Fig. 3.6 (a) Relationship between water use efficiency (WUE) and pre- and postanthesis evapotranspiration rate. (b) Relation-ship among WUE, yield, and (full and deficit) irrigation requirements. (Source: Geerts et al. 2008b).

anthesis, will have a large positive effect on WUE(Fig. 3.6). Therefore, the general advice is to con-sider irrigation in years when the onset of the rainyseason might be delayed, and during flowering andgrain filling when there are frequent dry spells.

Biotic threats: pests and diseases

Although quinoa can tolerate extremely unfa-vorable growing conditions, pests such as birds,insects, and rodents, and several diseases causedby fungi, bacteria, nematodes, and viruses cancause significant yield losses (Danielsen et al.2003; Rasmussen et al. 2003). Disease and pestoccurrence in quinoa often depends on plantdensity, presence of weeds, relative humidity,the nutrient state of the field, and on the croprotation used (Nieto et al. 1998; Mujica et al.2001b; García et al. 2001; Danielsen et al. 2003).Preventive actions against pests and diseases inquinoa fields are of primary importance, and anessential component of integrated pest manage-ment (IPM). Because a complete overview of allbiotic threats against quinoa is out of the scopeof this chapter, only a few important pest anddiseases of quinoa in the Andean highlands aredescribed. Export organizations and companies,as well as researchers, have stressed the need forresearch on host resistance and pest population

carry-over from one to another growing seasonto another. At present, there is a dearth in suchresearch.

An important fungal disease in quinoa is downymildew (Peronospora farinosa Fr.) (Danielsen et al.2003; Butron et al. 2006). To prevent this disease,local extension services are encouraging farmersto use healthy, certified seed (Mujica et al. 2001b).Early application of fungicide or organic remediesis extremely important for an effective mildewcontrol. Danielsen and Munk (2004) reportedspectral reflectance measurements as a methodfor yield loss prediction because of downy mildew.The critical period attaining peak disease severityis around flower bud initiation, occurring around60 days after sowing (Kumar et al. 2006). Siñaniet al. (2006) stressed the relationship betweenrelative humidity and mildew occurrence. Ingermplasm banks, several studies have beenconducted to identify quinoa accessions resistantto mildew (Gamarra et al. 2001). Althoughresistance to mildew depends largely on thevariety, Danielsen et al. (2001) reported severeyield losses up to 33% even in the most resistantvarieties. Highly susceptible varieties had almost100% yield losses.

Another important pest, occurring throughoutthe cropping cycle, is the moth “ticonas,” whichis actually a complex group of at least four genera.


Larvae of these insects are very harmful. It onlytakes one larva per plant to cause serious damage(PROINPA Foundation 2003b). In the central andsouthern Bolivian Altiplano, the Lepidopteranpest Eurysacca melanocamta Meyrick (K’conaK’cona) is very destructive, mostly during thelarval stage (Avalos and Saravia 2006). Thisspecies can survive all year round as it has severalpossible hosts (PROINPA Foundation 2003c). Forall pests and diseases, pesticides (either chemicalor organic mixtures) have to be applied at theright stage during the generative cycle of theinsect or fungus.

In addition to insects and fungi, bird androdent pests are an emerging problem and aprimary cause of yield loss in quinoa. Eventhough Bhargava et al. (2006) reported that lossesdue to birds and rodents are minor because ofthe defense accorded by saponins (which couldbe true for varieties with high saponin content),our own field experience and reports from otherresearchers estimate that yield losses could go ashigh as 60% (Rasmussen et al. 2003). Unfortu-nately, little research has been performed on thisarea to obtain a more generalized yield loss due tobird and rodent feeding.

Seed harvest and postharvest technology

The harvest time in the South American Andesmay extend from February to May, but April is theprincipal harvest month. The optimum time forcutting plants depends on several factors, such asquinoa variety, soil type, humidity, and prevailingtemperature. It is crucial to know when the plantsare ready for harvest. Usually, the leaves turn yel-low or red, depending on the variety. The grainscan be seen in the panicle through the openingof the perigonium, also indicative of physiologi-cal maturity (Aroni 2005). Another way to test ifthe plant is ready for harvest is to tap the paniclewith the hand. If the grains fall out, harvesting canbegin.

Quinoa is harvested mainly by pulling out theplants and leaving them in stacks on the field todry (Fig. 3.7). The disadvantage of this methodis that it removes the roots from the soil insteadof being left as organic matter. This method also

contributes to soil erosion and lowers soil fertility.Another disadvantage of this method is that soilparticles can be mixed with the grain.

Harvesting can also be done manually bycutting the plant with a sickle 10–15 cm abovethe soil and leaving the stubble in the soil, thushelping in soil conservation. The plants must becut at the right time, that is, when the paniclesstill retain grain upon handling, because whenthe plants exceed maturity, grains drop from thepanicle. The disadvantage of this method is that itcannot be used on very sandy soils because thesesoils do not have enough mechanical resistanceto permit these actions. Also, it is quite difficultto cut large plants with thick stems and thereforethe method of pulling out plants is preferred andcommonly used by farmers.

Semi-mechanical harvesting involves cuttingthe plants with a mechanical mower, which iseasier to use when the plants are arranged in holesor furrows. Use of a mechanical mower speedsup the harvest, which is a distinct advantage,and leaves the stem and roots in the soil forincorporation later (Aroni 2005). The first twomethods described require more hand labor andmore harvest losses are expected, as compared tosemi-mechanical harvesting. The crop can alsobe harvested using either combine harvesters orstationary harvesters.

Actual yields range from 500 to 1,000 kg ha−1ofgrain at farmers’ level, even though yields of upto 5,000 kg/ha can be achieved under suitableclimatic conditions. Adequate rainfall and favor-able temperatures do not always prevail in thedifferent agroecological areas of the Andes, thusthe discrepancy between potential and actualyields. Approximately 5–10 tons of chaff perhectare is gained as a by-product and can be usedas livestock feed.

Harvest can take up to 45 days due to asyn-chronous flowering and ripening, which is anatural defense mechanism of quinoa to theadverse climatic events common in the area.Threshing is carried out after additional dryingof the quinoa and can vary from completelymanual to mechanized (Salas 2003). Naturalor mechanized ventilation is used to removeimpurities and dust. Additional ventilation is


(a) (b) (c)

Fig. 3.7 Two methods of manual harvesting of quinoa: (a,b) pulling out the plants and leaving them in stacks on the field todry; (c) plants are piled above ground and left to dry (Del Castillo and Winkel, IRD – CLIFA, 2002–2008).

also used when the percent grain moisture istoo high from a commercial requirement (whichshould be <10%). Once the grain is cleaned, it isgenerally washed or toasted to remove saponin, abitter substance in the pericarp that constitutesa chemical defense against the feeding activity ofinsects and animals. The use of chemicals (e.g.,sodium hydroxide) to make saponins soluble iseffective but is not widely used. Saponin contentis higher in varieties classified as “bitter varieties”and lower in “sweet varieties.” Processing costsare related to the saponin content of the variety.Another complementary postharvest process isgrain size and color selection corresponding todifferent commercial uses such as direct grainconsumption and flour.

Improper postharvest practices are a majorcause of low yields in the South American Andes(up to 40% yield loss) and stagnant export(Salas 2003). Specifically, improper postharvestpractices cause poor grain germination, fungiand mold damage, and color and odor change. Toprevent postharvest losses and refine postharvesttechnology, fundamental researches on thephysical properties of quinoa seeds are to beconducted (Prego et al. 1998; Sigstad and Prado1999; Sigstad and Garcia 2001; Vilche et al. 2003;Tolaba et al. 2004; Gely and Santalla 2007).

Germination studies are often carried outtogether with seed and postharvest studies. Jacob-sen and Bach (1998) and Jacobsen et al. (1999)report that light had no influence on germinationrate or on final germination. On the other hand,harvest time, moisture content of seed at harvest,

and germination temperature seemed to havesignificant effects. Seeds that were harvestedlater, and thus had lower moisture content atharvest, had higher germination percentage.Furthermore, the thermal time to germination,defined as root protrusion, was 30∘ days (Jacobsenand Bach 1998).

Many of the quinoa commercial chain inAndean countries go through traditional inter-mediaries who have ways of transporting the cropproduce. The major portion of conventionallyproduced quinoa is processed traditionally inplants owned by intermediaries or wholesalers.Bio-quinoa for export is usually processed insemi-industrial plants (Brenes et al. 2001).

Within the quinoa cluster, organizations suchas the National Association of Quinoa Producers(ANAPQUI) and the Central de CooperativasAgropecuarias Operacion Tierra (CECAOT) areclassified as supporting organizations (Breneset al. 2001). ANAPQUI represents about 5,000of the approximately 20,000 quinoa producersin Bolivia. Its activities are concentrated in theSouthern Bolivian Altiplano and mostly onorganic quinoa. The quinoa produce, which ismostly organic, is destined in part for the exportmarket. Even though the international pricesof organic quinoa are 10–15% higher than forconventional quinoa, the demand for organicquinoa is increasing worldwide (Hellin andHigman 2003).

ANAPQUI is an association well known forits positive support of quinoa producers dueto guaranteed prices, extension, and certain


mechanization (Magliocca 2002). The impactof such an organization is proof of the positiveeffect of integrating activities at various levelsof the market and processing chain. There isalso increased jurisdictional security by havingan association of farmers. However, restrictionson the use of agricultural inputs, in some casesnot adapted to local family production, make itextremely difficult for farmers to practice organicagriculture. In fact, farmers in other areas ofthe Andes do not produce much organic quinoabecause they prefer to spend their labor on cropsthat they perceive to be less labor intensive andmore economically rewarding.

Hellin and Higman (2003) investigated thestability and viability of potato and quinoaproduction systems in Bolivia, Ecuador, andPeru under current market pressure. They reportthat quinoa consumption has been improvedby government-sponsored initiatives that usequinoa in food support programs (e.g., free schoolmeals). Initiatives by private or nongovernmentorganizations also strengthen quality production,processing, public image, and market accessamong smallholder producers. Private as well aspublic interventions are essential and are to besupported in remote areas where quinoa is oftenthe only subsistence crop (Hellin and Higman2003).

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Chapter 4

Trends in Quinoa Yield over the SouthernBolivian Altiplano: Lessons from Climate

and Land-Use Projections

Serge Rambal1,3, Jean-Pierre Ratte1, Florent Mouillot2

and Thierry Winkel21CNRS, UMR 5175, CEFE, F-34293, Montpellier cedex 5, France

2IRD, UMR 5175, CEFE F-34293, Montpellier cedex 5, France3Universidade Federal de Lavras Departamento de Biologia, CP 3037, CEP 37200-000, Lavras MG, Brazil

SUMMARY

The Southern Altiplano of Bolivia is the worldleader in quinoa export. In these arid high-lands, quinoa yield is largely influenced byon-going changes affecting both climate driversand land-use practices. We developed a simple“what-if ” simulation model for anticipat-ing such changes in quinoa yields over threetime-slices: a recent past (1961–2000), a nearfuture (2046–2065), and finally a remote one(2081–2100). Outputs from a global climatemodel (GCM) were used as drivers for pro-jections of regional climate patterns and forproviding risk information. For tackling furtherproblems arising from our limited understandingof what the local-level impacts of climate changeare likely to be in this arid mountain area, wedecided to consider a grid-level area centered onthe salar of Uyuni, a region experiencing markedchanges in climate and land use for the pastfour decades. Local land-use change scenarioswere derived from aerial photographs and datafrom high-resolution remote-sensing validated by


ground truth observations on sample areas repre-sentative of the region. Climate change scenarioswere linked to our yield model composed of asoil water balance model coupled with a simplecrop growth component. The daily climate fromGCM runs has been used for driving the soilwater balance model and calculating the droughtseverity that the crop might undergo. At thefield plot level, the yield index (defined as thesimulated yield relative to a fixed yield potential)depends on soil drought, mean air temperaturethat largely affects carbon assimilation throughphotosynthesis, and minimal temperature thatimpairs the yield during frost nights. At thelandscape scale, a mosaic of three land units isconsidered: cerros (steep slopes), faldas (gentleslopes in piedmonts), and pampas (flat plains). Wesimulated 2-year crop cycles taking into accountcomplementarities among these landscape units.In each land unit, growth efficiency parametersare affected by the decline in the biologicalpotential of the land. These parameters parallelthe rate of encroachment of the quinoa crop,the subsequent decline of pasture lands in the

47


pampas and the soil aeolian erosion caused by suchintensification. Results show an on-going decreasein the occurrence of frost that will be followed byan increasing drought frequency in the forthcom-ing decades. Long-term increase in soil drynessassociated with a decline in the biological potentialof the land may largely impair the sustainabilityof this area. This type of analysis, althoughspeculative, provides insights that can assistresearch and development organizations targetoptions for sustainability in crop production.

INTRODUCTION

The Andes are the most densely populatedhighlands in the world, with human settle-ments commonly found above 3800 masl andagricultural activities up to 4200 masl (Little1982). GCMs suggest that climatic changesin the Andean Altiplano might have seriousconsequences for water management and localagriculture (Thibeault et al. 2010; Seth et al.2010). Some climate scenarios even project thatthe montane climate currently known in theAndean region would disappear by the end ofthe twenty-first century (Williams et al. 2007).Specifically, climate analyses suggest that thewarming observed in the Andean highlands islikely to accelerate in the coming decades at arate greatly exceeding that of the surroundinglowlands (Vergara et al. 2007). Paradoxically, thisclimate warming would not necessarily lead to adecrease in the number of frost days (Thibeaultet al. 2010). There is more uncertainty withprojections on precipitation, but trends suggestan evolution toward a shorter, more intensewet season with less precipitation in spring(September–November) and more in summer(January–March) (Seth et al. 2010).

While our understanding of glacier retreatand its consequences has significantly improved(Vuille et al. 2008), assessing the vulnerabilityof Andean agricultural lands to the continuingclimate change requires more specific studies, inparticular the interactions between climate andland-use changes and their combined impacts on

the economic yield of indigenous crop species(Valdivia et al. 2010).

Among the Andean crops, quinoa (Chenop-odium quinoa Willd.) is an interesting casedue to the huge expansion of its cultivation inthe southern Altiplano of Bolivia, at the sametime that the impacts of climate warming areobserved in the region. Over the past 40 years,the southern Altiplano of Bolivia has become thefirst region to export quinoa worldwide. Quinoahas transitioned from an auto subsistence graincrop, limited mostly to small fields on slopes(a traditional frost avoiding strategy), to a com-mercial product cultivated over extended areasin the flat plains amenable to mechanization.In this arid region, quinoa is cultivated underrain-fed conditions and low plant density in fieldsthat, since the 1970s, have rapidly encroachedon pasture lands of native herb and shrubvegetation in the plains. It is estimated thatthe land surface dedicated to quinoa crop inBolivia has increased more than 230% between1980 and 1990 (FAO-Stat), most of this increasecorresponding to newly cultivated plains in thesouthern Altiplano. Quinoa grain yield, withan average value of 600 kg/ha in the region, isnotably unstable, due to harsh cropping condi-tions (Garcia et al. 2004; Geerts et al. 2009). Whatwould the quinoa grain yield become through thetwenty-first century under the projected trendsof increasing climate instability and expandingcrop land area?

Regional climate scenarios and crop modelingare useful tools to answer such a question, helpinganticipate agroclimatic risks and prepare adap-tation strategies that could reduce agriculturalvulnerability under climate and land-use changes(Hertel et al. 2010; Parry and Livermore 2002).After a brief presentation of the southern Alti-plano region, this chapter describes the methodsused to analyze the climatic risks affecting thestudy area as well as the climatic trends derivedfrom the current observations and GCM pro-jections. The subsequent section introduces theyield index approach, the water balance model,and the land-use scenarios applied to scale quinoaproductivity up to the landscape level. Resultssummarize the current and projected drought

Trends in Quinoa Yield over the Southern Bolivian Altiplano: Lessons from Climate 49

and frost limitations over the study area andshow the subsequent effects on quinoa yield atthe plot and the landscape levels at varying timepoints. From this, a picture of future quinoa cropproduction in the southern Altiplano can be seen,and adaptation options for a sustainable use oflocal land resources are discussed.

MATERIALS AND METHODS

The study area

The study area consists of highlands (Altiplano)located at the southwestern part of the Bolivianterritory, at the borders with Argentina and Chile.This region, bordered on its eastern and westernedges by the Andean cordilleras, is characterizedby the presence at its center of a ca. 100× 100 kmdry salt expanse, the salar of Uyuni, whereasa smaller salt lake, the salar of Coipasa, lies atits northern edge. Except for the vast salt lakeareas, the landscapes in this region show a mosaicof three types of land units: relatively extendedflat plains at an altitude of ca. 3650 masl, andan alternation of volcanic slopes and valleys inthe hinterland. The native vegetation of thistropical highland ecosystem, also known as puna,consists of a mountain steppe of herbaceous andshrub species traditionally used for extensivegrazing of llama and sheep herds. The southernAltiplano has an arid climate, with an annual meanprecipitation varying between 100 and 350 mmfrom the south to the north of the salar of Uyuni.Most of the precipitation (>70%) occurs duringaustral summer (December–January–February),when mid- and upper-level easterly winds bringmoist air that feed convective storms over theplateau (Garreaud 2000; Falvey and Garreaud2005). Summer precipitations exhibit significantsynoptic variations, largely explained by bothlocal boundary layer moisture and zonal windaloft (Garreaud and Aceituno 2001). The rest ofthe year, the Altiplano is influenced by a mid-levelwesterly flow that brings very dry air from thePacific and rare precipitation events (Vuilleand Ammann 1997). Between-year variationsin rainfall over this area may be explained by a

tendency for more precipitation during La Niñaand less during El Niño events (Ronchail andGallaire 2006), although the connection betweenthe rainfall regime and the El Niño SouthernOscillation (ENSO) still remains unclear (Gar-reaud et al. 2009; Thibeault et al. 2012; Seileret al. 2013).

Mean annual air temperature is about +9∘C,with daily thermal amplitudes much higherthan seasonal ones and radiative night frostoccurring virtually in any season. Frost risks for astandard temperature threshold of 0∘C have beendetailed by Pouteau et al. (2011). These authorsdemonstrated the nested effects of physiographicfactors across scales in this mountain area. Resultsshowed prominent effects of elevation, latitude,and salt lake proximity at regional scale, whereasslope, topographic convergence, and insulationhad more influence at local scales. As a result, theshores of the salt lakes appear less prone to frost,whereas highlands at the west and south of theregion are continuously exposed.

Recent past and present climate

We used the Standardized Precipitation Evapo-transpiration Index (SPEI), which is a site-specificdrought metric that quantifies deviations fromthe average water balance. The SPEI is cal-culated by means of a climate water balance,that is, the difference between precipitationand potential evapotranspiration, at monthlytime intervals. Different SPEIs are obtainedfor different time windows representing thecumulative water balance over the previousmonths (Vicente-Serrano et al. 2013). Monthlyclimate data at high-resolution 0.5 × 0.5 degreegrids for the study area are provided by theClimate Research Unit (CRU) of the Universityof East Anglia (United Kingdom). We used theCRU TS3.1 datasets for the period 1901–2009.Three time-windows of 3, 6, and 24 months wereretained for the analysis. The first time-window(SPEI3) is related to the top soil water limitationthat could impair the seedling stage, the second(SPEI6) is related to the whole productivity ofthe crop, and the last and longer one (SPEI24) isassociated with the availability of rain from the


previous year in the subsoil. Within a 2-year rota-tion, quinoa crop uses water stored in the subsoilduring the previous fallow year. If this additionalsoil water is insufficient, quinoa productivitymay be drastically impacted. We retain a value ofSPEI less than −1 lasting more than 3 monthsas a drought threshold for any time-window(3, 6, or 24 months). For the frequency analysisof drought events, we cut the whole sequenceinto three successive 36-year periods: 1901–1936,1937–1972, and 1973–2009.

Source of climate scenarios

We used climate scenarios from the Centre deRecherches Météorologiques Coupled GlobalClimate Model version 3 (CNRM-CM3). It isbased on the coupling of the ARPEGE-ClimateAtmospheric Global Climate Model, an oceanicGeneral Circulation Model OPA8.1, a sea icemodel GELATO2, and TRIP, a river routingscheme. CNRM-CM3 has been applied in theframework of the fourth assessment reportof the Intergovernmental Panel on ClimateChange (IPCC). We retained the IPCC-SRESA1B simulations for the twenty-first centurythat provided daily precipitation, minimal andmaximal temperatures, and global radiation forthree time-slices: 1960–2000, 2046–2065, and2081–2100. We used a coarse resolution of 2.5× 2.5∘ grid, which is a good compromise as itdoes not affect the large-scale patterns and allowsa reasonable level of regional description overSouth America (Boulanger et al. 2006, 2007).

Simulating the yield index at local or plotscale

We defined three abiotic limitation factors thatmay impair crop productivity and yield at a dailytime step: a soil water limitation factor, f1, whichwill be discussed in more detail further on; a limi-tation factor for carbon assimilation, f2, related tothe within-day variations of air temperature; anda frost limitation factor, f3, exponentially relatedto the minimal temperature. All these factorshave values ranging between 0 and 1, and theirproduct calculated over the entire growth period

(from early November to late March) defines thepotential yield index:

YIplot =∑

f3

∑

growth period

f1 f2Δt (4.1)

YIplot = 1 means that no limitation has beenobserved during the whole growth period.

For calculating f2, it was considered that,within a given day, the pattern of change of airtemperature follows two sinusoidal segments:first, a decline from the maximal value thatoccurred at 2 pm to the next minimal valuethat was observed at dawn; second, the increaseof air temperature from its minimal value tothe maximal 1. The theoretical duration of thedaylight period, d, was calculated for the latitudeof the study area using Milankovitch’s equation.Relative instantaneous carbon assimilation, Ar,follows a parabolic pattern with current time airtemperature, Ta, reaching a maximum (Ar = 1) atan optimal temperature of Topt:

Ar = 1 − α(Ta − Topt)2 (4.2)

with α being a thermal efficiency coefficient.The f2 factor was then calculated as

f2 = 1∕d∑

d

Ar Δt (4.3)

The f3 factor affects sequentially the yield(Eq. 4.1), quantifying the percent yield loss dueto frost. This factor is exponentially related tothe minimal daily temperature and scaled by avulnerability parameter. The vulnerability scalingparameter was fitted to produce realistic losses inthe recent period and was applied further to thewhole period.

The soil water balance model

The water balance of the top soil layer was simu-lated at a daily time step using a bucket-type modelwith a limited storage capacity and mathematicallyrepresented by a difference equation in which thedaily change in soil water storage, ΔS, equals raininput, R, minus outputs that are deep drainage, D,and actual evaporation, AET:

ΔS = R–AET–D (4.4)


Maximum stored water in the soil, S, is limitedby the field capacity, FC. When the soil waterstorage exceeds the field capacity threshold,extra water flows down as deep drainage. Actualevaporation AET extracts water from the soilcompartment. AET is a fraction of potentialevaporation PET, related to both the amountof stored water in the soil and to PET itself.PET was calculated using Priestley–Taylor’sequation (1972). Daily PET values were cal-ibrated for our regional applications with astandard Priestley–Taylor parameter of 1.26 thatcorresponds to the original equation (Geerts et al.2007, 2009). The net all-wave radiation term wasrelated to global incoming short-wave radiationusing Kalma et al.’s equation (2000) calibratedwith unpublished measurements over quinoafield. For reducing PET to AET, Linacre (1973)proposed a simplified algorithm: AET rate equalswhichever is the less of (i) the PET rate or (ii)β(S∕FC)2. Finally, the model may be summarizedby two coupled equations:

AET = min[β(S∕FC)2

,PET]

(4.5)

S(t + 1) = min[S(t) + R − AET,FC] (4.6)

β is fixed to 4.5 mm, a value slightly lower thanthe one retained in this area by Geerts et al.(2006). Retention properties of the sandy soilthat covers the study area have been derivedfrom Saxton et al. (1986). Percent sand rangesfrom 76% to 81% and clay fraction from 6%to 7%. Depending on the soil texture, fieldcapacity may be estimated to extend from 0.153to 0.167 cm3 H2O/cm3 soil, corresponding to thewater content reached at a soil water potentialof −0.02 MPa. The water content at wiltingpoint ranged from 0.067 to 0.074 cm3 H2O/cm3

soil. For modeling purposes, we retained asoil layer of 0.50 m depth with a 75 mm fieldcapacity and 37.5 mm storage at wilting point.For well-watered conditions, when S ranges fromfield capacity to a relative soil water content of0.8, f1 = 1 and then declines linearly down to 0 atwilting point.

Scenarios of land-use/land-cover changes

The whole land area potentially suitable forquinoa crops can be classified into three neigh-boring land units: cerros, faldas, and pampas. Thehilly cerros correspond to the higher altitudeareas cultivated manually and hardly affectedby night frosts. The pampas, previously usedfor livestock grazing, are now undergoing rapidcropping intensification. The faldas correspondto the transition area between cerros and pampas.The area of fallow lands equal that of crop landsin this arid region, as a result of 2-year croppingcycles. This “dry farming” practice, as well as theclump (pocket) sowing, is typical of local quinoafields. With this practice, for a given plot, thesoil is maintained bare the first year so rain watercan infiltrate the soil and will be used for thesubsequent cultivation year. We considered that,on average, the partitioning of the whole areasuitable for cultivation over the study area wouldbe 10% cerros, 20% faldas, and 70% pampas.

Scenarios of land-use/land-cover (LULC)changes came from maps derived from aerialphotographs taken in 1963, high-resolution scansof digital photographic data from the US geolog-ical survey of 1972, and high-resolution remotelysensed data from 1990 and 2005. Interpretationswere validated by ground truth observations onsampled areas. Five communities representativeof the study area were mapped since 1963: Cha-coma, Chilalo, Kapura, Palaya, and Otuyo. Forthe more recent period, we used SPOT satellitedata recorded in 1998, 1999, 2005, and 2007 over14 communities: Alianza, Cacohota, Cacoma,Chilaco, Chusiquiri, Colcaya, Irpani, Jirira, Lia,Otuyo, Pastos Lobo, Salinas, Tahua, and Vituyo.Results obtained at the community-level wereaggregated in three trajectories for each land unitexpressed in percent changes of the suitable areaand then extrapolated toward 2040.

Scaling local yield index up to the region

For all the simulations at plot scale, we assumedthat land use did not change over the consideredperiod.


The yield index at regional scale YIregiondepends on both LULC and “growth efficiency”parameters related to the biological potential ofthe land (detailed further):

YIregion =∑

i=1,3

εikiYIplot (4.7)

This regional yield index thus includes thetime changes of percent area ki and the changes inthe biological potential εi in the three land unitsconsidered over the entire region. We furtherapplied the same changes for faldas and pampasand assumed no change in growth efficiency forcerro. For faldas and pampas, the change wasrelated to the ratio of areas devoted to cultivationand those supporting pastures. We assumedthat the growth efficiency was not affected andmaintained equal to 1 until the pasture/cropratio is lower than 10, after that it declinedslowly to a new equilibrium. It reached 0.4 forpasture/crop ratios lower than 1. The fallow areasare considered independently in our simulation.

RESULTS

Drought history over the area

The time course of SPEI values over time is pre-sented in Fig. 4.1. Main results are summarizedin Table 4.1, and highlight (i) the frequency ofdrought events, (ii) their month of onset withinthe year, and (iii) their duration.

Over the whole 1901–2009 period, we observedan increase in the frequency of short droughtsquantified by SPEI3 with return periods of 4years in the last two time-slices. The overallreturn period is 4.9 years because we observedonly four events in the first time-slice with acorresponding return period of 9 years. The mostfrequent period when drought begins to occurwas December–January in the first time-slice.Progressively, this drought onset occurred laterin the wet season. This pattern of change wasobserved whatever the time-window (3, 6, or24 months) used for the SPEI calculation. Aninteresting result concerns the drought duration,which increased slightly with time from 3 to 6months with SPEI3. This pattern of change was

maintained for SPEI6 with a significant lineartrend of 0.89 month per decade that increased thedrought duration from 4 months at the beginningof the series to 13 months at its end. For SPEI24,the whole return period was 6.4 years with slightlyhigher frequency within 1936–1972 that hadseven drought events. The drought durationincreased with time with 7.0± 3.4, 8.1± 5.4,and 17.2± 13.6 years for the three time-slices,respectively. The most severe and long droughtswere observed in 1983 and 1992 with durations of28 and 33 months, respectively.

Climate projections and soil droughtlimitation

In our climate scenario, if we compare 1981–2000to 1961–1980 used as baseline, the on-goingwarming trends were 0.24 and 0.35∘C per decadefor minimal and maximal air temperatures,respectively. For the near future, we projectedan increase of 2.1 and 4.0∘C in the 2046–2065time-slice and 3.0 and 5.1∘C in the 2081–2100time-slice (Table 4.2) for minimal and maximalair temperatures, respectively. Direct results onthe amount of rain are not presented because weprefer to highlight their effects on the soil waterregime, thus answering the question: “how do thechange of the rain regime and the concomitantincrease of potential evaporation modify theavailability of soil water for quinoa crops?”

The seasonal pattern of the soil water storagedisplays three distinct phases (Fig. 4.2). Thefirst phase corresponds to a well-watered periodwith soil water storage S greater than 40 mmand no significant negative impact on the cropyield. It includes the period from March to earlyMay. Furthermore, the dry period begins in lateMay and ends mid-November with soil waterstorage lower than the wilting point. Finally, wecould consider the period from late Novemberto January as a transition period. This period ischaracterized by both a reduced amount of storedwater and a large between-year variation. Thistransition period corresponds to the onset of therainy season and the establishment of the crop, agrowth stage crucial for the final crop yield.


–4

–2

0

2

4

–4

–2

0

2

4

0

2

4

1950 20001900–4

–2SP

EI2

4S

PE

I6S

PE

I3

Fig. 4.1 Drought evolution from 1901 to 2009 on different timescales as assessed by the SPEIs. The series represents the evo-lution of the SPEIs with time-windows of 3, 6, and 24 months. Dry periods display negative SPEI values and humid ones havepositive SPEI values. The dotted lines at SPEI = 1 show the threshold value defining a moderate drought.

Table 4.1 Summary of results obtained by analyzing the Standardized Precipitation Evapotranspiration Index (SPEI) with threetime-windows of 3, 6, and 24 months.

SPEI3 F Return period (RP) = 4.9 years, larger RP for 1901–1936 with only four dry events, against nine eventsin the second and third time-slices

O The drought onset was observed earlier (December–January) at the beginning of the series andprogressively occurred later

D No significant increase of drought duration (D) but longer events in the second and third time-slices(3; 4.2± 1.7; 6± 5.3 months)

SPEI6 F RP = 6.4 years; lower RP (5.1 years) from 1936 to 1972 with seven eventsO Same pattern of change as for SPEI3D Significant increase of D with time (0.89 month each 10 years)

SPEI24 F RP = 6.4 years; shorter RP (4.5 years) from 1936 to 1972 with seven eventsO Same pattern of change as for SPEI3 and SPEI6D Significant increase of D in the third time-slice (7.0± 3.4; 8.1± 5.4; 17.2± 13.6 years); very severe

drought events in 1983 and 1992, when D = 28 and 33 months, respectively

The SPEI threshold value retained for defining a moderate drought is −1. F refers to the frequency of drought events in year, Ocorresponds to the month of the onset of the drought period, and D is the drought duration in months.

For the three time-slices that follow1961–1980, we did not observe any signifi-cant change in the soil water storage pattern(Fig. 4.3). However, the transition period showed

a decline in S for values lower than 40 mm. Atthis level of soil water storage, correspondingto relative water contents ranging from 0.6to 0.8, the impact of soil drought on carbon


Table 4.2 Changes over three time-slices from 1981 to 2100 in yearly averages ±SD ofminimal tn , maximal tx air temperatures, and drought duration DD with soil water storagelower than the wilting point, relative to the control period (1961–1980) retained as baseline.

Time-slice 1981–2000 2046–2065 2081–2100

Δtn +0.48± 0.11 +2.11± 0.11 +3.03± 0.13Δtx +0.69± 0.30 +4.03± 0.36 +5.05± 0.38ΔDD −1.5± 7.5 39.1± 10.9 34.9± 10.1Δf1∕f1 −1.7 −26.6 −24.4Δf2∕f2 5.8 23.3 27.1Δf3∕f3 2.5 7.3 8.1

Also reported are the relative changes of three abiotic limitations cumulated over the grow-ing season: the soil water limitation f1, the limitation of carbon assimilation related to thevariations of air temperature f2, and the frost limitation f3.

1.0

0.5

0.0Top

soi

l rel

ativ

e w

ater

con

tent

J F M A AM J J S O N DTime (month)

Fig. 4.2 Seasonal course of the daily relative soil water con-tent averaged over the second time-slice (1981–2000). Thegrey area shows the standard error.

assimilation and growth is already significant.The number of days within the growth period inwhich S is lower than the wilting point did notincrease significantly in the 1981–2000 time-slice(Table 4.2). Moreover, the number of dry daysincreased largely to 39.1± 10.9 and 34.9± 10 inthe last two time-slices, respectively. This directeffect of climate change was associated with adrastic increase in the between-year variation.

For any given day of the year, we calculated anunpredictability index based on the coefficientof variation of the soil water storage S (Fig. 4.4).In the first two time-slices, the unpredictabilityindex reached 40% at the beginning of the cropseason, in early November (Fig. 4.4). It increasedsharply to 60% in the projected time-slices(2046–2065 and 2081–2100). Thus, the expected

1.0

0.5

0.0

1961 – 19801981 – 20002046 – 20652081 – 2100

J F M A AM J J S O N D

Time (month)

Top

soi

l rel

ativ

e w

ater

con

tent

Fig. 4.3 Seasonal time courses of the daily relative soil watercontent averaged over each of the four time-slices from 1961to 2100.

consequence of this higher climate unpredictabil-ity is an extremely large between-year variation incrop yields at both field plot and landscape levelsin the near future.

Time variation of yield at local or plotscale

Initially, we analyzed how the three abiotic limi-tations changed with time. For that, we calculatedthe relative variation for each time-slice andeach limitation factor. The value observed in the1961–1980 time-slice was used as a baseline forcomparison.

The relative drought limitation quantifiedhere by Δf1∕f1 increased with time. This increase(resulting in negative values in Table 4.2) was


1961 – 19801981 – 20002046 – 20652081 – 2100

0.8

0.6

0.4

0.2

0.0

Impr

edic

tibili

ty in

dex

J F M A M J J A S O N D

Time (month)

Fig. 4.4 Seasonal time course of the daily unpredictabilityindex calculated over four time-slices from 1961 to 2100.

slight in the 1981–2000 time-slice and reachedlarger values in the last two time-slices, −26.6%and −24.4%. The positive effects of climatewarming appeared in both the carbon assimila-tion factor, f2, and the frost factor, f3. The firsteffect considerably reduced the negative droughteffect in the 1981–2000 time-slice. Furthermore,in 2046–2065 and then in 2081–2100, thispositive effect increased largely with values of23.3% and 27.1%, respectively. The cost of thefrost declined with the increase of Δf3∕f3.

The consequences of these changes in theclimate parameters on the yield index are sum-marized in Table 4.3 and Fig. 4.5. The yieldindex was calculated on a unit area basis. Ourcalculations did not include the fact that oneunit area of crop is always associated with oneunit area of fallow (this effect will be integratedin the simulation at landscape scale presentedlater). Neither did the yield simulations at plotscale consider any change in the land biologicalpotential with time. Over the recent periods, apositive effect of the warming trend facilitatedphotosynthesis and reduced the impact of frostevents. This positive linear trend was associatedwith a reduced between-year variation. Waterlimitations contributed significantly in impairingthe yield but these effects were largely counter-balanced by the increase in air temperature. In thefirst two time-slices pooled from 1961 to 2000, thepositive effect of warming had a significant effecton the quinoa yield that increased linearly by 5%per decade (Fig. 4.5). In the third time-slice, from

Table 4.3 Changes of the mean yield index at plot scaleYIplot and its standard deviation over different time-slicesfrom 1961 to 2100.

Time-slice YIplot ± SD ΔYIplot∕Δt (% per year)

1961–2000 0.31± 0.08 +0.51961–1980 0.30± 0.07 –1981–2000 0.33± 0.09 –2046–2065 0.32± 0.16 Negligible2081–2100 0.35± 0.13 −1.7

Linear trends in yield increase or decrease with time arereported for 1961–2000 and 2081–2100, respectively.

YI p

lot

0.6

0.4

0.2

0.01950 2000 2050 2100

Time

Fig. 4.5 Interannual variability of the quinoa yield index[0–1] at plot scale across the four time-slices 1961–1980,1981–2000, 2046–2065, and 2081–2100. Red lines show thetrends in each time-slice.

2046 to 2065, the mean yield would be slightlylower than the one observed during 1981–2000.Moreover, this value should be associated witha larger between-year variation reaching 50% ofthe mean. Thus, in some years, there would bevery low yields as a consequence of severe waterlimitations. It should be noted that both values ofmean and between-year variation were likely notwell estimated statistically, due to the low numberof years in the time-slices.

Keeping this caveat in mind, in the projectedfuture, the positive effect of the continued warm-ing should boost forward the potential of carbonassimilation through photosynthesis, and frostoccurrence should continue to decline drasticallyuntil its complete disappearance by the end ofthe twenty-first century (Tables 4.2 and 4.3).Despite these positive effects of climate warming,the simulated quinoa yield index remained stable


in the second time-slice, before decreasing inthe third time-slice (Fig. 4.5). In the third andlast time-slice, the between-year variation ofthe drought limitation had a greater effect thanboth warming factors f2 and f3. At the field plotscale, this resulted in a negative trend for cropproductivity, with an average decline in quinoayield of 17% per decade.

Model results at landscape level

From 1960 onward, the increase of cultivatedarea had been characterized by a slow exponentialincrease with an average doubling time of 20years in the five communities sampled. For thecurrent period, there was an exponential increasein the cultivated area remotely evaluated over1998–2007 on 14 communities. The doublingtime was about 10 years. This means that, onaverage, the cultivated area increased twofold overa decade. In some communities, such as Otuyo orLia, this area increased more than threefold, withdoubling times of 5.5 and 6.2 years, respectively.Communities with limited suitable crop area haddoubling time that may reach 40 years, suggestinga saturation level. For 1980, we estimated thepercent suitable crop area covered by quinoato be 9.5, 5.5, and 6% in cerros, faldas, andpampas, respectively. In 2000, these percent areasdecreased to 7.5% in cerros but increased to 7.9%and 25% in faldas and pampas. Finally, for the year2040, the projected areas covered by the quinoacrop are 5%, 27%, and 50% for cerros, faldas, andpampas, respectively. The projected time changefor this last land unit is presented in Fig. 4.6a.

We extrapolated toward 2040 a drastic declineof the pasture lands so that by the end of theperiod, a suitable area in the pampas is composedof about 50% in crop and 50% fallow. Figure 4.6band c shows the resulting extrapolations for thewhole area with a decline of quinoa crop in cerros,a slight increase in faldas, and an exponentialincrease in pampas.

The consequences of these LULC changesand those associated with the change in the landbiological potential for the yield index are plottedin Fig. 4.7. Pooling faldas and pampas together,we simulated first a sharp increase in the yieldindex. This is related to the rapid encroachmentof quinoa in the pampas and also to the positivewarming effect and to a nonsignificant change

0.08

0.06

0.04

0.02

0.00

Who

le-a

rea

yiel

d in

dex

1950 2000 2050 2100Time

Cerro

Pampa + Falda

Fig. 4.7 Time course of the quinoa yield index at landscapescale across the four time-slices 1961–1980, 1981–2000,2046–2065, and 2081–2100. Values corresponding to faldaand pampa (grey circles) are pooled and displayed separatelyfrom those corresponding to cerro (white circles). The trends(red line and red dotted line) have been calculated with splinecurves.

(a)

Per

cent

sui

tabl

e ar

ea 0.8

0.4

0.0

0.8

0.4

0.0

0.4

0.2

0.00 20 40 60 80

(b)

0 20 40 60 80

(c)

0 20 40 60 80

PastureFallow

Crop

Time since 1960

PampaFalda

TotalCerro

PampaFalda

TotalCerro

Fig. 4.6 Scenarios of land use and land cover changes used in our simulations. (a) The drastic land use change in the pampa landunit with projected crop cover reaching 50% of the suitable area at the 2040 horizon. (b) The change in the crop area aggregatedfor the whole study area, showing a sharp increase in the pampas, a moderate increase in the faldas, and a slight decline in thecerros. (c) Decline in the percent area devoted to pasture in the different land units.


in water limitation. In the second and thirdtime-slices, we simulated primarily a decline inthe average quinoa yield but with especially largebetween-year variations. In the cerros, the yieldfollows the decline of the cropped area with anenlargement of the between-year variations inboth remote time-slices.

DISCUSSION

It is commonly accepted that drought is amulti-scalar phenomenon as the periods whensoil water limitations impact the various com-ponents of crop productivity distinctly differ.Drought is a phenomenon that may occur simul-taneously across various timescales, for example,a short period of particular dryness embeddedwithin longer-term droughts. The SPEI resultshighlight the limit of a drought metric based ononly potential evaporation and rainfall amountsat monthly scale compared to results based onthe simulation of a soil water balance modeldriven by daily values of climate parametersand particularly of rains. However, for all thetime-windows we retained (3, 6, and 24 months),we found a decrease of the return period ofdrought events, a change in the onset of theseevents toward a shortening of the wet season, andan increase of their duration. All these changesappeared particularly accelerated in the recentperiod (1973–2009). Air warming was observedespecially since the year 1980 and onward, andthe associated air dryness increased the potentialevaporation. Thus, both the increase in PETand the slight decline in the amount of the rain(Vuille et al. 2003; Bradley et al. 2006) drasticallymodified the climate water balance toward morefrequent and severe droughts. The occurrenceof large drought periods in 1983 and 1992, withdurations of 28 and 33 months, respectively, mayin some ways presage the future climate. Moraleset al. (2012) stated that “a high concentration ofextreme dry events has occurred during the last70 years with four of the 12 driest years since AD1300.”

There is a large sphere of uncertainty associ-ated with climate projections, and unknown forces

in the future may affect the composition of theatmosphere and feedbacks from the land surface.Over the next three decades, projections of globalmean temperature rise are largely insensitive tocontrasted emission scenarios. Nevertheless, itis clear that present and future predictability ofclimate variations and change is not the sameeverywhere and that gaps in knowledge arerevealed by a lack of agreement between climatemodels in some regions, including projections ofrainfall patterns over large areas of South America(Rada et al. 1997; Boulanger et al. 2007). The Alti-plano region is poorly resolved in current GCMs,given their coarse resolution relative to thenarrowness of the Andean cordilleras. Not sur-prisingly, direct analysis of GCM outputs resultsin slight precipitation decline or increase overthe Altiplano, in contrast with a robust warmingtrend expected for the rest of the twenty-firstcentury and already fully documented since 1980onward. Glaciological studies have shown that thetemperature in the tropical Andean cordillera hasrisen between 0.10 and 0.11∘C per decade since1939 and the ongoing warming trends rangedbetween 0.32 and 0.34∘C per decade from 1974to 1998 (Vuille and Bradley 2000). In our climatescenario, the observed warming trends werepoorly represented if we compare 1981–2000to the baseline data of 1960–1980. However, forthe next time-slices, we projected an increase of2.1 and 4.0∘C in 2046–2065 and 3.0 and 5.1∘Cin 2081–2100 for both minimal and maximal airtemperatures. According to other GCM runs,temperatures are likely to increase in the range1.3–1.6∘C by the year 2030 and between 4.8 and6∘C by the year 2100 (Garreaud et al. 2009).

A compendium of results from GCM runs isambiguous about rain projections (Vuille et al.2003; Urrutia and Vuille 2009; Seth et al. 2010;Thibeault et al. 2012). To circumvent the problemwith rain projections, Minvielle and Garreaud(2011) proposed an interesting scheme andexploited a rather strong relationship betweenmid-tropospheric zonal winds and precipitationover the central Andes to project changes inregional rainfall by the end of the twenty-firstcentury. Owing to a projected weaker easterly flow,the central Andes will likely exhibit a decrease


in precipitation toward the end of the centurythat, when averaged over all stations, could reach15.3 mm/month for the A1B scenario, using1948–2007 as baseline. In our simulations, theincrease of PET with the concomitant slightdecrease in the amount of rain and change in theirdistribution induces large between-year variationof the quinoa crop yield and a significant declineof this yield in the remote time-slice 2081–2100.

Reynolds et al. (2004) conducted a compre-hensive simulation analysis to explore how plantsrespond to variations in amounts of rain and avail-ability of soil water in areas with limited water.They concluded that the so-called pulse-reservemodel, which relates plant productivity linearlyto annual precipitation as in rain-use efficiencyapproaches (Le Houérou and Hoste 1977; Hux-man et al. 2004), is inadequate. Our simulationresults showed that rainfall characteristics (e.g.,seasonality, frequency, and intensity of rainevents) and their consequences on availabilityof soil water are important for plant growth,and notably crucial for quinoa growth (Geertset al. 2006). Rainfall seasonality is a singularlyimportant driving variable, as it accounts formuch of the difference among water-limited areasand is likely to be quite sensitive to the on-goingglobal climate change already observed over thesouthern Altiplano (Thibeault et al. 2010). Smallchanges in seasonality could drastically impactquinoa yield.

In the context of crop productivity, theso-called land degradation results from a mis-match between land quality and land use. Ratherthan retaining disciplinary-oriented meanings,which could be prone to misinterpretation amongdisciplines, we prefer to use the idea of decline inthe land biological potential. While there is a cleardistinction between soil and land, the term “land”refers to an ecosystem perspective comprisingsoil, landscape, terrain, vegetation, and climate.Mechanisms that initiate decline in biologicalpotential include physical and biological pro-cesses. Important among physical processes area change in soil properties leading to erosion,desertification, and unsustainable use of naturalresources (see Reynolds et al. 2007 for a surveyincluding our study area). Biological processes

include reduction in total and biomass carbon,fertility depletion, and decline in biodiversity. Atleast two distinct schools of thought have emergedregarding the prediction, severity, and impact ofhypothetical land degradation on productivity.One school of thought believes that it is a seriousthreat posing a major challenge to humans interms of its adverse impact on crop productivityand environment quality. Most ecologists, soilscientists, and agronomists primarily supportthis argument. The second school of thought,propounded primarily by economists, asks why, ifdecline in the biological potential of land is such asevere issue, market forces have not taken care ofit? Supporters argue that producers have vestedinterest in their land and will not let it degrade toa point that would be detrimental to their profits.There are a number of factors that perpetuatethis debate as illustrated by Jacobsen (2011) andWinkel et al. (2012).

In the what-if exercise presented here, weadopt a neutral conservative position by whicha lumped metric is included for describing adecline in the biological potential of land. In thismetric, both physical and biological factors areaggregated in one continuously changing growthefficiency parameter. Thus, we do not retain thediscrete terminology used by specialists, whopropose terms such as “slight,” “moderate,”“severe,” and “very severe” to quantify the sever-ity of soil degradation (Lal 1997). Others haveused the terms “light,” “moderate,” “strong,”and “extreme.” All of these terms are difficult tocompare. Our continuously changing parameterparallels the rate of encroachment of the recentand rapid expansion of the quinoa crop and thesubsequent decline of the pampas. This expansionis done through agricultural intensification, andbased mainly on the mechanization of tillage andseed sowing operations. The mechanization ofthese processes causes a measurable yield declineat plot scale. The reasons for this include poorseedbed preparation and very irregular seedlingemergence, resulting in low plant density com-pared to fields with traditional manual practices,as those maintained in the cerros. Additionally,soil aeolian erosion has also been observed inthis area. This constitutes an objective warning


indicator often associated with the burial ofyoung seedlings during wind storms and thedecline in fertility in sandy soils under aridclimatic conditions. The decline in soil fertilityafter conversion of virgin land to agriculturehas been fully documented (Fonte et al. 2012)and typically shows two successive phases: amore or less fast decrease in the first years undercultivation, followed by a new equilibrium. Alarge socioeconomic survey conducted in a wetterpart of the Altiplano revealed the importance offallow and tillage practices in the soil nutrientloss processes and erosion (Swinton and Quiroz2003). This study also showed that the probabilityof a farm experiencing soil nutrient loss over thepast 20 years depended on natural factors andalso on both the social context and the agricul-tural management practices. The probability ofnutrient depletion increases in sandy soils (Fonteet al. 2012). To sustain soil fertility despite theexpansion of the quinoa crop, it is recommendedthat llama dung be incorporated in the soil, albeitan uncommon practice in the traditional autosub-sistence cropping system. This organic resourceis the only (if ever) nutrient input applied inthis region and it is largely dependent of thepampas and the livestock it supports. However,the beneficial effects of animal manure and, moregenerally, the effective importance of nutrientavailability in the soil are still poorly documentedin quinoa (Cárdenas and Choque 2008). A majorshortcoming is the lack of clear cause–effectrelationship between soil fertilization and cropproductivity in this particular agrosystem. Thisis hampered by the observation that inferiorsoil physical structure or low water availability,both caused by poor seedbed conditions, mightinterfere with nutrient availability. In turn, lownutrient availability causes low plant density andlow grain yield in mechanized field plots. In fact,assessing the relative effects of soil water, soilnutrients, and soil structure on quinoa produc-tivity still remains a challenging task, the same asevaluating the benefit/cost of the various optionsfor crop fertilization in this agricultural system.

In our yield simulations at plot scale, withoutchanges in the biological potential of the land,we observed over the recent past time-slices

(1961–1980 and 1981–2000) a positive effectof the climate warming trend that facilitatedcarbon assimilation and reduced the cost of frostoccurrence. This positive linear trend was alsoassociated with a reduced between-year variation.Water limitations contributed significantly indiminishing the yield but these effects weremostly counterbalanced by the warming trend.In the two near future time-slices, we observeda saturation of the crop yield followed by asharp linear decline. To scale these results upto the landscape level, we took into account theassumption that fallow areas equal the crop areas,a scenario of LULC change extrapolated fromchanges observed at present, and a decline in thebiological potential of land. This decline has beendiscussed previously. At the regional scale, themain result is a potential decline in yield from2020 onward, despite the continued saturation ofthe suitable crop area toward 2040. By the end ofour simulation, the average regional yield wouldbe half of the yield obtained at peak productionlevels.

In our landscape, there are many reasons, likelyconfounding, why smallholders let the biologicalpotential of their land decline. Some of thesereasons relate to the values that local societiesplace on land resources and their perception ofthe present vulnerability of these resources. Whileagronomists and development agents see the soilas a nonrenewable resource, this is not necessarilythe case for local farmers (Zimmerer 1993, 1994).In the end, the sustainable use of the soil andland resources will lie in the hands of the farmersthemselves who are subject to economic andsocial pressures from both the community andthe market within which they operate (Swintonand Quiroz 2003). Ongoing changes in climaticconditions, crop productivity, and land biologicalpotential are strongly interrelated and each mustbe addressed in the context of the others for acorrect assessment of its impact (Valdivia et al.2010). This is the challenge for the near future,and for which we must be prepared. A study onnatural ecosystems in the northern part of theAltiplano warns again an “Andean tipping point”for climate (Bush et al. 2010). This seems tocorroborate the climate projections at regional


scale that predict the Andean climate to disappearby the end of the twenty-first century (Williamset al. 2007).

We could question the use of speculativeexercises. Testing model simulations against fieldobservations and other model simulations is onlypart of the model validation process, and a goodagreement between simulated and measuredvalues alone does not guarantee the correctnessof using model projections (Geerts et al. 2007,2009; Lebonvallet 2008). To make further use ofthis approach in diverse ecological situations andhierarchies of scales, three challenges must beovercome. First, additional processes associatedwith land-use practices and decline in landbiological potential need to be incorporated.Second, appropriate spatially explicit simulationapproaches and scaling methods should beused to link landscape patterns and processes atmultiple spatial scales (e.g., local spot, landscape,and whole region). Correspondingly, multilayerspatial datasets need to be developed and con-tinuously updated (see Pouteau et al. 2011 fora significant account on frost mapping). Third,variables that show large changes associated withclimate, for example, warming trends and changein rainfall patterns, should be manipulated infield experiments to evaluate their effects onland productivity. Our results show that suchnumerical experiments are likely to provide astrong and realistic set of predictions with whichto compare actual long-term change in a rapidlychanging region. Thus, this study provides abasis for further investigating how abiotic andbiotic environmental changes influence quinoayield. Another arising problem is our limitedunderstanding of what the local-level impacts ofclimate change on crop yield are likely to be. Thisrelates to the uncertainties involved in GCMoutputs at the high spatial resolutions neededfor an effective application of such type of work(Challinor et al. 2005; Watson and Challinor2013). While there are still substantial gaps in ourcurrent knowledge and techniques, significantopportunities do exist for improving the produc-tion and evaluation of higher-resolution climatechange scenarios, as illustrated by the work ofBuytaert et al. (2010). Despite its limitations, the

type of analysis presented here should be able toprovide some insights to help research and devel-opment organizations target adaptation optionsfor a sustainable use of local land resources.

ACKNOWLEDGMENTS

This chapter is a tribute to Jean-Pierre Ratte whopassed away in 2011. The authors acknowledge thework of Roland Bosseno of the IRD (Institut deRecherche pour le Développement) for land-usechange analyses on SPOT images. Thanks also toD. Salas-Mélia from the CNRM (Centre Nationalde la Recherche Météorologique) Meteo Francefor climate scenarios. This study was carriedout with the financial support of the “ANR-Agence Nationale de la Recherche - The FrenchNational Research Agency” under the program“Agriculture et Développement Durable,” project“ANR-06-PADD-011-EQUECO.”

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http://dx.doi.org/10.1073/

Chapter 5

The Potential of Using Natural Enemiesand Chemical Compounds in Quinoa for

Biological Control of Insect Pests

Mariana Valoy1, Carmen Reguilón2, and Griselda Podazza1

1Instituto de Ecología, Fundación Miguel Lillo, Tucumán, Argentina2Instituto de Entomología, Fundación Miguel Lillo, Tucumán, Argentina

INTRODUCTION

Over the centuries, agriculture has transformednatural landscapes into agricultural landscapes,and modified not only plant diversity but alsoanimal diversity, including insect diversity.Insect life depends on plant populations, asthey feed, reproduce, oviposit, and shelter inplants. Changes in the structure and diversity ofvegetation, land use, cultivated area, type of cropmanagement, physical environment, and otherfactors influence the behavior of insects, turningmany of them into agricultural pests.

Agricultural intensification is one of the factorsthat modify an ecosystem’s ability to managepest populations by means of natural enemies(Altieri and Letourneau 1982; Oerke et al.1994; Matson et al. 1997; Wilby and Thomas2002; Bianchi et al. 2006; Parsa 2010). Thereare three hypotheses regarding the influence ofagricultural intensification on pest populationsand their natural enemies. First, with agriculturalintensification, natural enemy populations aredecimated by pesticides and/or decreased by thesimplification of local ecosystem structures andlandscapes driven by reduction of plant diversity(DeBach and Rosen 1991; Andow 1991; Bianchi


et al. 2006). Second, crop intensification alsocontributes to the increase and persistence ofpests by providing concentrated resources andan optimal environment for insects (Root 1973).Third, crop intensification entails the use ofinsecticides and techniques to enhance produc-tivity, ultimately weakening plant defenses againstherbivores (Harris 1980; Throop and Lerdau2004). In this context, it has been proposed thatecological knowledge, conservation, and handlingof biotic interactions (Médiène et al. 2011) areessential elements for reducing chemical use andpromoting ecosystem services, thereby slowingdown the loss of diversity in agroecosystems(Robinson and Sutherland 2002; Benton et al.2003; Bianchi et al. 2006; Farwig et al. 2009).

Since ancient times, Andean agroecosystemshave had a wide variety of cultivated species(Kraljevic 2006). Among these species, theAndean grains stand out, of which quinoa(Chenopodium quinoa Willd.) is one of the mostrepresentative species. Traditionally, quinoa cul-tivation has been intended for local consumption,with long periods of fallow land. In cultivatedareas, direct sowing, manure application, thresh-ing, and cleaning were all performed manually(Jacobsen 2011). This type of subsistence

63


agriculture was characterized by covering a smallarea of cultivated land and sowing seed in moun-tain slopes. However, due to the high internationaldemand for quinoa (Jacobsen 2011), its cultiva-tion has been extended to the plains. This marksthe beginning of a semi-intensive agriculture,going from a crop rotation system, which is akey component for sustainable agriculture, to amarked tendency toward intensified monoculture(CIRNMA 2009).

The intensification of quinoa production hasalso increased pests and diseases and is hasteningsoil deterioration to the detriment of the environ-ment and sustainability of the quinoa crop itself(Mujica 1993; Campos et al. 2012).

A study assessed the effect of crop intensi-fication on insect pest populations and showedan increase in the population density of thequinoa moth (Eurysacca melanocampta) beyondthe economic damage threshold, causing a yieldreduction and economic loss (Campos et al. 2012).Use of farm machinery, such as a plough andsowing machine, produces a loose soil substratumthat helps ticona larvae (Copitarsia sp.) and quinoamoth (Eurysacca quinoae) to penetrate the soileasily and complete their life cycles (Rasmussenet al. 2003; Sigsgaard et al. 2008).

At present, there has been little attentiongiven to the study of entomofauna associatedwith quinoa compared to other Andean cropssuch as corn and potato (Zanabria and Mujica1977; Sánchez and Vergara 1991; Yábar et al.2002; Valoy et al. 2011). Because of this, there isa critical lack of knowledge about insect diversityand the role they play in quinoa cropping systems.However, there is a recent movement towardimplementation of integrated pest managementstrategies in quinoa (Palacios et al. 1999; Dangleset al. 2009, 2010).

In this chapter, existing information on harm-ful and beneficial insects of quinoa is discussed.The short-term and long-term effects of changesin quinoa production are also examined. Possiblesolutions to the challenges posed by currentquinoa farming are explored within the contextof sustainable agroecosystems.

INSECTS IN QUINOA

Insects associated with quinoa consist of diversephytophagous and entomophagous organisms.The abundance and occurrence of these insectpopulations, and the intensity of herbivorydamage, may fluctuate according to quinoaphenological stages and the prevailing environ-mental conditions throughout the growing period(Mamani Quispe 2009; Valoy et al. 2011). Otherfactors involved are location and extent of crops,cultivars used, presence or absence of other cropsnearby, and presence of native vegetation patches,among others (Costa et al. 2009a, 2009b).

In order to implement integrated managementprograms with emphasis on biological control, itis fundamental to identify and study the insectscomprising the agroecosystem. Native and exoticinsect species have been reported associated withquinoa (Ortíz Romero 1993). These are membersof different functional herbivorous groups such asleaf miners, leaf cutters, leaf chewers, sap suckers,stem borers, defoliators, and grain and panicleconsumers (Alata 1973; Ortiz and Sanabria 1979;Bravo and Delgado 1992; Ortiz 1997; Zanabriaand Banegas 1997; Rasmussen et al. 2003).Moreover, many of these herbivores are vectors ofpathogenic microorganisms (FAO 1993).

The Neotropical region, an ecozone thatincludes South and Central America, the Mexi-can lowlands, the Caribbean islands, and southernFlorida, has 74 insect species associated withquinoa. These insect species are distributedin 25 families belonging to five orders: Lepi-doptera, Hemiptera, Coleoptera, Diptera, andThysanoptera (Barrientos Zamora 1985; FAO1993; Lamborot et al. 1999; Hidalgo and Jacobsen2000; Rasmussen et al. 2001; Yábar et al. 2002;Saravia and Quispe 2005; Costa et al. 2007, 2009a,2009b; Valoy et al. 2011; Campos et al. 2012). Mostof these insect records pertain to quinoa cropslocated in Bolivia, Peru, and Ecuador, whereas inthe more southern portion of the Andes, infor-mation is scarce, with a few descriptive papers(Lamborot et al. 1999; Reguilón et al. 2009; Valoyet al. 2011). A literature review revealed that in21 years (1987–2012) there are only 20 paperspublished on insects linked to Andean crops such

The Potential of Using Natural Enemies and Chemical Compounds 65

as quinoa, amaranth, and potato. Twelve of thesepapers mentioned insects of quinoa, includingharmful and beneficial ones (Valoy, unpublisheddata) (Table 5.1 and Figs 5.1–5.3).

Insect pests of quinoa

Among the insect pests of quinoa, several Lepi-dopteran species collectively known as the quinoamoth cause the greatest damage. Among thesemoths, E. melanocampta and E. quinoae (Lepi-doptera: Gelechiidae) are regarded as key pests,due to the direct damage their larvae make to theplant. Even though they affect all developmentalstages of the plant, most damage is inflictedduring the grain ripening state (Rasmussen2003). E. melanocampta, commonly known as“quinoa kuro,” causes between 35% and 60%of plant damage (Ochoa Vizarreta and Franco2013). Its distribution covers xeric environmentsof the Andes Mountains (1,900–4,350 masl)from Argentina and Chile to northern Colombia(Povolny and Valencia 1986; Povolny 1986, 1997).Adults have crepuscular or nocturnal habit andtypically lay their eggs in the glomeruli or inflo-rescence axils. When first-stage larvae emerge,they chew leaves and inflorescences. The moreadvanced larval stages subsequently roll leavesfor use as shelter as they wait to feed duringthe grain-filling and ripening stages (Rasmussen2003; Ochoa Vizarreta and Franco 2013). Thebiology and morphology of E. quinoae (commonlynamed “kona kona” or “grain grinder”) is verysimilar to E. melanocampta, but distinguishedfrom each other by differences in their wingspot patterns (Ochoa 1990; Povolny 1997). E.quinoae has often been described as a pest of morerestricted distribution than E. melanocampta,although recent papers mentioned E. quinoae as akey pest in Peru (Rasmussen et al. 2000; Camposet al. 2012) (Fig. 5.1).

Another Lepidopteran group that may occa-sionally cause important losses in quinoa is the“ticona complex,” a group composed of cut-worms belonging to family Noctuidae: Copitarsiaturbata, Feltia sp., Heliothis sp., and Spodopterasp. (Blanco 1982; Aroni 2000; Chambilla et al.2009). The most representative species of this

complex is C. turbata (Larrain 1996). Its larvaeare stemborers, usually causing damage in thebeginning of the season by cutting the stem ofyoung plants. In cases of severe infestation, theymay even eat leaves, inflorescences, and grains,aside from shoots and stems (Vela and Quispe1988; Zanabria and Banegas 1997).

Rasmussen et al. (2003) listed several phy-tophagous insects that affect quinoa, indicatingwhich are pests and potential pests. Included inthe list are the orders Orthoptera (Gryllidae) andDiptera (Agromizidae), together with Coleoptera(Bruchidae, Curculionidae, and Tenebrionidae),for a total of 54 species (Table 5.1 and Fig. 5.1).

South of the Neotropical region, in Brazil, theAtta sp. (Formicidae: Hymenoptera) and Diabrot-ica speciosa (Genn.) (Coccinellidae: Coleoptera)species have been reported in quinoa (CabreraAlmendros and Oliveira 2011). In the Amaichadel Valle, Tucumán, Argentina, Valoy et al. (2011)carried out studies in an experimental quinoaplot and reported the presence of three families,four genera, and seven species of phytophagousinsects that have not been mentioned previouslyin quinoa grown in the Neotropical region(Table 5.1 and Fig. 5.1).

Beneficial insects in quinoa

Natural enemies of phytophagous insects are alsocalled beneficial or entomophagous insects. Mostphytophagous insects have more than one andoften many natural enemies that regulate theirpopulations. A large number of beneficial insectsattack several species of herbivorous insects inquinoa, while there are entomophagous groupsthat are more specific (Table 5.2). Generally, natu-ral enemies of phytophagous insects are classifiedas parasitoids, predators, or pathogens. Specifi-cally, parasitoids and predators are categorizedas entomophagous and these will be discussedin more detail in this chapter. Another group ofnatural enemies of insects are entomopathogens,which are microorganisms that cause diseases oninsects. These are closely associated with insectpests and have been used to control insect pestsin quinoa but are discussed only briefly in thischapter.


Table 5.1 Insect species associated with quinoa crops.

Order Family Genus/species Source

Coleoptera Bruchidae Acanthoscelides diasanus Rasmussen et al. (2003)Chrysomelidae Acalymma demissa Rasmussen et al. (2003)

Calligrapha curvilinear Rasmussen et al. (2003)Diabrotica decempunctata Rasmussen et al. (2003)Diabrotica sicuanica Rasmussen et al. (2003)Diabrotica sp. Rasmussen et al. (2003)Diabrotica speciosa Rasmussen et al. (2003), Cabrera Almendros and

Oliveira (2011)Diabrotica undecimpunctata Rasmussen et al. (2003)Diabrotica viridula Rasmussen et al. (2003)Epitrix subcrinita Rasmussen et al. (2003)Epitrix yanazara Rasmussen et al. (2003)Epitrix sp. Saravia and Quispe (2005)

Coccinellidae Eriopis connexa Yábar et al. (2002), Valoy et al. (2011)Eriopis peruviana Costa et al. (2007)Eriopis sp. Valoy et al. (2011)Hippodamia convergens Hidalgo and Jacobsen (2000), Yábar et al. (2002),

Valoy et al. (2011)Curculionidae Adioristus sp. Rasmussen et al. (2003)Formicidae Atta sp. Rasmussen et al. (2003)Meloidae Epicauta adspersa Valoy et al. (2011)

Epicauta langei Valoy et al. (2011)Epicauta latitarsis Rasmussen et al. (2003)Epicauta marginata Rasmussen et al. (2003)Epicauta sp. FAO (1993), Hidalgo and Jacobsen (2000),

Saravia and Quispe (2005)Epicauta willei Rasmussen et al. (2003)Meloe sp. Rasmussen et al. (2003)Tetraonix sp. Valoy et al. (2011)

Melolonthidae Ancistrosoma vittigerum Valoy et al. (2011)Melyridae Astylus atromaculatus Valoy et al. (2011)

Astylus luteicauda Hidalgo and Jacobsen (2000), Rasmussen et al.(2003)

Astylus laetus Rasmussen et al. (2003)Tenebrionidae Pilobalia decorata Rasmussen et al. (2003)

Diptera Agromyzidae Liriomyza huidobrensis Rasmussen et al. (2003), Saravia and Quispe(2005)

Tachinidae Phytomyptera sp. Rasmussen et al. (2001)Unknown Valoy et al. (2011)

Hemiptera Aphidae Acrytosiphum kondoi Barrientos Zamora (1985)Aphis craccivora Rasmussen et al. (2003)Aphis gossypii Rasmussen et al. (2003)Macrosiphum euphorbiae Barrientos Zamora (1985), Yábar et al. (2002),

Rasmussen et al. (2003), Saravia and Quispe(2005), Campos et al. (2012)

Myzus persicae Yábar et al. (2002), Rasmussen et al. (2003),Saravia and Quispe (2005), Costa et al. (2007)

Myzus sp. FAO (1993)(continued)


Table 5.1 (Continued)

Order Family Genus/species Source

Cicadellidae Anacuerna centrolinea Saravia and Quispe (2005)Bergallia sp. Rasmussen et al. (2003)Borogonalia impressifrons Rasmussen et al. (2003)Empoasca cisnova Rasmussen et al. (2003)Empoasca hardini Rasmussen et al. (2003)Empoasca sp. Saravia and Quispe (2005)Paratanus exitiousus Rasmussen et al. (2003)Paratanus yusti Rasmussen et al. (2003)Paratanus sp. Rasmussen et al. (2003)

Coreidae Leptoglossus sp. Valoy et al. (2011)Nabidae Nabis sp. Valoy et al. (2011)Pentatomidae Nezara viridula Valoy et al. (2011)

Hymenoptera Encyrtidae Copidosoma gelechiae Hidalgo and Jacobsen (2000)Copidosoma koehleri Hidalgo and Jacobsen (2000)Copidosoma sp. Valoy et al. (2011)

Ichneumonidae Unknown Rasmussen et al. (2001), Valoy et al. (2011)Vespidae Spodoptera eridania Valoy et al. (2011)

Neuroptera Chrysopidae Chrysoperla argentina Valoy et al. (2011)Chrysoperla externa Valoy et al. (2011)

Lepidoptera Gelechiidae Eurysacca media Lamborot et al. (1999)Eurysacca melanocampta FAO (1993), Hidalgo and Jacobsen (2000), Rasmussen

et al. (2001, 2003), Saravia and Quispe (2005), Costaet al. (2007, 2009a, 2009b)

Eurysacca quinoae Campos et al. (2012), Rasmussen et al. (2001, 2003)Scrobipalpula absoluta Barrientos Zamora (1985)

Geometridae Perizoma sordescens Rasmussen et al. (2003), Saravia and Quispe (2005)Noctuidae Agrotis ipsilon Rasmussen et al. (2003)

Agrotis malefica Rasmussen et al. (2003)Agrotis sp. Rasmussen et al. (2003), Saravia and Quispe (2005)Copitarsia consueta Barrientos Zamora (1985), Rasmussen et al. (2003)Copitarsia turbata Saravia and Quispe (2005), Rasmussen et al. (2003)Dargida graminivora Rasmussen et al. (2003)Feltia experta Rasmussen et al. (2003)Feltia sp. Rasmussen et al. (2003), Saravia and Quispe (2005)Heliothis titicaquensis Rasmussen et al. (2003), Saravia and Quispe (2005)Heliothis zea Rasmussen et al. (2003)Peridroma interrupta Rasmussen et al. (2003)Peridroma saucia Rasmussen et al. (2003)Pseudaletia unipunctata Rasmussen et al. (2003)Spodoptera eridania Rasmussen et al. (2003)Spodoptera frugiperda Barrientos Zamora (1985), Rasmussen et al. (2003)Spodoptera sp. Saravia and Quispe (2005)

Psychidae Oiketicus kirbyi Valoy (personal communication)Oiketicus geyeri Valoy (personal communication)

Pyralidae Achyra similalis Lamborot et al. (1999)Herpetogramma bipunctalis Rasmussen et al. (2003)Hymenia recurvalis Saravia and Quispe (2005)Pochyzancla bipunctalis Saravia and Quispe (2005)Spoladea recurvalis Rasmussen et al. (2003)

Thysanoptera Thripidae Frankliniella tabaci Rasmussen et al. (2003)Frankliniella tuberosi Saravia and Quispe (2005)Frankliniella sp. Rasmussen et al. (2003), Campos et al. (2012)


(a)

(c)

(f) (g)

(h)

(j)(l)

(d) (e)

(b)

Fig. 5.1 Phytophagous insects associated with quinoa in the Neotropical region. (a) Lepidoptera, larvae feeding on quinoa leaf;(b) Leptoglossus sp. in quinoa leaf; (c,d) Oiketicus kirbyi, neotenic larvae coming out of bag or basket; (e) O. kirbyi bag or basketin quinoa branch; (f ) adult Eurysacca sp.; (g) Eurysacca sp. larvae feeding on quinoa leaf; (h) Pyralidae, larvae; (i) Nezara viridula,adult in quinoa panicle; and (j) adult Epicauta adspersa in quinoa leaf. (See color insert for representation of this figure.)


(a)

(d)

(g) (h) (i)

(l)(k)(j)

(e) (f)

(b)

(c)

Fig. 5.2 Entomophagous insect on quinoa in Amaicha del Valle. (a) Parasitoid Copidosoma sp. adult; (b) Copidosoma sp. para-sitism in Eurysacca larvae; (c) Eurysacca damaged pupa; (d) parasitoid Ichneumonidae; (e) unidentified parasitoid; (f–l) predatorinsects; (f ) Eriopis connexa, immature stage; (g) Chrysoperla argentina, adult; (h) C. externa, immature stage; (i) C. externa, adult;(j) C. argentina, preying on Spodoptera frugiperda (Lepidoptera) eggs; (k) C. argentina, immature stage preying on aphids; and(l) C. externa, immature stage preying on aphids. (See color insert for representation of this figure.)

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(a) (b) (c)

Fig. 5.3 Coleoptera species in quinoa crops. (a) Carabidae; (b) Ancistrosoma vittigerum; and (C) Astylus atromaculatus.

Parasitoids

Parasitoid groups are mainly distributed intwo insect orders, Hymenoptera (wasps) andDiptera (flies). In terms of number of species,the order Hymenoptera is dominant amongentomophagous insects and has been widely usedfor biological control of crop pests. Within thisgroup, there are interesting, specific biologicaladaptations related to their reproductive successin using other insect bodies that they parasitize.Mainly Hymenopteran parasitoids, and in a fewcases, Dipteran parasitoids, have been reportedin quinoa (Valoy et al. 2011) (Table 5.2) andparasitize egg, larval, and pupal stages (Fig. 5.2).

Predators

Predators belong to the most varied taxonomicgroups of insects and possess diverse adapta-tions and behaviors for prey capture. From theecological point of view, the most importantpredator species belong to the orders Neuroptera,Coleoptera, Diptera, Hemiptera, Hymenoptera,Odonata, and Mantodea (Fig. 5.2).

Coleopterans from the Coccinellidae andCarabidae families are among the predators ofquinoa pests (Table 5.2). These families arecomposed of species that are considered of greatimportance in agriculture for pest control. Bothlarvae and adults are active predators of smallherbivores; they are generally quite voracious

and have high fertility. In Argentinian quinoacrops, green lacewings (Neuroptera: Chrysopi-dae), Eriopis sp., and Eriopis connexa (Germar)(Coleoptera: Coccinellidae) have been observed,all of them in the beginning of the floweringstage (Valoy et al. 2011). These data suggestthat such predators might be preying on eggsand larvae of Lepidopteran species, such asEurysacca sp., whose larvae are also abundant inthis phenological stage of quinoa. Moreover, thepresence of the predator Hippodamia convergens(Guérin-Méneville) (Coleoptera: Coccinellidae)coincides with aphid infestation during the milkand dough stages of quinoa (Valoy et al. 2011)(Fig. 5.2). In the Peruvian Andes, the abundanceof predators fluctuates as plant growth progresses.This was observed in Coccinellidae (H. convergensand E. connexa) species, whose population peakedin the middle of crop development, whereasother predators such as Syrphidae were abundantduring the latest stages of the crop (Yábar et al.2002). In the Peruvian Altiplano, the followingspecies of carabid predators were found preyingon E. melanocampta larvae: Notobia (Anisotarsus)schnusei Van Emden, Notobia (Anisotarsus) laevisbolivianus Van Emden, and Meotachys sp. nearharvest, during which time these carabid predatorpopulations increase (Loza and Bravo 2001).

While phytophagous species prevail withinthe order Hemiptera, other entomophagousgroups within this order have also been noted.


There is also an important number of speciesthat comprise different beneficial families. TheLygaeidae (Geocoris sp.), Miridae (Rhinacloasp.), and Nabidae (Nabis sp.) families have beenreported in quinoa (Rasmussen 2003; Valoy et al.2011) (Fig. 5.2). Popularly known as “assassinbugs,” the adults as much as the nymphal stagesare predators; they possess a pick or rostrumusually bent or folded toward the abdomen thatthey use to catch their prey. They are very activeand voracious; their coloring camouflages themfrom their prey.

Entomopathogens

In natural pest control, entomopathogens canplay an important role, especially when epi-zootics occur. However, little is known aboutthe pathogens causing diseases on insects linkedto quinoa. Even though it is generally knownthat most common insect diseases are causedby bacteria, fungi, viruses, protozoa, and nema-todes, relatively few pathogen species havebeen identified compared with the number ofentomophagous insects. However, there aresome entomopathogens on which we have moreinformation. For instance, Bacillus thuringiensisMorrisoni and the fungi Beauveria bassiana(Bals.-Criv.) Vuill. and Metarhizium anisopliaeSorokin attack diverse insect species. Ento-mopathogens have already been mass-producedfor field application as microbiological insecti-cides or bioinsecticides. In quinoa, bioinsecticideswith granulosis virus have been tested againstE. melanocampta, reaching levels of 50% control(Calderón et al. 1996; Zanabria and Banegas1997). Other viruses have been isolated from E.melanocampta larvae and tested as bioinsecticides,where preliminary screening has shown thepresence of nucleopolyhedrosis virus (NPV)(Rasmussen unpublished data). One drawback ofusing entomopathogens is their inability to searchfor host, unlike entomophagous insects which cansearch for prey.

In summary, even though studies on biodiver-sity in quinoa crops in the Neotropical regionshave been oriented toward identifying insect pestspecies, the presence of natural enemies have

also been recorded. Groups belonging to 5 insectorders, 11 families, and 19 genera with 24 specieshave been reported in various studies and presenta promising prospect for biocontrol of insect pestsin quinoa.

Chemical responses of quinoa to insectherbivory

In this section, we introduce the concept ofchemical interactions between plants and insectsand discuss the chemical potential of quinoa torepel the attack of herbivorous insects. Manyspecies of the Chenopodium genus possess sec-ondary metabolites (SMs) with potential effectson herbivorous insects, such as flavonoids, gly-cosides, flavonols, phenolic amides, coumarins,alkaloids, lignin, phytosteroids (ecdysteroids),phenolics, and saponins (Verma and Agarwal1985; Jam et al. 1990; Dinan 1992; Gee et al.1993; Horio et al. 1993; Cuadrado et al. 1995;Berdegue and Trumble 1996; Gallardo et al. 2000;Hernández et al. 2000; Woldemichael and Wink2001; Zhu et al. 2001a, 2001b; Hilal et al. 2004;DellaGreca et al. 2005; Cutillo et al. 2006; Paskoet al. 2008; Kokanova-Nedialkova et al. 2009;Kumpun et al. 2011).

Studies have been conducted to characterizethe primary and SMs of quinoa, in order to explaintheir nutritional and medical properties includingthe chemical response of quinoa to unfavorableconditions during cultivation (González et al.1989; Ruales and Nair 1993; Cuadrado et al. 1995;Dinan et al. 1998; Woldemichael and Wink 2001;Hilal et al. 2004; Costa et al. 2007; Pasko et al.2008; Kokanova-Nedialkova et al. 2009; Jancurováet al. 2009; Kuljanabhagavad and Wink 2009;Rosa et al. 2009; Dowd et al. 2011; Kumpun et al.2011; Campos et al. 2012). Information aboutentomofauna associated with quinoa cultivation isalso available, especially concerning plant–insectinteractions (Yábar et al. 2002; Rasmussen et al.2003; Valoy et al. 2011; Campos et al. 2012) andchemical interactions (Costa et al. 2009a).

SMs present in quinoa cultivars have thepotential to counteract damage caused by her-bivores, such as phenolic acids (gallic acid,hydroxybenzoic acid, vanillic ester glucosidic


acid, ferulic acid, cinnamic acid, and phyticacid), tannins, flavonoids (isoflavone, glycosylatedkaempferol, rutin, and quercetin), as well as20-hydroxyecdysone and saponins (De Simoneet al. 1990; Bi et al. 1997; Lattanzio et al. 2000;Zhu et al. 2001a, 2001b; Sánchez-Hernándezet al. 2004; Dini et al. 2004; Cutillo et al. 2006;Pasko et al. 2008; Kokanova-Nedialkova et al.2009; Kumpun et al. 2011).

In general, plants possess biomechanical andbiochemical strategies to resist and/or endurestress. Biomechanical strategies consist of tissuearchitecture (presence of glandular trichomes andhigh density of nonglandular trichomes), whereasbiochemical strategies constitute metabolitessynthesized during plant growth or in response toexternal stimuli. These strategies provide tissueswith resistance, elasticity, hardness, protection,attractive colors, and smells for dispersion of fruitand flowers. The signal compounds also serve asstress warning responses when exposed to excessheavy metals, salinity, UV radiation, and changesin temperature and humidity (Bi and Felton 1995;Ramakrishna and Ravishankar 2011; Podazza et al.2012; Gómez-Caravaca et al. 2012; Whitney andFeder 2013). These strategies allow quinoa plantsto endure herbivore pressure, either because thetissue surface possesses structures that preventadequate adhesion or tissues at the biochemicallevel may be unpleasant for herbivory. Volatilecompounds, known as herbivore-induced plantvolatiles (HIPV), may also be released as partof the biochemical strategies (Howe and Jander2008; Ponzio et al. 2013).

Volatile compounds work against herbivores,attract parasitoids, and function as chemicalsignals that can “warn” neighboring plants ofthe presence of herbivores (Paré and Tumlinson1999; Li et al. 2012; Ponzio et al. 2013). In thiscontext, the plant’s capacity to avoid and/orrecover from herbivore damage will depend onherbivory intensity and frequency, phenologyand plant health status, chemical signals receivedfrom neighboring plants, and abiotic factors suchas photoperiod seasonal changes, bioavailabilityof nutrients, and water (Banerji 1980; Bi andFelton 1995; Lichtenthaler 1996; Rastrelli et al.1998; Sánchez-Hernández et al. 2004; Costa et al.

2009a, 2009b; Wink 2006; Wise and Abrahamson2007; Anttila et al. 2010).

The ability of plants to respond to biotic stressrequires the redistribution of metabolic resourcesand nutrients at the expense of energy meantfor development and performance (Nabity et al.2006; Pasko et al. 2008; Wink 2009; Wink andSchimmer 2009; Gómez-Caravaca et al. 2012).In an agriculture-based economy, the deviationof resources in cultivated species from energy todefense against herbivory can lead to economiclosses. In this context, it is extremely importantto design pest control management systems thatconsider the ability of cultivated species to defendthemselves against insect feeding without affect-ing yield and, at the same time, allow farmers toreduce the use of harmful pesticides (Griffiths1999; Wink 2006).

Insects have developed different physiologicaland feeding behavior strategies adapted to plantdefense mechanisms. They can select tissues tofeed on based on the balance among chemicaldefenses, nutritional compounds, and the antiox-idant content of plant tissues. This balance canenhance or decrease the toxicity of plant tissuesin response to herbivory (Berdegue and Trumble1996; Bi et al. 1997; Varanda and Pais 2006).

When classified according to behavioral strate-gies, insects can be generalists (polyphagous)that feed on plants from different families orspecialists (monophagous and oligophagous)that feed on one or few plants belonging to thesame family (Fürstenberg-Hägg et al. 2013).Specialist insects develop physiological strategiesthat allow them to perceive repellent or attractantcompounds, select plants and plant tissues forfeeding or oviposition, and metabolize planttoxins. In order to detect volatile compounds,they possess specific adaptations located inmouthparts and antennae, which function aschemoreceptors. For example, to avoid toxiccompounds, they have specific elicitors in salivarysecretions. Other insects use SMs ingested infood for survival and reproduction, and theyeven have digestive enzymes such as polyphenoloxidase, peroxidases, and oxidoreductases thatcan reduce the toxic effect of some metabolites(Simmonds 2003; Lattanzio et al. 2006) (Fig. 5.4).


Entomophagous insects

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TC

HAMPVolicitinIncepticinCaelipherinβ-Glucosidase (b)

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AvoidanceNon-resorptionResorption and accumulationUtilization

Fig. 5.4 Plant–insect biochemical interactions, with plant chemical responses after attack of phytophagous insects.(a) Function of inducible or constitutive secondary metabolites (SMs) such as phenolics, terpenes, and alkaloids; (b) plant rapidresponse related to damage, jasmonic acid signal, and herbivory-associated molecular patterns (HAMP); (c) plant slow response,herbivore-induced plant volatiles (HIPVs), monoterpenes act as signals to other plants and entomophagous insects.

In this respect, herbivorous species belonging tothe genus Eurisacca would be considered special-ists. However, their physiological characteristicsshould be studied more to expand our knowledgeand to help develop management strategies at themolecular level to discourage attacks from thesepests.

Quinoa secondary metabolites

Terpenoid compounds

Saponins are terpenoid compounds and couldbe considered as constitutive chemical defensesthat deter herbivory by insects. These com-pounds have a structure composed of a lipophilic


nucleus (steroid or triterpene) and a hydrophilicmoiety (different glycosylation patterns), whichdefines their membranolytic properties affectinginsect intestinal mucus and damage membranefunctionality (Gee et al. 1993; Wink 2006;Kuljanabhagavad and Wink 2009; Dowd et al.2011). Saponins are found in branches, leaves,flowers, and fruits of different quinoa varieties.However, it has been observed that saponincontent fluctuates among varieties. For instance,varieties with yellow seeds such as “Marangani”have higher saponin content than those withwhite seeds, because of high hederagenin andoleanolic acid content. Differences in saponinconcentration due to phytolaccagenic, deoxyphy-tolaccagenic, and serjanic acid content might alsobe influenced by water availability (Cuadradoet al. 1995; Woldemichael and Wink 2001; Yábaret al. 2002; Kokanova-Nedialkova et al. 2009;Gómez-Caravaca et al. 2012). Nevertheless, inspite of varying saponin content in quinoa vari-eties, insect pests would most likely be controlledby their natural enemies than by the presence ofsaponin (Yábar et al. 2002).

Other metabolites of the steroid typefound in quinoa seeds are ecdysteroids, alsocalled phytoecdysteroids. They are known as20-hydroxyecdysone, makisterone, and kan-collosterone (Dinan 1992) and are particularlypredominant in quinoa, with amounts rangingbetween 450 and 1300 μg.g-1DW ecdysteroidequivalents reported (Dinan 1992; Dinan et al.1998). The importance of ecdysteroids lies intheir structural similarity to insect steroids,hormones that regulate biochemical and physi-ological processes associated with reproduction,embryo maturation, development, and metamor-phosis (Dinan 2001; Thummel and Chory 2002).Phytoecdysteroids are present in numerous fam-ilies of the plant kingdom and play a protectiverole against nonspecialist herbivores and alsoagainst soil nematodes. These compounds affectmolting of nematodes and can even be lethal.The presence of phytoecdysteroids in quinoa hasled to the development of breeding programswith the goal of increasing these compounds inquinoa lines and varieties. Aside from helpingcontrol pest outbreaks, these compounds also

have nutritional benefits to humans. They cansupplement the caloric intake of the human dietand have remarkable chemical stability duringby-products manufacturing (Kumpun et al.2011).

The terpenes found in quinoa are limonene,α-terpinolen, β-phellandrene, α-terpinene,aromatic monoterpenoids such as p-cymene,trans-carveol, carvone and pinocarvone, piperi-tone, and aromatic sesquiterpenes such asβ-elemene and β-caryophyllene. Limonene,α-terpinolen, and β-phellandrene are accumu-lated in plant tissues against herbivory damage(Lerdau et al. 1994; Loughrin et al. 1994). More-over, aromatic sesquiterpenes such as β-elemeneand β-caryophyllene might be associated withHIPV response, as it is known that many volatilecompounds can originate from membrane lipids(during the “quick response”) or they can beterpenoid-type (during the “slow response”).In the “quick response” situation, volatile com-pounds derived from cell membrane fatty acidsact as precursors of signals for the synthesis ofprotease inhibitors, which interfere with thedigestion of plant tissues. For example, responseto herbivory injury is triggered when tissuesrelease a polypeptide hormone called systemin,which is then coupled to a plasma membranereceptor. A lipase is then induced to releaselinoleic acid molecules inside the cell, which areprecursors of jasmonic acid synthesis. Jasmonicacid is a signal molecule that simultaneouslyactivates genes for protease inhibitors. Thus, thissuite of events makes the tissue unpalatable toinsects (Sánchez-Hernández et al. 2004; Fig. 5.4).In the “slow response,” volatile terpenes, usuallymonoterpenes, are released. The volatiles canattract predators and parasitoids or act as warningsignals to neighboring plants so that they activatetheir defenses (Paré and Tumlinson 1999; Howeand Jander 2008; Li et al. 2012).

On the other hand, the salivary secretions ofmany orders, including Lepidoptera, Diptera,and Orthoptera, have a mixture of compoundsrelated both to feeding and oviposition andalso function as elicitors or effectors of plantreactions. Some of these compounds havebeen identified as β-glucosidase, violicitin,


incepticin, and caelipherin and are useful tocharacterize herbivory-associated molecularpatterns (HAMPs). Furthermore, it should benoted that microorganisms participate in thisinteraction, being present both in plant and insectsurfaces and in insect salivary secretions, and alsocause a signal sequence that is a component ofthe microorganism-associated molecular patterns(MAMPs). The joint action of compoundscoming from plants, insects, and microorganismscan suppress the toxic effects of some compoundssynthesized by plants and enable herbivory, aswell as induce the release of volatile compoundsthat can serve as attractants and ovipositionstimulants for parasitoids and as warning signalsto neighboring plants. These reactions would alsobe linked to P450s, a versatile enzyme systempresent in plants and specialist insects, involvedboth in plant SM biosynthesis and in insectdetoxification catabolic systems (Schuler 1996)(Fig. 5.4).

Phenolic compounds

Among the phenolic compounds in quinoa,some metabolites act as signaling molecules andare responsible for raising the alarm againststressors such as UV-B radiation, herbivores, andpathogens. Other phenolic compounds defendplant tissues against resulting oxidative stress.Within this group, there are some pigments, suchas flavonoids and anthocyanins, that not onlyprevent UV-B damage but also act as opticalsignals to attract pollinators and dispersal vectorsbecause of their bright colors (Bi and Felton 1995;Simmonds 2003; Lattanzio et al. 2006; Wink andSchimmer 2009; Prado et al. 2012).

Phenolic compounds accumulate in vacuolesand are linked to epidermal and sub-epidermalcell walls of leaves, stems, cutin, and wax depositsfrom outer surfaces of plant organs. Phenoliccompounds can even form complexes with DNAmolecules in order to provide oxidative protection(Simmonds 2003; Lattanzio et al. 2006). The roleof phenolic content in plant–insect interactionsis directly related to PAL activity (phenylalanineammonia lyase), a key enzyme in the synthesisof phenolics. Therefore, analysis of PAL activity

may serve as a response indicator to herbivory.Moreover, the phenolic profile in tissues mayserve as an estimate of herbivory occurrence.

Although the anti-herbivory role of phenolsand polyphenols has not been studied in quinoa,it has been reported that these compoundshave anti-herbivory properties in Amaranthus,another genus belonging to the Chenopodiaceaefamily (Niveyro et al. 2013). On the other hand,quinoa seed has compounds with anti-herbivoryproperties, such as rutin, orientin, vitexin, morin,hesperidin, neohesperidin, cinamic acid, caffeicacid vanillic acid, and gallic acid (tannin synthesis)and kaempferol and quercetin glycosides (Diniet al. 2004; Pasko et al. 2008). For example, rutinacts as a phagostimulant, whereas kaempferol hasgenotoxic properties, acts as feeding deterrent,and can affect the emergence of aphids. Vanillicacid glucose ester acts with greater intensityon broods of aphids, whereas tannins decreasethe palatability of plant tissues because of theirastringent properties or hinder digestion byforming complexes with proteins and/or inacti-vate digestive enzymes (Bi et al. 1997; Lattanzioet al. 2000, 2006; Simmonds 2003; Pasko et al.2008; Wink and Schimmer 2009; Steffensen et al.2011). Phytic acid in quinoa chelates many ionsand interferes with their incorporation into theinsect diet (De Simone et al. 1990; Bi and Felton1995; Bi et al. 1997; Zhu et al. 2001b; Dini et al.2004; Pasko, et al. 2008; Wink and Schimmer,2009; Steffensen et al. 2011; Niveyro et al. 2013).

In summary, there are various chemical com-pounds produced in quinoa as a response toherbivory. These present an exciting new area forstudy, especially assessing their potential use forbiological control.

POTENTIAL OF BIOLOGICAL CONTROL INQUINOA

At present, most of the information on biologicalcontrol in the Andean quinoa crop comes fromstudies on entomophagous insects (parasitoidsand predators). Cultural practices and host plantresistance are also important factors to consider


in establishing a phytosanitary management pro-tocol for quinoa. It is encouraging to know thatin the field, up to 45% of parasitoid and predatorspecies exert natural biological control in keyquinoa pests such as the quinoa moth (Eurysaccasp.) and ticona complex (Heliothis, Copitarsia, andSpodoptera sp.) (Rasmussen et al. 2003). Fluctu-ations in key and potential pest populations inAndean crops follow a similar temporal patternin different regions and are associated with cropphenology. However, relative densities of keypests, such as quinoa moths and ticona complex,exhibit variations between different Andeanzones. In the Northern Altiplano, pest densitiesare low, with 1–6 larvae/plant; in the CentralAltiplano, 7–15 larvae/plant have been recorded;and in the Southern Altiplano, pest densities havebeen recorded from 9 to over 45 larvae/plant(Saravia and Quispe 2005), indicating that thesepests could be a limiting factor in the southernareas for quinoa production.

The percentage of parasitism on E.melanocampta in the field during a completecycle of quinoa cultivation has been measuredby Mamani (1998). The percentage of parasitismranged from about 25% during the soft doughstage to 45% during the milk grain phenolog-ical phase, reaching 80% during physiologicalmaturity (Mamani 1998). The main parasitoidsof this Lepidopteran pest are Copidosomagelechiae Howard (Encyrtidae) and Diadegma sp.(Ichneumonidae) (Rasmussen et al 2003).

In addition to parasitoids, natural biologicalcontrol relies on a complex of insect predatorsthat regulate the populations of phytophagouspests of quinoa. Among the predator insectgroups, the Coccinellidae (Coleoptera) andChrysopidae (Neuroptera) species have a moresignificant role in pest control in agroecosystems.The Chrysopidae is the most important predatorgenus used in biological control and can be bredon a large scale and commercialized for releasein the field (Tauber et al. 2000). The larvae ofthese predator families are extremely active, fastmoving, and have considerable ability to searchfor prey. They are polyphagous predator speciesand feed on a large number of economicallyimportant insect pests. They can also feed during

different life stages of the insect prey, such as theegg, larvae (nymphs), and adult stages.

It is important to have the correct taxonomicidentification of predator species in quinoa,particularly of Chrysopidae (Reguilón et al. 2006,2009), as they are only mentioned at the genuslevel in studies conducted in the Neotropicalregion. Correct species identification is the firststep to study the biology of natural enemiesand their predation capacity to develop methodsfor mass rearing and design biological controlsystems to be applied in quinoa.

We followed the course of a quinoa crop inTucuman, Argentina for two periods (fromNovember 2008 to March 2010), which allowedus to establish the dynamics of two Chrysop-erla species associated with quinoa (Reguilón,personal communication). Chrysoperla externaHagen and Chrysoperla argentina GonzálezOlazo-Reguilón (González Olazo and Reguilón2002) were collected throughout the crop phe-nology (Fig. 5.5). This is the first report of C.argentina in quinoa. As shown in Figure 5.5, thepresence of C. argentina was evident on all cropsurvey dates. The highest predator populationdensities occurred in the months of Novemberand March and coincided with the presenceof herbivorous lepidopteran genus Eurysaccaand Pyralidae family. Lacewings such as Eriopissp. and E. connexa (Coleoptera: Coccinellidae)were also observed at the beginning of floweringand during the flowering stage, though in lowerdensities (Valoy et al. 2011). These data sug-gest that predators in these phenological stageswere actively preying on eggs and larvae of theLepidoptera species mentioned. Aphids wererecorded in milky and dough stage, coincidingwith the presence of the predator H. convergens(Valoy et al. 2011).

POTENTIAL FOR ECOLOGICALMANAGEMENT OF QUINOA

The use of biological control agents (parasitoids,predators, or pathogens) is a necessary componentof integrated pest management to regulate pop-ulations of insects that cause economic damage


C. argentina

C. externa

NOV DEC

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Fig. 5.5 Chrysoperla species associated with quinoa in Amaicha del Valle, Tucuman, Argentina. The population dynamics ofChrysoperla externa Hagen (light grey bar) and Chrysoperla argentina González Olazo-Reguilón (dark bar) species for two periods(from November 2008 to March 2010). A: eggs; B: larvae; C: adult.


to crops (Kogan and Shenk 2002; Romero 2004;Hruska 2008) and to reduce the use of agro-chemicals. However, this practice frequently doesnot consist of a comprehensive agroecosystemmanagement, which should, in all cases, includethe application of ecological principles takinginto account all key aspects of insect–plantinteractions, besides the use of biocontrol agents.It is especially important to understand howthe dynamics of species interactions may affectherbivore outbreaks and the expression of pestresistance within an agricultural system. Inthis context, one of the advantages of plants innatural populations is phenotypic and geneticheterogeneity, which translates into variability inexpression of individual plant defenses (Whithamet al. 1984; Nyman 2010). Such heterogeneity canreduce the likelihood of herbivores developingcounterdefenses, thus allowing plants to preservetheir defense mechanisms over time (Letourneau1997).

Ecological principles, from their origin in natu-ral systems to their application in agroecosystems,take into consideration several concepts. One ofthese concepts, and perhaps the most comprehen-sive one, postulates preservation of biodiversity asthe cornerstone for operation and sustainable useof agricultural systems (Altieri et al. 1983; Altieri2009; Butler et al. 2007; Attwood et al. 2008) asit considers the preservation of beneficial bioticinteractions and ecosystem services (Shennan2008; Letourneau et al. 2009; Kremen and Miles2012). In addition, agroecosystem management iscompatible with the system community approach,which decentralizes attention focused solely onpests while understanding the temporal dynamicsof nonpest species (Ordano et al. 2013) that arealso part of the agroecosystem (Griffiths 1999;Wink 2006).

The use of intercropping or mixed croppingsystems is one of the practices that has beenproposed as a means of preserving biodiversity(Vandermeer 1989; Altieri and Nicholls 2004;Perfecto et al. 2009; Lithourgidis et al. 2011).Different cultivars or types of crops could beintercropped. The companion plants may or maynot have commercial value (Parker et al. 2013) butact as repellents or as shelter for beneficial insects.

This has been tested on numerous occasionsand types of crops but with different results.In a review, Poveda et al. (2008) found thatdiversification of vegetation schemes tested inagriculture in the past decade served to reduceherbivore densities in approximately half of thecases included in the review.

In Latin America, a significant portion of thetropical crops are produced in intercropping ormixed cropping systems. However, this type ofmanagement is uncommon in the Andean crop-ping systems (Altieri 1999; Altieri and Toledo2001). There are only a few cases where the effectof corn-and-potato mixed systems has been tested(Raymundo and Alcazar 1983; Thiery and Visser1986; Lal 1991; Rhoades and Bebbington 1990;Silwana and Lucas 2002; Gianoli et al. 2006;Seran and Brintha 2010) and where several typesof biological control have also been carried out(Weber 2012; Kroschel et al. 2012). The effectof agricultural intensification on changing thestatus of insect pests has also been explored inthese mixed systems (Risch 1980; Trenbath 1993;Smith and McSorley 2000; Mojena et al. 2012).

Traditionally, quinoa crops are grown inmonoculture or polyculture systems side by sidewith corn, bean, or potato crops that extendto areas where the vegetation is more diverse,consisting of eucalyptus, turnip, and Poaceae,Asteraceae, and Lamiaceae species. The place-ment of the quinoa crop in relation to othercrops is important as it has been shown that inCusco, Peru, the number of species of parasitoidsof quinoa moth (E. melanocampta) present inthe agroecosystem increased as the diversityof the surrounding crops also increased (Costaet al. 2009a, 2009b). The results of this studyshould spur further research on this topic sothat it can be incorporated in pest managementstrategies.

Currently, several quinoa-producing countriesare changing their crop management practices,gravitating toward monoculture, partially orcompletely replacing crop rotation and resting orfallow periods (Nieto-Cabrera et al. 1997; Fonteet al. 2012; Soto et al. 2012). The practice ofsowing different species that are annually rotatedin the same plot is also slowly being phased out


(Clades 1992). Increasing crop intensificationof quinoa in Bolivia and Peru has replaced theexisting quinoa cultural management, leadingto problems of desertification, decline in soilfertility, and loss of natural vegetation. In Bolivia,the plowing of large tracts of land has led to lossof native vegetation such as “thola” (Pharastrepiasp.), which is used as feed for llamas. Tholamay also be a significant element of the agroe-cosystem as it is a shelter for beneficial species.Moreover, this species possesses anti-herbivoryproperties. Together with another native species(Minthostachys sp.), Pharastrepia sp. is used tomanufacture natural insecticides for applicationin organic quinoa production (Gallegos et al.1982; Jaldin 2010).

Complementary to these management strate-gies, the intrinsic characteristics of quinoa shouldbe known, such as its properties and mechanismsagainst insect pests and how these characteris-tics vary among selected cultivars. One of themechanisms acting on herbivore populations isthe emission of volatile compounds (terpenes andgreen leaf lipid-derived volatiles) that can repelherbivores, attract entomophagous insects (preda-tors and parasitoids), or act as warning signalsto neighboring plants. Quinoa has monoterpenesand sesquiterpenes (Whitman et al. 1990) thatcould be studied further to evaluate whetherthey participate in the exchange of chemicalsignals or as defense mechanism to avoid damageby herbivore feeding or oviposition. It has alsobeen reported that these chemicals decrease theability of the males and females of the quinoamoth to connect with each other (Costa et al.2009a, 2009b). In addition, the study of phenoliccomposition of different quinoa varieties wouldhelp determine which varieties have the potentialto be more repellent to insects and thus incur lessdamage.

Given the current demand for quinoaworldwide, it is particularly urgent to startimplementing ecological crop management, withbiological control as an integral component.Ecological management of the quinoa crop wouldalso consider restoring traditional agriculturalpractices, such as the use of organic fertilizers,to mitigate soil degradation while taking into

account that soil nutritional quality influences theability of plants to withstand herbivore attacks(Altieri et al. 2012; Ghorbani et al. 2008).

In conclusion, it is vital to conduct researchand promote the sustainable management ofquinoa to preserve plant and animal biodiversitywhere quinoa is grown and to protect the bioticinteractions between quinoa and other Andeancrops. We are convinced that conscious efforts tomanage the quinoa crop in an ecologically sus-tainable framework would preserve this Andeanlegacy for generations to come.

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Chapter 6

Quinoa Breeding

Luz Gomez-PandoUniversidad Nacional Agraria La Molina-Agronomy Faculty, Lima-Peru

HISTORY – DOMESTICATION PROCESS

Quinoa was probably among the earliest culti-vated plants in the Andes region. The earliestarcheological evidence indicates that the pro-cess of quinoa domestication began around5000 BC in Ayacucho, located in the centralhighlands of Peru (Lumbreras et al. 2008) andin several other locations of South America.Remnants of Chenopodium sp. seeds were foundin the Chinchorro Complex of Chile dating to3000 BC, in Indian graves at Tarapaca, Calma,Calchaqui-Diaguita, Tiltil, and Quilagua in Chile(Bollaert 1860; Tapia 1979). The progress ofquinoa cultivation has been studied intensively inthe Lake Titicaca basin in Peru and Bolivia and itwas found as a part of an agricultural complex thatdeveloped during the regional Formative Period,from 1800 BC to AD 500 (Bruno and Whitehead2003). Seeds and fruit of cultivated species ofthe genus Chenopodium were identified frombotanical remnants recovered at the archeologicalsite of Punta de la Peña 4, layer 3, dated to ca.760–560 BC at Sierra, Catamarca, SouthernArgentinean Puna (Rodríguez et al. 2006).

In view of the archeological findings, quinoaimprovement began many thousands of years agowhen men and women started selecting seedsand plants. After centuries of natural and humanselection, the different quinoa phenotypes andgenotypes show adaptation to different partsof the Andean region, similar to the way that


selection has affected hundreds of annual andperennial plant species worldwide (Duvick 1996).Seeds are the only available evidence to show theimprovement of plant characteristics by naturaland human selection through time. The majorchanges reported from the wild types and thedomesticated varieties of chenopods are in themorphology of seeds, specifically those relatedto seed coat thickness, seed size, margin config-uration, and surface patterns. The occurrenceof a thin seed husk and the truncated marginamong the domesticated chenopod seeds reflectsan adaptive response to the selective pressuresof human domestication, in terms of seedlingviability and reduced seed dormancy (Murray2005). Another character affected by humanmanipulation is the color of seeds, as there wasa decrease in the number of black seeds amongsamples of varying ages as determined by C14

dating (Tapia 1979).Farmers from the Highland Andean region

required a complex combination of traits fromthe quinoa that they grew, traits needed to meettheir food needs, and agronomic characteristics toenable them to grow in countless microclimates,from driest to wettest, coldest to hottest, andlowest to highest elevation. The products ofnatural and human selection are five quinoaecotypes, each adapted to a particular growingenvironment. The Salares ecotype is recom-mended for the salt plateau (Salares) of southernBolivia; the Altiplano ecotype for the high plateau

87


(Altiplano) of Peru and Bolivia surrounding LakeTiticaca; the Valley ecotype for the low valleys ofthe highland below 3,800 masl; the Sea-level eco-type for sea level or low altitudes in central Chileand high altitudes in southern Chile; and the Sub-tropics ecotype for the eastern, subtropical slopesof the Andes.

As a result of natural and human selection,complex populations were developed as cultivars,some of which are still used at present. Thevariability of these cultivars is seen in traitssuch as duration of the growth cycle, dormancy(time elapsed between physiological maturity andsprouting), disease resistance, and yield stabilitybecause of tolerance to frost, salt, and drought. Onthe other hand, quinoa cultivars share commoncharacteristics such as plant height, seed color,and quality characteristics related to quinoa enduse and commercialization. Besides importantagronomic criteria, consumption criteria werealso considered by farmers in their selection,such as suitability for traditional dishes or drinksand secondary use of the leaves as vegetables oranimal feed.

Together with potato and maize, quinoabecame an important food source for the IncaEmpire with almost 15 million inhabitants in theAndean region. After the Spanish conquest ofthe region around 1532 AD, quinoa was replacedby crops such as barley, wheat, broad beans, peas,and oats. From that time on until the 1960s,almost 500 years since Pizarro’s conquest, quinoaremained as a neglected crop in the highlands.During this period, quinoa had received littleattention from researchers or scientists, andalmost no commercial advancement. Although itwas largely lost to the outside world, quinoa didnot become extinct because farmers maintainedthis crop mainly in the Peruvian and BolivianAltiplano (Cusack 1984; National ResearchCouncil 1989; Mujica 1992; Jacobsen and Stolen1993).

Beginning in the 1960s, interest in quinoaincreased, eventually leading to the establishmentof several new breeding programs in differentcountries. Several factors have contributed to thisincreased interest in quinoa, namely awareness ofthe role of quinoa in food security in the Andean

South America, its unique potential as a cropfor marginal soils worldwide, and a growinghealth food export market. Genetic improve-ment of quinoa started in Bolivia in 1965 at theExperimental Station Patacamaya supported byFAO-OXFAM (Oxford Famine Relief) and theBolivian Government (Gandarillas 1979a). InPeru, it started almost at the same time in theTechnical University of Altiplano in Puno.

COLLECTION OF GENETIC RESOURCES

Crop genetic improvement in the Andean regionstarted in the 1960s with the collection andcharacterization of quinoa germplasm preservedby the farmers. Gandarillas (1968) made one ofthe first descriptions of quinoa germplasm ofBolivia, Peru, and Ecuador. On the basis of thedescriptors such as plant habit, type of inflores-cence, leaf shape, seed, and leaf dentation number,Gandarillas (1968) described 17 different races ofquinoa: four races in the North of Cusco (Pich-incha, Ancash, Cajamarca, Junin), three races inCusco (Cusco, Sicuani, Puca), four races aroundthe basin of Lake Titicaca (Copacabana, Dulce,Achacachi, Puno), four races in the Andean valleylocated at the southeast of Lake Titicaca (Potosi,Sucre, La Glorieta, Cochabamba), and two racesaround the Poopo Lake basin (Real, Challapata).On the basis of these characteristics and researchconducted on quinoa genetic diversity, it isaccepted that the region with the highest quinoadiversity is located between Cuzco (Peru) andPoopo Lake (Bolivia) (Wilson 1988; Christensenet al. 2007).

Quinoa germplasm and that of otherChenopodium species are mainly preserved ex situ.In Bolivia, around 5,000 accessions are preservedin several institutions, such as the TorolapaCentre of the National Institute of Agricul-tural and Forestry Innovation, the ChoquenairaExperimental Station of the Universidad Mayorde San Andrés-UMSA, the Biotechnologyand Phytogenetic Resources Research Centre(CIBREF) of the Technical University of Oruro(UTO), the Tiahuanacu Academic Unit of theBolivian Catholic University-UCB, the Kallutaca

Quinoa Breeding 89

Experimental Centre of Public University ElAlto-UPEA, and the Centre of CommunalResearch and Promotion-CIPROCOM. Thesegermplasm collections are preserved mainly in theINIAF Toralapa Centre that currently maintains3,121 accessions, both cultivated and wild, whichwere gathered from communities in the Altiplanoand the valleys in the Bolivian departments of LaPaz, Oruro, Potosi, Cochabamba, Chuquisaca,and Tarija. It also has germplasm from Peru,Ecuador, Colombia, Argentina, Chile, Mexico,and the United States. Eight wild species ofquinoa were identified among 270 accessionscollected (Rojas et al. 2010).

In Peru, around 5,351 accessions are alsomaintained in several institutions. The Instituteof Agricultural Research (INIA) at the Experi-mental Station of Illpa preserves 536 accessions.The National University of the Altiplano (UNA)in Puno has a collection of 1,873 accessions thatwere collected in Bolivia (457), Altiplano (990),Valley (357), Colombia (1), Ecuador (18), Chile(8), and the United States (2) (Bravo and Catacora2010). At La Molina Agrarian University, 2,942accessions are preserved, collected from thedepartments of Cajamarca, La Libertad, Ancash,Junín, Ayacucho, Arequipa, Apurimac, Cusco,and Puno, as well as from Bolivia (Gómez andEguiluz 2011). Other universities housing quinoagermplasm are the National University of theCentre in Junín, the National University of SanCristobal de Huamanga in Ayacucho, and theNational University of San Antonio Abad inCusco (Mujica 1992; Bonifacio et al. 2004).

Aside from Bolivia and Peru, there are othercountries that also preserve quinoa germplasm.In Ecuador, around 642 accessions are pre-served at the Santa Catalina ExperimentalStation of the National Institute of Agricul-tural Research-INIAP. In Chile, 25 accessionsare maintained at the Austral University and59 accessions in the North of Chile (Fuenteset al. 2006). In addition, 164 quinoa accessionsare maintained in the USDA National PlantGermplasm System (NPGS) (Christensen et al.2007). The reduction in the genetic diversityof quinoa in countries of the Andean regioncould be a result of founder effects associated

with the dispersal of the crop from its center oforigin or response to selective adaptation to otherecological regions. In the past centuries, the lossof biodiversity probably was due to the systematicdecline and, in some areas, the disappearance ofthe quinoa crop and its use outside the Peruvianand Bolivian Altiplano and the salt flats of Bolivia.

The in situ conservation systems for quinoa arefound mainly in Bolivia and Peru. Germplasm ispreserved by cultivation and utilization of quinoaand wild types through traditional systems infarmers’ communities. In Peru, it is kept in theaynokas, ancient systems maintained for severaldifferent purposes such as food security, adequatemanagement of soils and pests, conservation ofgenetic diversity in situ, and rational use of plantdiversity (Ichuta and Artiaga 1986). In Bolivia,five microcenters have been identified wherefarmers still keep customs and traditions such asbiological indicators or signs during the crop yearthat are used in crop management, rituals, andfestivals. The quinoa crop has a spatial and tem-poral distribution in traditional farming systemscalled aynoqas, sayañas, huyus, and jochiirana.The social system of community organizationsannually elects families called yapu campus orfarm caretakers, who are responsible for the careof crops against adverse weather such as hail,frost, and floods (Rojas et al. 2010b).

In these in situ conservation systems, cultivatedquinoa and wild relatives are preserved. Thesesystems are widely distributed in the Andeanregion and are known by different names such asmandas and laymes (Mujica and Jacobsen 2000).The related wild species growing alongside culti-vated quinoa in the Altiplano and the valleys areChenopodium carnosolum, Chenopodium petiolare,Chenopodium ambrosioides, Chenopodium hircinum,and Swaeda foliosa (Bonifacio 2003; Mujica andJacobsen 2005). The wild relatives are sometimesfound in isolation, either at the edges of thefarmers’ fields or in places considered sacred(Gentilwasi o Phiru). Still, these wild relativesof quinoa are cared for by farmers and used asfood, medicine, or for ritual purposes, especiallyin times of drought or extreme weather disasterscharacteristic of the Andean highlands of Peruand Bolivia. The young leaves of wild quinoa are


used as a salad and the precooked, toasted seed ismade into flour.

Domesticated chenopods are distinguishedfrom wild Chenopodium species on the basis ofseveral characteristics. Domesticated chenopodshave (i) more compacted inflorescences; (ii) losttheir natural seed shattering mechanisms; (iii)uniform maturation of fruit; and (iv) reducedgermination dormancy (Smith 1984; Gremillion1993; Bruno and Whitehead 2003).

Quinoa germplasm has been generally char-acterized and evaluated using the morphologicalcharacteristics of vegetative and reproductiveorgans and agronomic characters such as plantheight, life cycle, yield potential, susceptibility tostress, and resistance or tolerance to pathogensand diseases. In addition, quality characters ofthe seeds such as size and color as well as protein,oil, and saponin content have been used. In somecases, variation in these characters was measuredin different years and locations to determinethe performance of the same genotype in dif-ferent environments (genotype × environmentinteraction). This work has permitted, thoughin a preliminary way, a method of knowingthe magnitude of the variation and the sourcesof genes for many characters, thus facilitatingbreeding programs. A number of this type ofresearch has permitted the formation of core col-lections to simplify the management and enhancethe utilization of quinoa genetic resources(Ortiz et al. 1998).

At present, quinoa germplasm is dividedinto five ecotypes (Tapia et al. 1980). Theseecotypes differ in adaptation to altitude, toler-ance to drought and salinity, and photoperiodresponse. These populations have most likelyreceived different selection pressures from theirenvironments as well as during the domesticationprocess.

1. Valley Type: These quinoas have evolved atvalleys situated at altitudes from 2,000 to3,800 masl. Plants of this ecotype are generally2–3 m in height and have branched stems, alife cycle of more than 210 days, low saponincontent, and some resistance or tolerance todowny mildew (Peronospora variabilis).

2. Altiplano Type: These quinoas originatearound the Lake Titicaca basin that has analtitude of 3,800 to 4,000 masl and is character-ized by adverse conditions (drought, frost, andhail). The plant height ranges from 1 to 1.8 mand the life cycle from 120 to 210 days. Ingeneral, they do not have branched stems andthe seeds are rich in saponin. These quinoasvary in their reaction to downy mildew and canbe tolerant, resistant, or highly susceptible.

3. Salar Type: These quinoas have evolved inthe salt flats of the southern altiplano inBolivia with altitudes around 4,000 masl, lowrainfall (300 mm), and soils having a pH above8.0. The plant characteristics are similar tothe Altiplano ecotype. In general, they haveblack seeds with sharp edges and are rich insaponin. Among the Salar ecotypes, thereare some sweet, saponin-free genotypes andsome “Real”-type quinoa, which have largewhite seeds.

4. Sea Level Type: These quinoas originate fromsouthern Chile, at latitudes around 40∘S. Theyare mostly unbranched and will flower in longdays. They have small, yellow translucent seedswith high saponin content. They are reportedto be resistant to fungal diseases such as downymildew (Fuentes et al. 2009).

5. Subtropical Type: These quinoas are found atthe subtropical Yungas of Bolivia. Plants havean intense green coloration that turns orange atmaturity and produce very small yellow-orangeseeds (Tapia 1982).

After the 1960s, there had been exchanges ofgermplasm among different organizations suchthat the quinoa population distribution of thepast has been changed in different degrees. Somenew sites have been identified in the Americanand European Test of quinoa, organized bythe FAO. Field trials in Italy and Greece haveshown promising results with reported seedyield of 2,280 and 3,960 kg/ha, respectively(Mujica et al. 2001).

Using morphological and agronomic charac-teristics, 95–100% of the quinoa collections ofBolivia had been characterized and evaluated,

Quinoa Breeding 91

whereas 12% of the collections had been evalu-ated using nutritional value and characteristics(Rojas et al. 2010). In a similar way, 100% of thePeruvian collections are being morphologicallyand agronomically evaluated. In the collection atLa Molina National Agrarian University, 43% ofthe collection was evaluated by quality character-istics. Some of the results of these evaluations arepresented in Tables 6.1 and 6.2 and show the widegenetic variability in quinoa collections of Boliviaand Peru.

A limited number of the germplasm studiedfrom Ecuador and Argentina has shown lowdiversity, indicating that the most probable pointof introduction for Ecuadorian accessions was theAltiplano (Peru-Bolivia), whereas for Argentina,the original introduction could have been fromthe Chilean highlands and coastal zone (southof Chile) (Christensen et al. 2007). The otherreasons are probably due to potential genetic driftowing to abandonment of the crop or the isolationof farmer communities.

Table 6.1 Variation in morphological characters of quinoa (Chenopodium quinoa Willd.) described in germplasm from diverseorigins.

Morphological characters Boliviaa Peru (UNALM)c

Color of the plant beforeflowering

Green, purple, red, and mixed –

Color of leaves before flowering – Green, purple, mixed, and redColor of leaf axil – Green, purple, red, and pinkColor of stem streaks – Yellow, green, purple, pink, and redColor of the plant atphysiological maturity

White, cream, yellow, orange, pink, red,purple, brown, and black

–

Color of the Inflorescence atphysiological maturity

– Yellow-green, yellow,yellow-orange, orange, orange-red,red, red-purple, purple,purple-violet, violet, violet-blue,white, white-gray, white-yellow,white-orange, gray-yellow,gray-orange, gray-red, gray-purple,gray-green, gray-brown, brown,gray, and black

Inflorescence shape Amaranthiform, glomerulate, orintermediate

Amaranthiform, glomerulate, orintermediate

Inflorescence density Compact, lax, or intermediate Compact, lax, or intermediateSeed color White, cream, yellow, orange, pink, red,

purple, brown, and blackb–

Seed color pericarp (fruit coat) – Yellow, yellow-orange, orange,orange-red, red, red-purple, white,white-yellow, white-orange,gray-yellow, gray-orange, gray-red,gray-purple, gray-green,gray-brown, brown, gray, and black

Seed color episperm (seed coat) – Yellow, yellow-orange, orange,red-purple, purple, white,white-yellow, white-orange,white-gray, gray-yellow,gray-orange, gray-purple, brown,and black

aRojas et al. 2001; Rojas 2003; Rojas et al. 2008; Rojas et al. 2009bCayoja (1996) reported 66 colors considering different shadescGómez and Eguiluz (2011)


Table 6.2 Agronomical variation and quality characters of quinoa (Chenopodium quinoa Willd.) described ingermplasm from diverse origins.

Peru (UNALM)c

Agronomic and quality characters Boliviaa Altiplano type Valley type

Vegetative cycle (days) 110–210 – –Date of flowering (days) – 46–100 50–115Date of maturity (days) – 115–195 140–220Seed yield per plant (g) 48–250 – –Seed yield (kg/ha)b – 165–2,975 109–3,531Seed diameter (mm) 1.36–2.66 1.4–2.2 1.2–2.2Weight of 100 seeds (g) 0.12–0.60 – –Seed protein content (%) 10.21–18.39 7.0–24.4 10.3–18.5Seed saponin content (%)b – 0–1.42 0–1.57Starch grain diameter (μm) 1.5–22 – –

aRojas et al. 2001; Rojas 2003; Rojas et al. 2008; Rojas et al. 2009bEguiluz et al. (2010)cGómez and Eguiluz (2011)

Chilean quinoa has been characterized asmorphologically diverse and bifurcated intocoastal and highland ecotypes. The quinoa iscultivated primarily by indigenous Aymara in thenorthern Chilean Altiplano. Chilean quinoa ischaracterized by a broad range of morphologicaldiversity that likely resulted from artificial andnatural selection and genetic drift as landraceswere introduced to south-central Chile via tradeand migration of indigenous peoples. Little focuson germplasm collection, conservation, and eval-uation has been placed on the quinoa populationsfound in coastal lowlands of south-central Chile(Fuentes et al. 2009). Bhargava et al. (2007a)evaluated quinoa lines from different originsunder subtropical North Indian conditions andreported that Chilean lines were more adapted tocountries having a monsoon climate such as India,with markedly cold winters and hot summers. Inanother study, G ¸esinski (2008) reported that con-ditions in Europe are favorable to Chenopodiumquinoa for green matter and seed yield, and themost favorable seed yield was recorded in Greece.

There are several studies that have used molec-ular markers in quinoa to characterize germplasmdiversity. According to Rojas et al. (2010), 86%of Bolivian germplasm has been characterizedusing molecular markers. Fuentes et al. (2009)indicated that highland and coastal quinoas fromChile shared 21.3% of alleles. On the other hand,

highland quinoas contained 28.6% of uniquealleles, whereas coastal quinoa had 50% of uniquealleles. Wilson (1988) and Christensen et al.(2007) demonstrated a high genetic similaritybetween highland and coastal quinoas.

GOALS AND METHODS OF QUINOABREEDING

The main aim of quinoa breeders is the develop-ment of cultivars adapted to diverse agroclimaticregions with high seed yield and good qualitycomponents for food and industry use. Thesedesirable cultivars should combine valuablecharacteristics for the farmers, industry, andconsumers.

Requirement of the farmers

Higher yield

The primary objective of most breeding programsis to improve quinoa yield, as the yield of quinoa inthe Andean region is generally low. In the periodbetween 2005 and 2012, the yield in Bolivia rangedfrom 570 to 642 kg/ha; in Peru, it ranged from958 to 1,163 kg/ha, whereas in Ecuador, it rangedfrom 63 to 848 kg/ha (FAOSTAT 2014).

Yield stability is one of the most importantobjectives of any quinoa breeding program.

Quinoa Breeding 93

In some cases, quinoa genotypes that have beenselected for good yield at a given location willnot perform well at another location. Thus, it isimportant to identify genotypes that give goodyields in a broad range of environments. In theAndean region, where subsistence agricultureis prevalent, a cultivar with the ability to give aconsistent yield under variable climatic conditionsis preferred to a cultivar that has the potentialfor outstanding yields but only under favorablegrowing conditions.

To assess the possibility of genetic improve-ment of seed yield, it is necessary to determinethe extent and nature of genetic variation, geno-type (G) × environment (E) interactions, andheritability. According to Bertero et al. (2004),the extremely high levels of environmentalvariation encountered within the quinoa growingregion require breeding and testing strategiesstructured to accommodate the effects of large G× E interactions. Mujica et al. (2001) reportedseed yields of 2,280 and 3,960 kg/ha in Italyand Greece, respectively, from some genotypesselected in the American and European Test ofQuinoa organized by the FAO. These findingsshowed good yield potential for quinoa. Bonifacio(2003) indicated that the improved varietiesobtained at the Patacamaya experimental stationyielded about 1,200 kg/ha on a commercial scalein the Altiplano, though their potential is muchgreater (3 t/ha) with increased inputs and theuse of modern technology. This is a considerableimprovement when compared to 700 kg/haobtained by the farmers using native varieties.However, acceptance of the improved varietiesdepends on their adaptation to local conditionsand their commercial and culinary characteristics.

It is also necessary to study seed size, plantheight, and lodging in relation to seed yield.Correlations among these characters are usefulin determining both favorable and unfavorablecorrelated responses to selection. Bertero et al.(2004) found that simultaneous progress for seedyield and seed size can be expected from selectionbecause no association was found between theaverage cultivar responses for seed yield and seedsize and no associations were found betweenthe G × E interaction effects for both traits.

Bhargava et al. (2007a) reported that plant height,leaf area, branches/plant, inflorescence/plant,seed size, 1,000 seed weight, dry weight/plant,and harvest index exhibited significant positiveassociation with seed, and the maximum valuewas recorded for inflorescence/plant. In anotherstudy, Bhargava et al. (2008) used direct andindirect selection for some parameters. Theyfound that stem diameter, chlorophyll a, totalchlorophyll, and leaf carotenoid content hadhigh correlated response and relative selectionefficiency values for seed yield. Thus, these traitscan be used to increase seed yield. Protein andcarotenoid contents in seed showed negativecorrelated response. Relative selection efficiencyvalues for seed yield indicated that direct selectionfor seed yield would lead to a slight decreasein these quality characters. Bertero and Ruiz(2008) reported a negative association betweenreproductive efficiencies and panicle biomass.Seed size was not of much significance eitherin increasing seed yield or any of the qualitycomponents. Seed yield can also be increasedthrough indirect selection for stem diameter,whereas leaf pigments are likely to play a majorrole in enhancement of quality traits such as leafand seed carotenoid levels.

Plant height

Plant height is generally considered to be aquantitative character, although several reportsindicate that reduced height or semidwarf char-acteristics may be controlled by single recessivegenes. There are significant variations in plantheight among quinoa ecotypes. Plants withshorter heights are usually found among theAltiplano and Salares ecotypes and the tallerplants (more than 2 m high) are found in theValley ecotypes. Plant height could be reduced byselection among genotypes without a semidwarfallele. Another way to reduce plant height is bythe use of mutagens to develop dwarf mutants,as reported by Gomez-Pando and Eguiluz-dela Barra (2013). It is also important to note thatthere are indications of a positive correlationbetween plant height and inflorescence length(Ochoa and Peralta 1988; Rojas et al. 2003).


Stalk strength

Major advances in yield have been achieved bythe development of cultivars with resistance tolodging, planted in highly productive environ-ments managed with good farming technology.Resistance to lodging ensures good seed fillingand minimal harvest loss. In most crops, stemstrength must be dealt with as a quantitative trait.Several individual characters influence resistanceto lodging, including stem diameter, stem outerwall thickness, plant height, and type of rootsystem. The genetic control of stalk strength isalso quantitative.

Life cycle

Another important objective in breeding quinoais the development of early-maturing cultivarsthat can be grown in areas where the averagenumber of frost-free days in the growing seasonis <120–150, such as in the Andean region. Earlymaturing cultivars could also be less vulnerableto inclement weather and have more potentialto fit into multiple cropping systems in thecoastal areas. According to Mujica (1988), thenumber of days to flowering has a heritabilityof 0.82. Late-maturing genotypes frequentlyproduce higher seed yield but run a higher risk ofencountering frost, drought, or hail damage to anunacceptable degree.

Resistance to biotic stresses

Quinoa improvement programs in the Andeanregion have made it a priority to breed for pestand disease resistance, especially because farmersin the highlands can increase their income byselling organic quinoa. Many programs concen-trate on resistance to the fungus P. variabilis, thecausal agent of quinoa downy mildew. Downymildew causes serious yield losses throughout theAndean region and other locations in the world.At a number of locations, the focus has been onscreening germplasm for resistance, and geneticmaterials with different levels of resistance havebeen identified. Ochoa et al. (1999) determinedthe factors of resistance and virulence groups inthe quinoa-downy mildew pathosystem. Using 60

accessions of quinoa in Ecuador and 20 isolatesof P. variabilis, they identified three factors ofresistance and four virulence groups or races ofthe pathogen. The specific interaction betweenfungal isolates and host genes indicated thepresence of major genes. Accessions ECU-291,ECU-470, ECU-379, and ECU-288, were pro-posed as a set of preliminary differentials toidentify pathogenic races of downy mildew inquinoa. However, virulence tests showed that thevariability in P. variabilis is much more complexthan could be revealed using the Ecuadorian C.quinoa differentials used in the study (Danielsenet al. 2000). In India, 34 quinoa accessions wereevaluated for response to downy mildew. Sevenaccessions were found to be resistant, suggestingphysiological specialization of current pathotypesfor C. quinoa (Kumar et al. 2006).

Insects can be very damaging in quinoa, espe-cially when the insects feed on floral structuresor seeds, thus reducing seed yield and quality.Breeding for resistance to insects must considerthe genetics of the pest and the host becausecomplex interactions occur between insects andplants that may be morphological, biochemical,or physiological in nature. Plant resistance maybe obtained through nonpreference (suppressionof feeding or oviposition), antibiosis (adverseeffects on normal growth or survival of insects),and tolerance (ability of the plant to survive wheninsects are present).

Bird predation is another problem in quinoa.Variations in seed saponins, which cause dif-ferences in bird feeding preferences, have beenreported to deter bird feeding and thus decreaseinflorescence damage. Achenes with high amountsof saponin are often less damaged. Developinglines with tolerance to bird predation is a complexprocess, apparently requiring a combination ofmany characters that are independently inheritedbut contribute to overall tolerance.

Resistance to abiotic stresses

Quinoa is cultivated under a wide range ofenvironments in the Andean region. Quinoahas been noted to have tolerance to droughtand salt stresses (Jacobsen et al. 2001; Jacobsen

Quinoa Breeding 95

and Mujica 2002; Jacobsen et al. 2003; Jacobsenet al. 2005; Jacobsen et al. 2007; Gomez-Pandoet al. 2010; Ruiz-Carrasco et al. 2011; Verenaet al. 2013). It is important to understand thegenetic principles and the mechanisms governingtolerance to these factors and apply this knowl-edge to develop improved varieties of quinoa.There are two approaches to achieve drought-and salt-tolerant varieties: breed cultivars witha plant growth type that escapes the water andtemperature stress conditions and/or breed forcharacteristics that contribute to physiologicaldrought and salt tolerance.

Plant morphology

In some cultivars, it will be necessary to modifythe architecture of plants to allow for mechanizedharvesting. The areas devoted to quinoa cultiva-tion have been expanding rapidly and traditionalways of harvesting quinoa must be replaced bymechanical methods. Nonbranched or simplestem plants with an adequate plant height andunique terminal inflorescence and uniformseed maturity will be suitable for mechanizedagriculture.

Harvest index

The harvest index measures the photosyn-thetic capacity and the effective translocationof assimilates to the seeds. The harvest indexcan be modified by agronomic practices andenvironmental growing conditions (Berteroand Ruiz 2010). Rojas et al. (2003) reported avariation in the harvest index of quinoa from 0.06to 0.87. Traditional cultivars, especially valleyecotypes, have low harvest index due to the highamount of branching relative to plant height andmore partitioning of assimilated products to thevegetative parts rather than the seeds.

Requirements of the industryand consumers

Within the quinoa germplasm, significant differ-ences have been found in some qualitative traitsthat can be used in breeding to improve the nutri-tional quality of quinoa.

Protein content and composition

The protein concentration in quinoa seeds, asseen in other crops, is linked with soil nitrogen(N) availability and uptake, N transport andassimilation in the vegetative structures, directN transport and remobilization from plantstructures into developing seeds, carbohydratedeposition in the developing endosperm, andthe number and size of seeds per unit area. Thesecomplex relationships may cause a wide range inprotein percentages for the same genotype grownin different parts of the same field, in differentfields, in different regions, or in different years.The range of seed protein content reportedwas from 7% to 22% (Koziol 1992; Prakashet al. 1993; Wright et al. 2002; Repo-Carrascoet al. 2003; Bhargava et al. 2007a; Gómez andEguiluz 2011). High protein percentage generallyresults from low carbohydrate deposition in thekernel so that increased yield is often associatedwith lower protein content. However, Bhargavaet al. (2007a) reported insignificant correlationand low values of direct path among seed yieldand protein content in quinoa lines of differentorigins and remarked that this result could helpthe development of cultivars with good yieldpotential and high seed protein content.

Quinoa proteins have a remarkably high bio-logical value. However, raising the level of someamino acids is not yet possible at the moment, dueto the lack of knowledge regarding the variabilityof amino acid composition among genotypes andthe effect of environment. Even with this lackof knowledge, this is a promising area of futureresearch because the potential to increase thelevel of some amino acids exists.

Seed characteristics

Color

Until the 2000s, white- or cream-colored quinoaseeds had been preferred by consumers and theindustry. In the past decade, however, quinoawith darker-colored seeds had been incorporatedto the market probably due to the high associationof seed color with carotenoid content. The resultsof Bhargava et al.’s study (2007a) showed that


accessions with dark seed coat color have highseed carotenoid content.

Size of seeds

Another potential goal in breeding quinoa is todevelop cultivars with homogeneous seed size inthe inflorescence. The size of quinoa seed variesfrom <1.4 mm diameter to more than 2.0 mm,and it is very common to find such variability ina single inflorescence (Gómez and Eguiluz 2011).Highly significant correlations between seeddiameter and seed weight have been determinedin quinoa (Ochoa and Peralta 1988; Cayoja 1996;Rojas et al. 2003). Temperature and photoperiodafter anthesis also affect seed diameter to aconsiderable extent. Short photoperiod and cooltemperatures after anthesis promote larger seeddiameters, whereas long photoperiods and hightemperature after anthesis negatively affect seedsize (Bertero et al. 1999; Bhargava et al. 2007a).Large seed size is preferred when the seed is useddirectly as pearled seeds or flakes, whereas seedsize is immaterial when seeds are to be used forflour.

Seed saponin content

The saponin content has different implicationsfor quinoa growers, consumers, and the industry.For the consumers, saponin gives seeds a bittertaste and must be removed from the seed, thusincreasing the time for food preparation. Onthe other hand, under some circumstances,growers will prefer bitter quinoa as the saponincould reduce damage due to birds and cer-tain insects. For the industry, saponin removalrequires specific equipment and a good sourceof quality water, thus increasing processingcosts. Recently, several uses have been found forsaponin, namely as an organic detergent, as foamfire extinguishers, and as deodorant and otheruses in the cosmetic industry. To fulfill thesediffering requirements for saponin content, thereare several accessions in the gene banks withoutsaponin (sweet), with very low content (mediumsweet), and with high levels (bitter) (Ward 2000a;Malt et al. 2006).

Further investigation into the genetic inher-itance of several quinoa characteristics will beuseful in developing methodologies for cultivardevelopment and for determining short- orlong-term breeding goals. Genetic studies inquinoa have provided knowledge regarding theinheritance of some qualitative and quantitativecharacters such as plant color, axillary pigmen-tation, inflorescence type, saponin content, seedcolor and type, genetic and cytoplasmic malesterility, earliness, and plant height (Gandarillas1968, 1974, 1979a, 1979b, 1986; Rea 1969; Espin-dola 1980; Bonifacio 1990, 1995; Saravia 1991;Ward 2000b).

Methods in genetic improvement

Reproductive biology

Quinoa is predominantly autogamous, thoughsome out-crossing is also possible. The sex-ual reproduction system of quinoa providesopportunities to produce new combinations ofgenes or mutations, passing on to the succeedinggenerations traits that might provide superioradaptability to changing environments. Eventhough quinoa is mainly grown from seed, in vitrovegetative propagation of quinoa has also beenreported (Ruiz 2002).

Gynomonoecy is the predominant breedingsystem in quinoa. The inflorescence bears threebasic flower types, namely, hermaphrodite,chlamydeous female, and achlamydeous female.There can be five flower types based on flowersize. On the other hand, there can be 10 flowertypes based on the proportion of hermaphroditeand female flowers and their arrangement andalso on the number of divisions of the dichasiumon the glomerule (Leon 1964; Rea 1969; Bhargavaet al. 2007b).

Quinoa is predominantly autogamous, thoughsome out-crossing is also possible. In studiesconducted in Peru and Bolivia, the amount ofcross pollination of different genotypes variedfrom 1.5% at a distance of 20 m to 9.9% at adistance of 1 m (Gandarillas and Tapia 1976).Some studies in the United States showedsimilar percentages of cross pollination, with

Quinoa Breeding 97

out-crossing exceeding 10% (House 1982;Jennings et al. 1981). In Argentine-Mendoza,out-crossing rates of 17.36% were observed(Silvestri and Gil 2000). The amount of crosspollination depends on (i) the proportion of thedifferent types of flowers in the inflorescence; (ii)the proportion of hermaphrodite flowers on aplant, which can vary from 2% to 99%; (iii) thenumber of androsterile hermaphrodite flowers;(iv) the presence of self-incompatibility and pro-togyny; and (v) the environment and presence ofinsects. Temperatures lower or higher than 30∘Cretard anthesis and affect pollen viability. Windpollination studies of fertile quinoa (CO 407) withan orange panicle crossed with a near-isoline (CO407R) with a red panicle showed that pollen canmove as far as 36 cm. In South America, pollencan be transported by some insects such as thripsand green aphids (Aphis sp.). However, in the SanLuis Valley, Colorado, no insect activity in theflowers was observed, although various Dipteraspp. visit quinoa flowers and may add to winddistribution of pollen (Rea 1969; Gandarillas1979a; Aguilar 1980; Johnson and Ward 1993;Lescano 1994; Silvestri and Gil 2000). However,there are also reports of some extreme cases ofcomplete self-pollination through cleistogamy(Nelson 1968) and obligatory out-crossing dueto self-incompatibility and male sterility (Nelson1968; Gandarillas 1969; Simmonds 1971), indi-cations that quinoa has a fairly versatile breedingsystem.

Male sterility was reported in many quinoaaccessions collected from the Central highlandsand from those growing around the Lake Titicacabasin of Peru-Bolivia and northern Bolivia. Theinheritance of male sterility has been found tobe controlled by nuclear genes and cytoplasmicfactors. Cytoplasm was classified as normal (N)and sterile (S) and the nuclear genes as fertile(Ms) and sterile (ms). Sterile cytoplasm fromthe cultivar “Apelawa” has been denoted asA-cytoplasm, whereas the older source and thatin PI 510536 are referred to as C-cytoplasm(Gandarillas 1969; Saravia 1991; Ward and John-son 1993; Ward 1998). The anthers of normalfertile quinoa are generally bright lemon yellow(Rea 1969), but the anthers of quinoa possessing

a gene for male sterility are whitish-yellow.Plants with male sterile cytoplasm produceflowers without anthers and show a prominentexertion of stigmas, whereas male sterile plantsfrom PI 510536 have shrunken anthers that donot produce pollen (Ward and Johnson 1993;Ward 1998).

The cultivars “Amachuma” and Apelawa aretwo potential sources of male sterile quinoaplants. Male sterility in the Amachuma typeappears to be a simply inherited genetic trait.On the other hand, the Apelawa type is a cyto-plasmic male sterile and has been transferredinto four additional background genotypes.Progeny from the crosses of Apelawa with theweedy species Chenopodium berlandieri had par-tially restored male fertility (Ward and Johnson1993).

Polyploidy level

Polyploidy in quinoa is also an important fac-tor in plant breeding because it can influencereproductive compatibility, fertility, and phe-notypic traits. The base chromosome numberof the genus Chenopodium is n= x= 9 chromo-somes. Quinoa has 2n= 36 chromosomes andis considered an allotetraploid. It is the resultof the cross between two diploid species with asubsequent doubling of chromosomes leading tothe development of a fertile allotetraploid (Gan-darillas 1986; Simmonds 1971; Maughan et al.2004, 2006).

Allelic segregation analysis showed disomicinheritance with independent assortment athomologous loci. Several sources have reportedclassic Mendelian ratios for qualitative traitssegregating in the F2 generation for one or twogene pairs (Cardenas and Hawkes 1948; Gandar-illas and Luizaga 1967; Gandarillas 1968, 1979b,1986; Simmonds 1971; Saravia 1991; Bonifacio1990, 1991). Ward (2000b) reported that allelicsegregation analysis in the F1 and F2 ratiosindicate both disomic-digenic and tetrasomicinheritance in two of the three traits studied,as well as distorted F2 ratios suggesting erraticmultivalent formation at meiosis.


QUINOA BREEDING METHODS

Several breeding methods have been used withquinoa, such as selection (individual selectionand/or mass selection), introduction of foreigngermplasm, hybridization, backcrossing, andinduction of mutation.

Selection

The early stages of quinoa improvement began inthe different areas of the Andean region, drivenby selection of individuals from the naturalpopulations or land races developed throughoutthe centuries. Both individual selection and massselection had been applied.

Individual selection

Individual selection consists of selecting indi-vidual plants with one or more outstandingcharacteristics from a landrace population andsowing a single inflorescence per row. The off-spring are evaluated and selected in and betweenrows for characters under consideration. A modi-fication of this method, named inflorescence-row,follows the same procedure described earlier butwith one difference – selfing of the inflorescenceis controlled in each season. This modifiedprocedure was repeated for two or more cycles,enough to achieve homogeneity (Gandarillas1979a; Bonifacio 2003). Using this method, thecultivar “Sajama Amarantiforme” was obtained.

The selfing process could take place in all theinflorescence or only in some selected glomerulusor group of flowers. When the whole inflorescenceis to be selfed, it is necessary to cover it with agrease-proof paper bag and the leaves removed.When only a small number of glomeruli in theinflorescence are to be selfed, the major part ofthe inflorescence should be removed, and 8–10glomeruli in the base of the inflorescence areselected and isolated from the rest by enclosure ina glassine bag. Plants should be checked period-ically to avoid damage from diseases and insectsbecause isolated glomeruli are often preferred bylarvae that consume growing seeds.

Mass selection

This method consists of the selection of alarge number of superior plants with similarphenotype. Their seeds are then harvested andmixed together to constitute the new variety.Mass selection is applied multiple times in thesame population to improve the base populationperformance as mass-selected cultivars maycontain considerable genetic variation. Cultivarsdeveloped by mass selection have wide adaptabil-ity, a wide genetic base, and yield stability overa long period of time. Characters such as plantheight, plant and seed color, seed size, diseaseresistance, saponin content, and life cycle havebeen considered in the mass selection process.The main characteristic of cultivars developedthrough mass selection is that they are a mixtureof different genotypes, generally uniform in size,seed color, and saponin content, and in othercharacters preferred by the general market andthe industry. In Bolivia, stratified mass selectionwas used to produce seeds of cultivars developedfrom the Real landrace and also used to preservethe identity and composition of establishedcultivars. The most important cultivars obtainedusing mass selection are “Real” (Bolivia), “Baer”(Chile), “Dulce de Quitopamba” (Colombia),“Pasankalla,” “Chewecca,” “Blanca de Juli,”“Amarilla de Marangani,” “Blanca de Junín,”“Rosada de Junin,” and “Blanca de Hualhuas”(Peru).

Participatory plant breeding (PPB)

Although initially developed for smallholderagriculture in difficult and diverse environments,participatory plant breeding (PPB) appears tobe a viable alternative for improving quinoagermplasm in small-scale farmers’ fields. PPBinvolves farmers and other stakeholders in thebreeding process. Stakeholders may work withscientists in any of the five basic steps of the plantbreeding cycle: setting goals, creating variability,selecting experimental lines/genotypes, testingexperimental lines/genotypes, and cultivarrelease/diffusion. In Ecuador, the PPB processeswere applied and the farmers’ field selection

Quinoa Breeding 99

criteria for quinoa were based mostly on yield,earliness, and plant color. At seed selection,farmers with insecure food sources chose linesbased on yield, whereas farmers who had moreresources also considered seed size, color, saponincontent, and marketability in addition to yield(Ceccarelli et al. 2000; McElhinny et al. 2007).

Introduction of foreign germplasm

For the past several decades, germplasm andcultivars of quinoa have been exchanged amongcountries of the Andean region. After a series ofevaluations and multiplications, some of theseintroduced materials have been developed ascommercial cultivars. On the whole, the intro-duction of cultivars from the Bolivian southernaltiplano to the Bolivian northern altiplano andPeru altiplano had not been successful, due to thehigh susceptibility of these quinoas, especiallythe Real race, to downly mildew, although therehave been some exceptions. Similarly, accessionsfrom the Northern and Central Highlands didnot adapt very well because these accessions areof the Valley ecotype, have a long life cycle, andare susceptible to drought and frost. An exceptionis the “Sayaña” cultivar that is currently adaptedto the surrounding area of Uyuni. Cultivarsdeveloped at Patacamaya such as “Sajama,”“Kamiri,” “Huaranga,” and “Chucapaca” wereintroduced by farmers and research institutionsto Peru and had adapted well in Puno. These areused as commercial cultivars mainly because ofthe high quality of their seed. The cultivar “Patade Ganso” from Ecuador was developed fromintroduced Bolivian material.

Quinoa was also introduced to other countriesoutside of the Andean region. Approximately 300accessions from Bolivia, Peru, and Chile havebeen introduced to England (Risi and Galwey1984; Risi 1986). Outstanding accessions ofquinoa from the region selected by differentinstitutions were included in the American andEuropean Quinoa Test, which was conductedin different countries (Mujica et al. 2001). Thepreliminary results showed that accessions fromthe Peruvian and Ecuadorian Valley have goodtolerance to mildew, whereas material from

Bolivia showed high susceptibility to the samedisease. Accessions from the Coast maturedearlier but were highly susceptible to hail atthe highland locations. Adaptation to NorthIndian subtropical conditions were reported byBhargava et al. (2007a) who studied 27 germplasmlines of C. quinoa and two lines of C. berlandierisubsp. nuttalliae over a 2-year period. Seedyield ranged from 0.32 to 9.83 t/ha, with higheryields recorded in four Chilean, two US, oneArgentinian, and one Bolivian line.

Hybridization

Hybridization has been used to improve quinoa.The main objectives of hybridization are to bringtogether desired characters from different acces-sions into one new plant or plant line to improvecertain quantitative characteristics.

Selection of parents

Selection of parents is the first and one of themost important steps in a successful quinoabreeding program. The choice of parents willdepend on the objectives of the program andthe availability of genotypes to meet the specificobjectives. Crossing two genotypes with comple-mentary traits is a common practice. Valuablecharacteristics are scattered among germplasm ofdifferent origin such as saponin-free ecotypes thathave small to medium seed size and bitter eco-types that have large seeds; tolerance/resistanceto mildew (P. variabilis) is present in Valleyecotypes combined with branched stems and along life cycle; Altiplano ecotypes are suscep-tible to downy mildew but have a single stemand mature earlier. All these characters can becombined into one genotype using hybridizationand subsequent selection. Risi and Galwey (1989)concluded that quinoa characteristics requiredfor temperate conditions are available to a largeextent in accessions collected near sea level insouthern-central Chile, whereas seed character-istics are scattered throughout the germplasm.Carmen (1984) recommended the utilization ofearlier genetic material available from the quinoacollection of the Germplasm Bank of AndeanCrops at the Altiplano-Puno National University


(UNAP). Quinoa breeders might focus on intro-ducing resistance to downy mildew from coastalgermplasm to Altiplano germplasm. Conversely,coastal cultivars need the introduction of moreattractive agronomic characteristics, such aslarger seed size, that are present in the Real-typequinoas from the Andean highlands (Fuenteset al. 2009).

Flowering biology

Anthesis in quinoa starts at the apex of eachglomerulus or group of flowers. Hermaphroditeand female flowers generally open at the sametime. Most flowers open in the morning and themaximum number of flowers open at midday.Rain reduces the number of open flowers. Antherdehiscence occurs from early morning until lateafternoon. It is also highest at midday duringwhich large quantities of pollen are produced.Flowers remain open for 5–13 days. In eightlandraces and five commercial varieties of quinoa,the average duration of anthesis was 14.5 days andthe average duration of dehiscence was 18.2 days.An average of 2.5% floral aberrations had beenobserved (Ignacio and Vera 1976; Gandarillas1979a; Lescano 1980).

Emasculation and pollination procedure

Procedures for artificial hybridization of quinoahave been described by Rea (1948), Gandarillasand Luizaga (1967), Gandarillas (1979a), Lescanoand Palomino (1976), and Bonifacio (1990, 1995).Emasculation techniques and artificial pollinationare often simple procedures in many other cropsbut are quite laborious in quinoa due to inflores-cence characteristics and extremely small flowersize. Quinoa crosses can be made in the fieldand in the greenhouse but it is very importantto have favorable environmental conditions forplant growth and development. Crosses between“Pasankalla” × “Salcedo” INIA and “Pasankalla”× “Choclo” made under field conditions resultedin 41% and 63% seed set in the female parent,respectively (Leon 2004, 2005).

Crossing may be simple or reciprocal, but inall cases, it is important to have one or more

morphological markers or qualitative characterspresent in one of the parents, to be used asmorphological marker to identify the hybrids inthe F1 generation. The female parental line musthave the recessive character and the male parentalline the dominant character. It is also important toselect parental lines that can withstand handlingduring the whole process, which can take 10–14days. The female parent must tolerate repetitiveemasculation and pollination and the male parentmust provide an adequate amount of viable pollen.

The equipment needed for crossing consistof small scissors with sharp and pointed blades,finely tipped forceps or needles, glassine bags,paper clips or staples, and small tags. The femaleplant must be prepared by choosing two or threeequidistant glomerulus from the base of theinflorescence before flowering time. Leaves of theinflorescence must be removed, retaining onlyone leaf under each glomerulus and the rest of theinflorescence also removed. The optimum timeto emasculate quinoa flowers is when the anthershave obtained full size but are not yet ready todehisce. Hermaphrodite flowers are chosen foremasculation, which is the process of removingthe anthers with a needle before they have shedpollen without damaging the stigmata. Afterwhich, the female flowers of the glomerulus areretained. Five anthers in each inflorescence mustbe removed. The process can take 10–14 days.The inflorescence must be covered with a glassinebag or a paper bag depending of the size of theinflorescence to exclude unwanted pollen once theprocess has been initiated. The bag should be justwide enough to cover the inflorescence and longenough to be folded and stapled or secured with apaper clip. In the field, crossed inflorescences aresometimes supported by a stake. An identificationtag must be used, containing the names of parentlines, the date of emasculation, and the name ofthe operator.

Emasculation using hot water (42∘C), as in thecase of sorghum (Alvarez 1993), has not been suc-cessful in quinoa. The use of the suction pumprecommended for rice (Jennings et al. 1981) hasnot been tested in quinoa, though presumably itwill be ineffective due to the tightly closed peri-anth lobes enveloping the anthers.

Quinoa Breeding 101

Clear days with temperatures near to 24∘C areideal for gathering viable pollen. Cloudy dayswith high relative humidity and low temperature,near or below 15∘C, are not favorable for anthesis.Quinoa pollen must be collected in a watchglass, paper bag, or Petri dish. The selectedinflorescence must be bent over and shaken tocollect pollen. Viable pollen can be recognizedby the appearance of fine yellowish powderwithout agglutination, whereas old pollen showsagglutination and the presence of pollen sacs.

The phenomenon of male sterility in quinoacan also be utilized in crossing quinoa. However,using male sterility requires prior development ofmale sterile lines and maintainer lines, as well asthe introduction of male sterility into the selectedparents for each cross. Conversely, if there areexcellent lines possessing male sterility, theycan be used directly as female parents withoutbeing emasculated. The process begins with theidentification of male sterile plants, in whichapical parts of the inflorescence must be removedto eliminate any flower that could have alreadyreceived foreign pollen. Plants are then isolatedfor 1 week and flowers forming seed are removed.Male sterile plants (to be used as female parents)are then pollinated with pollen collected fromthe male parent. Pollination can be repeated fora second time to ensure greater seed production.Ward and Johnson (1993) made crosses usingmale sterility, where the selected male parent wasplaced next to the male sterile plant. This methodis simple and may be applicable in greenhousesfor a single or few crosses where foreign pollencontamination can be easily controlled.

Bulk or mass selection

The F2 population must be large so that there areenough recombinant plants to develop a new pop-ulation combining desirable characteristics. Bulkselection, pedigree selection, and the single-seeddescent (SSD) method could be used to managethe segregating population.

Bulk selection is a preferred breeding methoddue to its simplicity and low labor cost. Plantsfrom F2 to F6 are harvested in bulk. The follow-ing year, a sample of the bulk in each generation

is planted in a plot with the expectation thatnatural selection will reduce the frequency ofmaladapted types in the population. In quinoa, itis recommended to have more than 30,000 plantsin each generation for mass selection. At the F6generation, plants are considered to have thedesired level of homozygosity and breeders makeinflorescence selections. In the next generation,inflorescence rows are planted. Each is treated asa line and yield trials are begun.

In Bolivia, the cultivar Sajama was developedfollowing this method. In the F2 generation, allthe bitter plants were discarded. In the followinggenerations, plant vigor, seed size, compactinflorescence, and sweet seeds were the traits usedin the selection procedure (Gandarillas 1979a,1979b). Other varieties obtained by this methodare “Chucapaca,” “Huaranga,” and “KamiriRobura” (Bonifacio 2003).

Individual or pedigree selection

Individual or pedigree selection requires themaintenance of records on selected material, fromF2 to F6 or until the generation when the seed isbulked to start yield trials. Each F2 plant selectedfrom a cross is identified by the number of thecross and selection number. Inflorescence rowsare grown from each F2 plant and selection ismade among and within the F3 progeny rows.Each plant selected is identified by a number,and seeds from each plant are grown as the F4progeny. This procedure can be continued untilthe desired level of homozygosity is reached, atwhich point seeds within selected rows are bulkedand planted as new lines in yield trials.

In the F2 or F3 generation, it is advisableto select for the most heritable characterssuch as sweet seeds, color of inflorescence,and color of seeds. In the F3, F4, or moreadvanced generations, selection will be made forcharacters controlled by multiple genes. Morerecently, this method has been modified by theinflorescence-row systems.

In Bolivia, in a joint effort among thePROINPA 2002-2003, PREDUZA, andMcKnight projects, a cross with 25 diverse


parental varieties was made to obtain 36 suc-cessful crosses that generated true F1 hybrids.The F2, F3, and F4 generations were managedusing two generations per year in a “waliplini”(semi-subterranean greenhouse). The progenieswere selected for favorable characteristics, suchas resistance to mildew, large seed size, earlymaturity, white and colored seeds, and plantvigor. Advanced generations were tested in a yieldtrial in five locations. Line L-26(85) was selectedbecause of its yield, earliness, and seed size. It wasreleased as a new variety with the name “Jach’aGrano,” which in the native language means“large seed” (http://www.proinpa.org).

Combination of individual and mass selection

A combination of individual selection and massselection can also be used in the F2 population.The combination permits the evaluation of theindividual offspring and the broadening of thegenetic base of future varieties. The varietiesobtained by this combined method are “Sayaña,”“Jilata,” “Patacamaya,” “Ratuqui,” “Jumataki,”“Intinaira,” “Surumi,” and “Santamaria”(Bonifacio 2003).

Single-seed descent

In the SSD method, the objective is to maintaina high level of heterogeneity among a largernumber of plants in a population as they arebrought rapidly toward homozygosity. The basicprocedure is to remove one or two seeds from theinflorescence of selected plants from the F2 to F6generations. In quinoa, due to the small size ofseeds and the difficulty in the initial establishmentof the plants, it is recommended to remove 5–10seeds in each plant per generation. After plantingall seeds, the most vigorous plant is chosen to beadvanced. The SSD method advances cycles inthe greenhouse and field and reduces the timeneeded to develop a new cultivar. The F7 andmore advanced generations are grown in the field,and outstanding plants are selected with farmerparticipation.

Interspecific and intergeneric crosses

Interspecific crosses (simple and reciprocal) aredone in quinoa to recombine favorable traitspresent in different species and concentrate themin the selected offspring. However, hybrid sterilityhad been observed, with fertility only restoredthrough backcrossing (Bonifacio 1995). It was alsopossible to obtain hybrids from the intergenericcross between quinoa and Atriplex hortensis, buthybrid sterility was more difficult to overcome.Another intergeneric cross between quinoa andS. foliosa showed that high level of frost and saltresistance present in Swaeda (Kauchi) may beincorporated into quinoa (Bonifacio 2003).

Backcross method

The backcross method can be used improve acultivar that is outstanding in many traits but isdeficient in certain qualitative characters. Oneexample is the work done in Bolivia, where theline 1638 (donor parent) was crossed with thecultivar “Patacamaya” (recurrent parent). Thedonor parent is an accession of the Real race, aPandela (pink) type with large bitter seeds and therecurrent parent is green in color and has sweetseeds. The resultant F1 was a Pandela (pink) typewith bitter seeds. The F1 was backcrossed to thePatacamaya cultivar, resulting in progenies thatare of a Pandela (pink) type cultivar with large,sweet seeds. Backcrossing has also been usedprimarily after cultivated and wild progenitorswere crossed to clean up the genetic backgroundof the progeny (Bonifacio 2003).

Using heterosis in quinoa

Hybrid vigor in quinoa, as observed by Wardand Johnson (1993), has generated interest inthe production of commercial hybrids. Wilson(1990) differentiated groups in quinoa, which arethe result of crosses between accessions of verydifferent origin and sources of male sterility. InColorado crossing trials, quinoas within Wilson’sdesignated groups have shown no heterosis foryield, whereas crosses between his groups have

http://www.proinpa.org

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shown heterosis varying between 201% and491% (Wilson 1990).

Mutagenesis

The advantage of nuclear techniques such asmutagenesis, compared to conventional methodssuch as hybridization and recurrent selection,is that a single or few traits can be targeted forimprovement in local or native cultivars that arealready superior in many traits. Hybridizationinvolves the recombination of parental genomebut the selection of target traits will require a largeamount of time and land. In contrast, the use ofmutagenesis to select for target traits can be fasterand with less use of land and other resources. Thefirst work on mutagenesis in quinoa was reportedin Peru (Gomez-Pando and Eguiluz-de laBarra 2013). Dry seeds of the cultivar Pasankallawere irradiated with gamma rays at doses of150, 250, and 350 Gy. In the M1 generation, thegermination process was delayed with increas-ing radiation dose, whereas seedling height, rootlength, and leaf development were mostly reducedat a dose of 250 Gy. At the 350 Gy dose, no plantssurvived. In the M2, the maximum spectrumof chlorophyll mutations corresponded to the150 Gy dose, whereas the maximum frequency ofchlorophyll mutations were at 250 Gy. The chlo-rine mutation was predominant, followed by thexanthan mutation. In both doses, changes wereobserved in branch number, pedicel length, plantheight, life-cycle duration, stem and foliage color,and leaf morphology, with overall improvementsin plant type, especially with increased vigor andyield potential. More than one mutation per plantwas found, especially at the 250 Gy. In the M3,the same spectrum of mutations was observed,along with desirable changes such as reduction inplant height. Some quinoa traditional cultivarscan reach more than 2 m, are prone to lodging,and present difficulties in harvesting. In suchcultivars, reduced plant height is desirable.Changes in seed color (from red to white) can alsobe achieved, especially to target markets wherethe white seed color is preferred (Gomez-Pandoand Eguiluz-de la Barra 2013).

Marker-assisted selection (MAS)

Modern techniques that permit the use ofmarkers linked to quantitative trait loci (QTL)in quinoa could be exploited for future culti-var improvement. In a joint effort among thePROINPA, PREDUZA, and McKnight projects,a medium-density genetic map was developed.Hundreds of single-sequence repeat (SSR) andsingle-nucleotide polymorphism (SNP) markershave been developed by scientists at the BrighamYoung University (BYU) and are being mappedto three mapping populations to produce ahigh-density genetic map for marker-assistedselection (MAS) in Bolivia. Molecular markersfor important traits such as resistance to mildew,saponin content, and seed protein content andcomposition had been mapped using these mark-ers (Maughan et al. 2004; Coles et al. 2005; Masonet al. 2005; Stevens et al. 2006; Jarvis et al. 2008;Rodriguez and Isla 2009), making it possible touse MAS in quinoa breeding programs.

CONCLUSION

Genetic improvement of the quinoa crop can beachieved by various methods such as classicalbreeding, mutagenesis, and molecular geneticstechniques to obtain outstanding genotypes.Quinoa is an underutilized crop that could be avaluable alternative crop to help the world facecritical challenges such as climatic change, foodsecurity, human nutrition, and overdependenceon a few plant species for the world food supply.

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Chapter 7

Quinoa Cytogenetics, Molecular Genetics,and Diversity

Janet B. Matanguihan1, Peter J. Maughan2, Eric N. Jellen2, and

Bozena Kolano3

1Department of Crop and Soil Sciences, Washington State University, Pullman, WA, USA2Plant and Wildlife Sciences, Brigham Young University, Provo, UT, USA3Department of Plant Anatomy and Cytology, University of Silesia, Poland

INTRODUCTION

Quinoa, Chenopodium quinoa, is the domesti-cated South American member of a complexof allotetraploid taxa (2n= 4x= 36) native tothe New World. This complex includes theweedy North American Chenopodium berlandierisubsp. berlandieri, the weedy and malodorousSouth American Chenopodium hircinum, andthe two domesticated Mesoamerican forms ofC. berlandieri subsp. nuttalliae. An additionalmember of the complex, now extinct but knownfrom archeological remains, was the domesticatedeastern North American C. berlandieri subsp.jonesianum (Smith and Yarnell 2009).

Quinoa’s importance as an internationallyexported food crop has expanded greatly withinthe past decade. As cultivation of this crop movesout of the highland Andes and relatively isolatedcoastal lowlands of central and southern Chile,there is a real danger that the crop will contractnew diseases and pick up new pests against whichit does not currently harbor genetic resistance.Consequently, existing quinoa breeding programsin the Andean region will need to pay moreattention to germplasm diversification. Emergingquinoa breeding programs in other parts of the


world, particularly in the Eastern Hemispherewhere quinoa’s close genetic cousins of the lamb-squarters complex (Chenopodium album et al.)have been widespread weeds for thousands ofyears, will need to be extra vigilant in identifyingand exploiting existing genetic variation forpest and disease resistance in C. berlandieri andother taxa cross-compatible to C. quinoa. In thischapter, we describe the cytogenetic and genomicstructure of quinoa – information that points topotentially close genetic relatives and, therefore,exploitable exotic gene sources – along with aseries of advanced, DNA-based molecular genetictools to facilitate and accelerate the transfer ofexotic genes into C. quinoa.

CYTOGENETICS AND GENOMESTRUCTURE OF CHENOPODIUM QUINOA

C. quinoa is an allotetraploid species with 2n = 4x= 36 chromosomes. Its haploid genome size (1Cvalue) has been estimated at between 1.005 and1.596 pg (Bennett and Smith 1991; Stevens et al.2006; Bhargava et al. 2007a; Palomino et al. 2008;Kolano et al. 2012a). This discrepancy in genomesize among different reports could be due either

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to intraspecific polymorphism in genome sizeor to the use of different measurement meth-ods.Until now only limited intraspecific genomesize variation (5.9%) was demonstrated for thisspecies (Kolano et al. 2012a). The cytogeneticcharacterization of the quinoa karyotype hasstill been limited, partly due to its somaticchromosome morphology and a scarcity of chro-mosome markers. Quinoa chromosomes are small,ranging from 0.94 to 1.60 μm, and are mainlymetacentric (Bhargava et al. 2006; Palominoet al. 2008). Methods of classical cytogeneticsallowed for characterization of the distributionof heterochromatin in quinoa chromosomes.The heterochromatin revealed by C-banding islocated preferentially in centromeric and pericen-tromeric positions in most quinoa chromosomes;however, the size of the heterochromatin blocksdiffered considerably among chromosomes(Fig. 7.1a, Kolano unpublished). Other types ofheterochromatin bands were distinguished usinga GC-specific fluorochrome – chromomycinA3 (CMA). Two CMA+ bands were observedin one pair of homologous chromosomes in

the terminal position. These CMA+ bandscolocalized with secondary constructions andAgNOR bands, indicating that this type ofheterochromatin is correlated with 35S rRNAgene loci (Fig. 7.1b, Kolano et al. 2001).

The rRNA genes were the first tandem repet-itive sequences mapped to the quinoa karyotypeusing fluorescence in situ hybridization (FISH).The 35S RNA gene loci were localized in theterminal regions of two chromosomes. The5S rRNA genes were arranged in two pairs ofloci – one of them was located in the termi-nal position and the other interstitially in twodifferent chromosome pairs (Maughan et al.2006). These results showed that one or morepairs of the 35S rDNA loci were deleted duringquinoa evolution because the locus numberwas lower than the expected additive valuesof any known diploids. This phenomenon wasalso observed for other polyploid Chenopodiumspecies, such as the tetraploid C. auricomum andhexaploid C. album (Kolano et al. 2012b). Theother tandem repetitive sequence mapped inquinoa chromosomes was a telomeric repeat.

(a)

(b) (d)

(c)

Fig. 7.1 Metaphase plates of Chenopodium quinoa (a) after C-banding and (b) stained with CMA3. Localization of (c)Arabidopsis-type telomere repeat and (d) clone 12-13P on metaphase chromosomes of quinoa. Scale bar = 5 μm.

Quinoa Cytogenetics, Molecular Genetics, and Diversity 111

Quinoa has an Arabidopsis-type telomere repeatlocated exclusively in the terminal positionin each chromosome arm (Fig. 7.1c, Kolanounpublished). Centromeric and pericentromericlocalization in quinoa chromosomes was iden-tified for clone 12-13P (Fig. 7.1d, Kolano et al.2011). This repetitive sequence showed partialhomology to satellite DNA (pBC1447) detectednear the centromere of Beta corolliflora chromo-somes (Gao et al. 2000). Hybridization signals of12-13P were observed in each chromosome of C.quinoa; however, the intensity of the FISH signalsdiffered considerably among chromosomes indi-cating that varying numbers of 12-13P repeats arepresent at each locus. The pattern observed on C.quinoa chromosomes after FISH with 12-13P wasvery similar to C-banding results, suggesting thatthe 12-13P sequence constituted a major part ofthe heterochromatin of C. quinoa (Kolano et al.2011). The 12-13P sequence also hybridized tocentromeric and pericentromeric chromosomalregions of related North American tetraploidC. berlandieri as well as European accessionsof hexaploid C. album; however, the intensityof hybridization signals was somewhat lower(Kolano et al. 2011).

The second group of repetitive DNA, whichare dispersed repetitive sequences, comprisemainly mobile elements (retrotransposons andDNA transposons). Kolano et al. (2013) ana-lyzed the chromosomal distribution of reversetranscriptase-coding fragments of LTR retro-transposons and discovered that both Ty1-copiaand Ty3-gypsy retrotransposons were preferen-tially located in pericentromeric heterochromatinof quinoa chromosomes. Apart from retro-transposons, dispersed distribution in quinoachromosomes was demonstrated for two repet-itive sequences (pTaq10 and 24-18J) withouthomology to mobile elements. The first sequence,pTaq10, hybridized across the quinoa genome,without a specific chromosome or subgenomedistribution pattern (Kolano et al. 2008a). In con-trast, the second dispersed repetitive sequence,24-18J, hybridized primarily to one subgenome(18 chromosomes) of quinoa (Kolano et al. 2011).A similar hybridization pattern was observed forC. berlandieri, which supports the hypothesis that

C. berlandieri and C. quinoa are descended fromat least one common diploid ancestor (Maughanet al. 2006). Both C. berlandieri and C. quinoashare the A-genome (Chenopodium standleyanum)and the B-genome (Chenopodium ficifolium, OldWorld). After allopolyploid speciation of C.quinoa and C. berlandieri, at least one of theancestral subgenomes experienced loss of the35S rRNA gene locus. Comparison of the chro-mosomal distributions of 18–24J homologousand rDNA sequences revealed that in quinoaand C. berlandieri, rRNA gene loci were retainedin the subgenome to which 18–24J abundantlyhybridized (Kolano et al. 2011). As probe 18-24Jalso abundantly hybridized to metaphase chromo-somes of a diploid form of Eurasian C. album, aswell as to one of the subgenomes in allohexaploidC. album, we conclude that this subgenomeoriginated in the Eastern Hemisphere (Kolanoet al. 2011).

Another item of interest with respect to quinoacytogenetics is that C. quinoa is a polysomaticplant (Kolano et al. 2008b). Polysomaty isthe occurrence of cells with different ploidylevels in the same organ or tissue (Joubesand Chevalier 2000). During quinoa seedlingdevelopment, endopolyploid cells (cells withmore than the 4C DNA value) were observedin roots, hypocotyls, and in young cotyledons.Its tissues comprised a mixture of cells withDNA content ranging from 2 to 16 C in varyingproportions and the polysomaty patterns cor-responded to the developmental stage and theindividual organ. Endopolyploidization was notpresent in nuclei from leaves and the shoot apex(Kolano et al. 2008b).

CROSSABILITY OF QUINOA AND ALLIEDTETRAPLOID TAXA

The New World allotetraploid “quinoacomplex” consists of three taxa that arecross-compatible – C. berlandieri, C. hircinum,and C. quinoa. This is an important observationbecause the extensive geographical distributionof weedy C. berlandieri, from Alaska and theCanadian Maritimes in the north to Mesoamerica


and perhaps the northern Andes in the south,suggests that this taxon possesses a wealth ofgenetic diversity, including novel pest and diseaseresistance genes (Jellen, personal observations).Similarly, the native range of C. hircinum in SouthAmerica extends across the temperate and sub-tropical lowlands of the Argentinian pampas, anarea in which it has been in contact with invasiveEurasian pests and pathogens since the period ofthe Spanish Conquest. Heiser and Nelson (1974)first reported that quinoa×Mexican huauzontle(C. berlandieri subsp. nuttalliae) domesticatedhybrids were fertile; interestingly, the hybridshad dark seed, unlike either parent. Wilson(1980) again reported that quinoa×weedy C.berlandieri and quinoa× huauzontle hybrids werefertile. Wilson and Manhart (1993) providedisozyme-based evidence that >30% of the off-spring of C. berlandieri plants surrounding quinoafields in the Pacific Northwest carried allelestransferred sexually from quinoa; these hybridswere also partially fertile and displayed heteroticphenotypic effects.

At Brigham Young University (BYU), we arecurrently analyzing F3 plants derived from a crossbetween a large-seeded weedy C. berlandieri var.macrocalycium (BYU 803, from Maine) and high-land quinoa cv. “Ingapirca.” The F2 generationplants were highly diverse and phenotypicallyvigorous, though between 10% and 30% hadvarying degrees of pollen sterility, presumablydue to summer greenhouse heat stress. In total,19 of the 115 F2 plants displayed phenotypicevidence of hybrid breakdown, including leafwhorling, abnormal coloration, or dwarfing. Allof the recovered seed had the wild, black-pericarptrait from BYU 803 (Jellen unpublished). Morerecent DNA sequence evidence, however, sug-gests that C. berlandieri var. macrocalycium is arelatively distant member of the allotetraploidcomplex and may have a different origin or at leastintrogression from a different diploid species(Jellen and Walsh unpublished).

With respect to crossability between the NewWorld allotetraploid complex and Eurasian-originC. album, Wilson (1981) failed to detect transferof isozyme marker alleles from C. hircinum tosympatric populations of allohexaploid C. album.

Consequently, as quinoa begins to be cultivatedmore extensively in areas of the world wherelambsquarters is a common weed, transfer ofexotic alleles into the quinoa crop from thissource is probably not going to be an issue, nordoes C. album appear to be a promising source ofbreeding alleles to improve quinoa’s biotic stressresistance.

DNA SEQUENCE EVIDENCE FOR QUINOA’SGENOMIC ORIGINS

Maughan et al. (2006) sequenced portions of 35SrRNA gene NOR intergenic spacer (IGS) and 5SrRNA gene nontranscribed spacer (NTS) regionsfrom five cultivars of C. quinoa and a weedyaccession of C. berlandieri. They also performedFISH on metaphase chromosome preparationsof both species along with domesticated C.berlandieri subsp. nuttalliae to verify locus copynumbers. While subsp. nuttalliae had either oneor two 35S loci – presumably, the ancestral locusnumber in an allotetraploid – both the weedyaccession and C. quinoa carried only a singlelocus. However, for 5S, the subsp. nuttalliaegenotypes carried three loci, whereas C. quinoaand weedy C. berlandieri had only two. DNAsequencing experiments identified two NTSsequence variants in C. quinoa – apparently,from each of the two loci – one of which wasalmost an exact match (196/200 bases) with thesequence of the weedy C. berlandieri clone. Theother NTS sequence was much more divergent(158/200 bases). The IGS region was moredivergent among five varieties of quinoa and asingle weedy C. berlandieri; the latter possesseddifferent numbers of B, C, and H subrepeats thanthe former, while the five quinoa varieties variedmostly for SNPs. These combined observationssuggest that ancestors of quinoa and the weedyaccession of C. berlandieri lost different 35S loci;this hypothesis could be tested by sequencing thetwo IGS loci in subsp. nuttalliae.

Another gene studied extensively is Salt OverlySensitive 1 (SOS1), which encodes a plasmalemmaNa+/H+ antiporter protein (Shi et al. 2000).The two full-length genomic orthologs from


quinoa were previously cloned and sequenced(Maughan et al. 2009a) and introns 16 and 17 wereselected for further phylogenetic study. Extensivesequencing of introns 16 and 17 of SOS1 in anumber of cultivated and weedy Chenopodium taxaand quinoa cultivars at the 2x, 4x, and 6x ploidylevels has confirmed the Eurasian and New Worldorigins of the two constituent subgenomes of C.quinoa, C. berlandieri, and C. hircinum (Walshet al. manuscript in preparation). The New Worldsubgenome is now referred to as “AA” and theEurasian subgenome as “BB.” These studieshave also pointed to a North American origin ofthe allotetraploid, followed by dispersion – mostlikely as a wild or weedy ecotype – to SouthAmerica (C. hircinum), with domestication eventsoccurring on both continents.

QUINOA GENETIC MARKERS ANDLINKAGE MAPS

The recent awareness of the importance of quinoain food security of the Andean region as wellas a growing export health food market hasled to the establishment of several new quinoabreeding programs. In addition to germplasmmanagement, principal objectives of these pro-grams include enhancing grain yield, earliness,disease resistance, drought tolerance, and modu-lating saponin content (Ochoa et al. 1999). Theseprograms recognize that the development anduse of molecular markers is critical to meetingthese objectives (Bonifacio, PROINPA personalcommunication).

Marker-assisted selection methods, includ-ing association mapping applied directly tobreeding populations (Kraakman et al. 2004;Crossa et al. 2007) and genomic selection(Jannink et al. 2010; Windhausen et al. 2012),are quickly becoming the commercial standardfor enhancing breeding efficiency (Eathingtonet al. 2007; Moose and Mumm 2008). Key tothese enhanced breeding methodologies is easyaccess to numerous, inexpensive, reliable, andeasily scored genetic markers. Unfortunately,few researchers have reported the developmentand use of molecular markers in quinoa. Wilson

(1988a) reported the development of the firstset of allozyme markers, whereas Fairbankset al. (1990) identified the first seed proteinsvariants within the USDA quinoa germplasmcollection. Ruas et al. (1999) reported the use ofrandomly amplified polymorphic DNA (RAPD)markers to detect DNA polymorphisms amongseveral C. quinoa cultivars and Chenopodium weedspecies. Maughan et al. (2004) used amplifiedfragment length polymorphism (AFLP) markersto generate the first low-resolution linkage map ofquinoa. Unfortunately, all of these markers havehad only limited utility in breeding programs,due at least in part to the inherent problems ofcost, reproducibility, and technology transfer ofthese types of markers, especially to laboratoriesin the developing world where resources arelimiting.

In an attempt to make quinoa marker technol-ogy more widely available, Mason et al. (2005)and Jarvis et al. (2008) developed the first largesets (>400) of microsatellite (also termed simplesequence repeats or SSRs) markers for quinoa.Jarvis et al. (2008) also reported the first quinoalinkage genetic map consisting primarily ofmicrosatellite markers. This early map was com-posed of 38 linkage groups (n= 18) and coveredjust over 900 cM. Microsatellite loci consistof short tandemly repeated nucleotide motifsflanked by conserved sequences (Tautz 1989).Polymorphism is detected as variation in thenumber of repeat units among individuals usingstandard polymerase chain reaction (PCR) tech-niques (Weber and May 1989). Microsatellitesare multiallelic and generally more informative,based on polymorphic information content(PIC) values, than RAPD or AFLP markers(Powell et al. 1996). Microsatellite loci, whileubiquitous in eukaryotic genomes (approximately1 microsatellite per 33 kb in plants; Chawla 2000),are not the most abundant marker type.

Single nucleotide polymorphisms (SNPs) arethe most abundant type of DNA polymorphismfound in eukaryotic genomes (Garg et al. 1999;Batley et al. 2003) and are the marker of choice inmarker-assisted plant breeding programs (Batleyand Edwards 2007; Eathington et al. 2007). Thehigh frequency of SNPs in plant genomes is


well documented (Russell et al. 2004; Ossowskiet al. 2008), with actual SNP densities rangingdramatically depending on the species type(auto- or allogamous), number and geneticdiversity of the cultivars being assessed, andwhether coding or noncoding regions are beingconsidered. For example, in soybean [Glycinemax (L.) Merr.], SNPs occur at a frequencyof 1 per 2038 bp in coding sequence and 1 per191 bp in noncoding sequence (Van et al. 2005),whereas in maize (Zea mays L.), 1 SNP wasobserved per 124 bp of coding sequence and 1per 31 bp in noncoding regions (Ching et al.2002). In quinoa, Coles et al. (2005) identified 38single-base changes and 13 insertions–deletions(indels) in 20 EST sequences analyzed acrossfive quinoa accessions, suggesting an average of1 SNP per 462 bases and 1 indel per 1812 bases.The high frequency of SNPs in most speciesoffers the possibility of constructing extremelydense genetic maps that are particularly valu-able for map-based gene cloning efforts andhaplotype-based association studies.

Several technical methods have been reportedfor the initial discovery of SNPs in plant genomes,specifically (i) EST sequencing (Barbazuk et al.2007); (ii) targeted amplicon resequencing(Bundock et al. 2009); (iii) gene space rese-quencing with methylation-sensitive digestion(Gore et al. 2009; Deschamps et al. 2010); and(iv) genomic reduction based on restriction siteconservation (Maughan et al. 2009b). Whencombined with next-generation DNA sequencingtechnologies, these methods can be used toidentify large numbers of SNPs with limitedtechnical expertise and at minimal cost. SNPs canthen be cost-effectively genotyped using severalnext-generation technologies, including beadarrays (Shen et al. 2005), nano-fluidic devices(Wang et al. 2009), and genotyping by sequencing(Miller et al. 2007; Maughan et al. 2010; Elshireet al. 2011). In 2012, Maughan et al. reported theuse of a reduced representation protocol and geno-typing by sequencing to identify >14,000 putativeSNPs in five bi-parental quinoa populations.Transition mutations (A/G or C/T) were themost numerous, outnumbering transversions(A/T, C/A, G/C, G/T) by 1.6× margin,

which was in accordance with the observationthat transition SNPs are the most frequentSNP type reported in both plant and ani-mal genomes and are thought to result fromhypermutability effects of CpG dinucleotidesites and deamination of methylated cytosines(Zhang and Zhao 2004; Morton et al. 2006).Maughan et al. (2012) converted 511 of theputative SNP into functional SNP assays.A diversity screen of 113 quinoa accessions usingthese 511 SNPs clearly revealed the two majorquinoa subgroups corresponding to the Andeanand coastal quinoa ecotypes (Maughan et al.2012). Minor allele frequency of the SNPs rangedfrom 0.02 to 0.50, with an average MAF of 0.28.Linkage mapping of the SNPs in two recombi-nant inbred line populations (KU-2× 0654 andNL-6× 0654) produced an integrated linkagemap consisting of 29 linkage groups with 20large linkage groups, spanning 1,404 cM with amarker density of 3.1 cM per SNP marker. Thefunctional SNP assays were developed usingKBioscience KASPar™ genotyping chemistrydetected using a Fluidigm integrated fluidicchip (Fig. 7.2). The combination of the KASParchemistry with the nano-fluidic chip technology(9.7 nL reaction volume) not only significantlyreduces the marker data point genotyping costs(∼US$0.05) but also significantly increases thespeed of genotyping. Indeed, a single Fluidigm96.96 IFC is capable of producing 9216 PCRs ina single run (∼3 h) with little technical expertise.

Given the dramatic decrease in costs andrelative ease of genotyping, we anticipate thedevelopment of fully saturated genetic maps ofquinoa within 12–18 months. These maps shouldquickly open up the possibility to integratemarker-assisted selection protocols, specificallygenomic selection, into accelerated quinoa breed-ing programs. However, before genomic selectioncan be fully realized, quinoa breeders must iden-tify a “training population” of quinoa accessionsand develop rigorous phenotyping strategies.The training population will need to be bothfully genotyped and phenotyped to develop thestatistical models necessary to estimate breedingvalues of genomic regions (Jannink et al. 2010).


(a) (b)

Fig. 7.2 Example of SNP assays using the KASPar™ genotyping chemistry on the Fluidigm access array in the quinoa RILmapping population. (a) The genotyping across the 96.96 IFC chip (96 DNA samples on the vertical, 96 SNP assays on the hori-zontal). (b) Individual SNP loci in a Cartesian graph. A no template control (NTC) and a synthetic heterozygote are identified (Seecolor insert for representation of this figure.).

QUINOA DIVERSITY

The phenotypic and genetic diversity of quinoais borne out by its wide distribution in the Andes,covering Bolivia, Peru, Ecuador, Colombia,and the north of Argentina and Chile, attestingto its adaptation to a range of agroecologicalconditions. Quinoa can survive in adverse cli-matic and edaphic conditions and thrive inlocations where few crops can (Bonifacio 2003).Ecotypes of quinoa specifically adapted to majorecosystems have been identified: (i) Valley (fromthe inter-Andean valleys); (ii) Altiplano (fromthe highland plateau in Bolivia and Peru); (iii)Salares (from the salt flats of Southern Bolivia);(iv) Sea level (from Central Chile); and (v) Sub-tropical (from the Bolivian Yungas) (Tapia et al.1980). Each of these ecotypes is associated withsubcenters of diversity that originated aroundLake Titicaca (Fuentes et al. 2012). The pheno-typic and genetic diversity of quinoa is also shownin the variability in plant color, inflorescence type,growth habit, and chemical composition.

Over the past few years, scientists havecharacterized the genetic diversity of quinoa tounderstand its biological diversity as a function

of its eco-geographic distribution and to identifygenetically distinct groups (del Castillo et al.2007). This knowledge is a prerequisite in quinoaconservation strategies and effective germplasmmanagement and characterization (Roa 2004).The study of quinoa’s genetic diversity is alsoessential in plant breeding programs, especially inthe identification of diverse parental combinations(Fuentes and Bhargava 2011).

Phenotypic diversity

Initially, scientists have studied the geneticdiversity in quinoa using morphological markers.Wilson (1988a) combined morphological andisozyme data to elucidate the genetic relationshipsamong the quinoa ecotypes. He used the variationin electrophoretic patterns of 21 isozyme locitogether with the morphometric data to compare98 quinoa populations from South America. Hiswork showed two main groups: a Coastal typefrom south-central Chile and an Andean typedistributed at elevations above 1,800 m fromnorthwest Argentina to southern Colombia. Thislast group was also divided into northern andsouthern Andean quinoa. Wilson (1988b) also


constructed the first phylogenetic tree of theChenopodium species and his data supportedthe hypothesis that the Altiplano was the centerof origin and diversity of quinoa. A follow-upstudy, conducted using seed protein variationand morphological markers (Fairbanks et al.1990), confirmed Wilson’s initial conclusion(Jellen et al. 2011).

Ortiz et al. (1998) demonstrated that eightphenotypic descriptors can be used to derive acore collection of 103 accessions (10%) from apool of 1,029 accessions from the Peruvian quinoagermplasm bank at the Universidad National delAltiplano-Puno (UNAP). The core collectionrepresents most of the genetic diversity of thewhole collection, with a high correlation observedbetween quantitative trait variation and altitude.The authors recommend that a comprehensivequinoa core collection should also include acces-sions from Bolivian, Ecuador, and Chile, togetherwith cross-compatible, wild Chenopodium speciessympatric with cultivated quinoa.

Rojas et al. (2000) used morphological traitsand agronomic performance of 1,512 acces-sions of the Bolivian national quinoa collectionto analyze genetic diversity. Genotypes werecollected in Chile, Argentina, and Peru, aswell as native Bolivian materials. Using threemultivariate procedures, including principalcomponent, cluster, and discriminate functionanalyses, quinoa germplasm was classified intoseven distinct groups, including five within theAltiplano and two from lower altitude valleys ofthe eastern Andean mountain range. The traitsused in the study did not discriminate for theChilean lowland germplasm, which grouped withone of the Altiplano clusters.

More recently, Bhargava et al. (2007b) usedmorphological and quality traits to investi-gate genetic diversity in C. quinoa germplasm.Twenty-nine lines of C. quinoa and two lines of C.berlandieri subsp. nuttalliae were evaluated for 12morphological and 7 quality traits. Cluster anal-ysis and principal component analysis conductedfor the 19 traits revealed a high level of geneticvariability existing in the lines tested. Althoughcluster analysis grouped those lines with greatergenetic similarity, it did not group those lines

from the same origin, indicating heterogeneity oflines within a geographical region. The authorssuggested that heterogeneity, genetic architectureof population, history of selection, and/or devel-opmental traits could account for this populationdiversity within a geographical region. In anotherstudy, Bhargava et al. (2007c) used morphologicaland qualitative traits to analyze the degree of sim-ilarity/dissimilarity among 27 diverse germplasmlines of C. quinoa in the Indian subcontinent.These traits were discussed in relation to theirutility for plant breeding efforts.

Fuentes and Bhargava (2011) presented thefirst report on quinoa germplasm grown underlowland desert conditions. A total of 11 mor-phological descriptors were used on 28 quinoaaccessions collected from the northern highlandsof Chile, and cluster analysis classified the acces-sions into 6 discrete groups. Multivariate analysiselucidated the genetic relationships among theaccessions, with yield being the most importantdescriptor for discriminating the accessionsused. Significantly, Chilean quinoa under desertconditions did not show particularly extremevalues for any of the variables measured.

Curti et al. (2012) characterized 34 quinoapopulations from the northwest Argentina regionusing quantitative and qualitative phenotypictraits. Northwest Argentina represents the south-ern end of what is known as the C. quinoa Andeancomplex. Quinoa is considered marginal in termsof its cultivation in this region. Curti et al. (2012)analyzed the data using descriptive and multivari-ate techniques. On the basis of quantitative traits,both the principal component analysis and thecluster analysis differentiated between accessionsfrom the highlands, transition zone, centraldry valleys, and eastern valleys. On the otherhand, the principal coordinates analysis based onqualitative traits only discriminated accessionsfrom transition zone and eastern valleys. Theaccessions from the highlands and dry valleyspresented the more advanced domesticated traits,whereas accessions from transition zone andeastern valleys showed traits more similar towild-type-related Chenopods from the Andeanregion. This is the first phenotypic diversitystudy of accessions from Northwest Argentina.


Genetic diversity

With the development of molecular markers, thegenetic diversity of quinoa germplasm collectionshas been studied, as well as the genetic diversityof quinoa populations, for both cultivated andwild/weedy populations. Molecular markersprovide unique and effective tools for evaluatingand characterizing plant genetic diversity ina way that is unaffected by the environment(Gupta and Varshney 2000). Random amplifiedpolymorphic DNA (RAPD) markers were thefirst markers used to detect DNA polymorphismsamong different quinoa accessions (Fairbankset al. 1993). RAPDs have also been used toidentify true hybrids from intergeneric crosses(Bonifacio 1995). The genetic relationshipsamong 19 Chenopodium species were investigatedby Ruas et al. (1999) using RAPD markers. TheChenopodium species used in the study includedC. quinoa cultivars and weed species. Polymor-phisms were detected among these species butaccessions clustered according to their speciesclassifications. Wild and crop populations of C.quinoa shared a low level of molecular varia-tion, without differentiation between sympatricdomesticated and weedy populations, and lowlevels of intraspecific variation within accessions(Ruas et al. 1999).

In contrast to the study of Ruas et al. (1999)and del Castillo et al. (2007) studied the geneticdiversity and relationships among wild andcultivated populations of quinoa collected directlyfrom farmer’s fields. Ruas et al. (1999) comparedaccessions, whereas del Castillo et al. (2007)compared individuals of the cultivated and wildforms of quinoa, growing sympatrically withincultivated fields. del Castillo et al. (2007) sampledfrom three distinct regions of the altiplano andone inter-Andean valley in Bolivia. Using RAPDmarkers, the wild and cultivated populationsshow a significant but very low level of globaldifferentiation. However, there was a stronggenetic differentiation among the eight popula-tions in the study, with a strong correlation withthe regional ecogeography. The population struc-ture appears related to three major biogeographiczones: (i) the northern and central altiplano, (ii)

the interandean valley, and (iii) the southern Salar.A small proportion of the variation was explainedby geographical distance.

Aside from RAPD markers, AFLP markershave also been used to study genetic diversityin quinoa. Anabalón Rodríguez and ThometIsla (2009) used AFLP markers together with20 morphological descriptors to characterize14 accessions of quinoa located in the southof Chile, and also highland accessions. Theselocal, ancestral varieties are usually conservedand selected by Mapuche communities andother smallholder farmers, passed down throughthe generations. Also included in the study arethree varieties from the Tarapacá region and oneenrolled variety (Regalona-Baer), with C. albumand Chenopodium ambrosioides as the controls.The accessions clustered into two groups: (i)the coastal type, which included accessions fromthe north of Chile, and highland accessions, and(ii) the pre-cordillera accessions. The resultsare in accordance with previous morphologicaland isozyme studies, which separate quinoainto two types: a coastal type (Chile) and anAndean plateau type. This study indicates thatthe Chilean lowland germplasm could be moregenetically diverse than previously thought.The authors explained that this level of geneticdiversity could also be due to out-crossingwith the weedy populations of C. album andC. hircinum, coupled with the ancestral seedexchange system and selection due to edaphocli-matic and photoperiod factors. This work alsocomplements the work of Ruas (1999) in thatthe C. album and C. ambrosioides accessions werealso differentiated from the C. quinoa accessions.However, with the use of AFLP markers, one C.album accession was grouped together with oneC. ambrosioides accession (Anabalón Rodríguezand Thomet Isla 2009), whereas with the use ofRAPD markers, the C. album and the C. ambro-sioides accessions were placed in different groups(Ruas et al. 1999).

More recent studies have utilized microsatel-lites or SSR because these are frequentlycodominant, multi-allelic, highly reproducible,polymorphic, ubiquitous and widely distributedin the plant genome (Bhargava and Fuentes


2010). Christensen et al. (2007) used 35 ofthe first SSR markers developed to assess thelevel of genetic diversity in quinoa germplasmcollections. A total of 152 accessions from theUSDA and CIP-FAO collections were used in thestudy, including accessions from Peru, Bolivia,Ecuador, Argentina, and Chile. Results show thatthe accessions clustered into two main groups:one group included accessions from the lowlandsof Chile together with a set of USDA accessions,whereas the other group consisted of accessionsfrom the Andean highlands of Peru, Bolivia,Ecuador, Argentina, and extreme northeasternChile.

Using multiplex fluorescent SSR markers,Fuentes et al. (2009) studied the genetic diversitypatterns of 59 accessions from the northern andsouthern regions of Chile. These accessionswere classified as Altiplano (28) and coastal (31)ecotypes. Both cluster analysis (UPGMA) andprincipal component analysis separated the acces-sions into two discrete groups. The first groupcomprised quinoa accessions from the north(Andean highlands), whereas the second groupconsisted of accessions from the south (lowland orcoastal). Coastal quinoas showed more diversitythan Chilean highland quinoas using both clusterand principal component analysis. The coastalgroup showed continuous variation betweenextreme subgroups represented. Their resultsare in contrast with those of del Castillo et al.(2007), which showed that Chilean accessions,as representatives of coastal quinoas, were notgenetically diverse from the highland populationsof Peru and Bolivia.

Fuentes et al. (2012) examined the correlationof seed exchanges on the genetic diversity ofquinoa in Chile. In total, 34 quinoa accessionsrepresentative of Chile, 20 SSR markers, and 92field interviews were used in their study. Resultsshowed that a wide genetic diversity exists inquinoa grown along the main growing areas inChile. The accessions were classified into twomajor groups, and further subdivided into fivepopulations. Population I has nine accessionsrepresentative of the northern zone of Chile;Population II has seven accessions of the centralzone; Population III has nine accessions from

the southern zone and one from the centralzone; Population IV has six accessions from thehighlands of Peru, Bolivia, and Argentina; andPopulation V had two accessions, one each fromEcuador and Colombia. The genetic distancesamong populations were consistent with theirgeographic origin. Thus, quinoa populations withthe lowest genetic distances between them werePopulations I and IV (highlands) and II and III(lowlands). This grouping correlated well withthe geographic origins of the accessions, togetherwith edaphic and climatic conditions of theirorigin. This grouping also correlated with theexpansion of quinoa and is a genetic reflectionof the sociolinguistic context of ancient peopleinhabiting the Andes region.

Costa Tártara et al. (2012) studied the geneticstructure of cultivated quinoa in NorthwestArgentina, a region that has been underrepre-sented in germplasm collections and previousstudies. Aside from being underrepresented,Northwest Argentina is also the southernextreme of quinoa distribution within the CentralAndes. The authors used 22 SSR markers on35 accessions, which showed a high level ofgenetic diversity. Cluster analysis separatedthe populations into four distinct groups; thegroupings were consistent with the geographicorigin of the accessions. The first group consistedof 5 accessions from the Transition area thatis characterized by high altitudes, whereas thesecond group consisted of 12 accessions fromPuna, the highland Plateau. The third groupconsisted of 8 accessions from Eastern humidvalleys, and the fourth group consisted of 10accessions from the dry valleys. Even though theNorthwest Argentina is considered marginal interms of quinoa cultivation, high levels of geneticdiversity was still found in the accessions used.This genetic differentiation could be related toregional ecogeography and is also affected by theuse of landraces.

SUMMARY

A better understanding of quinoa genetic diversityhas been gleaned from all the studies discussed


earlier. First, the wide range of environments inwhich quinoa can grow has a direct influence onits genetic diversity. Over a long period of time,the adaptation of quinoa to extremely dissimilarclimatic conditions may have contributed to itswide genetic diversity (Costa Tártara et al. 2012).Phenotypic and genetic diversity studies haveshown that quinoa accessions are most oftenclustered according to their geographic origin,indicating that genetic variability has a spatialstructure and distribution (Risi and Galwey1989a, 1989b; Ortiz et al. 1998; Rojas 2003; delCastillo et al. 2007; Costa Tártara et al. 2012;Curti et al. 2012). The effect of populationisolation on genetic diversity was linked not onlyto geographical distance but also to climatic andorographic barriers (del Castillo et al. 2007).Furthermore, the congruence between geneticdifferentiation and ecogeography suggests thatquinoa all over the southern Andes may be under-going similar processes of genetic differentiationand that variation in quinoa ecotypes may beinfluenced significantly by gradients of frost andaridity (Curti et al. 2012).

The use of more informative molecular mark-ers has made it possible to elucidate the geneticdiversity of quinoa accessions. In their study,Christensen et al. (2007) suggested that theArgentinean accessions represent introductionsfrom both the southern Bolivian highlandsand the Chilean lowlands. A later study, usingmorphological data, also proposed that the mainintroductions of quinoa to Argentina came fromsouthern Bolivia (Curti et al. 2012). On the otherhand, instead of the Chilean lowlands, it is theChilean highlands that could be the alternativeroute for quinoa introduction to Argentina (Curtiet al. 2012). In Southern Chile, the high geneticdiversity of coastal/lowland ecotypes has beeninvestigated using dominant AFLP markers(Anabalón Rodríguez and Thomet Isla 2009)and codominant SSR markers (Fuentes et al.2009; Fuentes et al. 2012). These studies showedthat Chilean lowland germplasm is much moregenetically diverse than previously thought. Thishigh genetic diversity could be due to the contin-uous hybridization with relatives that coexist inthe field (Fuentes et al. 2009), active crop/weed

complexes having a monophyletic coevolvingbehavior (Rana et al. 2010). Christensen et al.(2007) also reported diversity data that were moreconsistent with an allogamous system rather thanan autogamous one.

Genetic events, such as genetic drift, geneticbottlenecks, and founder effects, have beenillustrated by genetic diversity studies in quinoa.Quinoa may have been domesticated twice – oncein the High Andes and a second time in theChilean lowlands (Christensen et al. 2007;Fuentes et al. 2009). This Chilean domesticationevent is a genetic bottleneck (Jellen et al. 2011).Fuentes et al. (2012) showed a fragmented patternof diversity between the central zone and thesouthern zone of Chile, corresponding with theisolation of quinoa farmers. The average het-erozygosity and proportion of polymorphic lociin the central zone of Chile were lower than thatfor the southern zone. This indicates a subpatternof geographic bottleneck within lowland/coastalquinoa. The reduction in genetic diversity levelsin the northern highland and coastal lowlandregions compared to the southern highlandregions near Lake Titicaca could be a result offounder effects associated with the dispersal ofthe crop from its center of origin; alternatively, itcould be a response to selective adaptation in themore uniform ecological regions of the northernhighlands and coastal lowlands (Christensen et al.2007). The diffusion of quinoa into NorthwestArgentina from the centers of origin and diversitycould also have been mediated by foundingevents associated with early dispersal fromthe central Andean region of Peru and Bolivia(Curti et al. 2012).

Human activities, specifically seed exchanges,have significantly affected the genetic diversity ofquinoa. The influence of ancient exchange routesaffecting germplasm distribution contributes tothe genetic structure of quinoa (Costa Tartara2012). As the earliest societies along the Andeanrange tested new soils and climates, the geneticdiversity of quinoa probably evolved throughcycles of seed exchange and the domesticationprocess (Fuentes et al. 2012). It has been shownthrough genetic data and farmer interviews thatgenetic population structure can be reinforced


by seed exchanges among farmers (del Castilloet al. 2007). Genetic relationships within quinoapopulations have revealed the influence of variousproduction systems on quinoa biodiversity. Thus,studies of genetic diversity in quinoa must belinked with sociological and agronomic studies(Fuentes et al. 2012).

The results of genetic diversity studies inquinoa has implications in our conservationefforts and, consequently, on our plant breedingprograms. Since the 1960s, ex situ germplasmbanks of quinoa have been established (Bonifacio2003). However, some ecological zones are stillinadequately represented in these gene banks,such as the northern Andes (especially Ecuadorand Colombia), the Yungas (eastern slopes ofthe Bolivian and Peruvian Andes) (Christensenet al. 2007), and Argentina (Mujica and Jacobsen2002). In areas such as Northwest Argentina,where it has been shown that phenotypic andgenetic diversity is structured according to thesite of origin (Curti et al. 2012; Costa Tártaraet al. 2012), conservation programs shouldcarefully consider the areas to be preserved. Also,some accessions in the USDA and the CIP-FAOcollections could be heterogeneous lines of mixedgenotypes as multiple alleles at marker loci havebeen detected. Accessions should be screened andpurified before use in plant breeding programs(Christensen et al. 2007). Germplasm collectionsshould also be replenished (Mujica and Jacobsen2002). Meanwhile, in situ germplasm banks arefound in specific ecological environments ofthe Andean region. The conservators of thesequinoa landraces are farmers of the indigenouspopulation (Bonifacio 2003). As the pattern ofgenetic diversity in ex situ collections does notnecessarily reflect the extant genetic structureof in situ landraces, caution must be taken whenextrapolating the results of studies using ex situaccessions to in situ collections (del Castillo et al.2007). Armed with the knowledge of quinoadiversity in a particular region, the challengethen for plant breeders is to preserve the geneticdiversity so that quinoa could still adapt tostressful environments, while achieving a level ofhomogeneity required for commercial production(Curti et al. 2012).

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Chapter 8

Ex Situ Conservation of Quinoa:The Bolivian Experience

Wilfredo Rojas and Milton PintoPROINPA Foundation, Av. Elias Meneces km 4, El Paso, Cochabamba, Bolivia

INTRODUCTION

During the past four decades, germplasm collec-tions maintained ex situ have grown in numberand size as a result of the intense worldwideefforts to conserve plant genetic resources forfood and agriculture (PGRFA). These collectionsare kept under very different conditions, depend-ing on policies at the national or internationallevel, the institutional environment, availableexpertise, facilities and budget, and the degree ofnational and international collaboration (Engelsand Visser 2003). According to the second reporton the state of the art of PGRFA (FAO 2010), thetotal number of samples stored ex situ worldwidehas increased by approximately 20% (1.4 million)since 1996, reaching a total of 7.4 million samples.This growth in quantity and diversity of samplesover a range of germplasm requires that collec-tions be managed with the highest standards ofconservation.

Genebanks are essential for the food securityand sovereignty of every nation. They are part ofa nation’s ancestral and cultural heritage, and assuch are a responsibility that should be assumedby society and the state. Toward this goal, conser-vation of genetic resources requires institutionalsupport, including sustained financing, trainedstaff with specialized expertise and essential


equipment needed to maintain germplasmcollections and conduct conservation activities.

However, the mere creation of a genebank doesnot guarantee the conservation of plant geneticresources of a country, as shown by the first andsecond reports on the state of the art of PGRFAin the world (FAO 1996, 2010). Increasingly,more attention is paid as to how and when toregenerate germplasm from a collection, becauseof the increasing costs of germplasm maintenanceand regeneration (Engels and Visser 2003). Thereis also the possibility that, in time, genetic erosionoccurs in a bank that is improperly managed.The economics of genebank management andoperation is implicit in all conservation efforts.It does not merely consist of assigning budgetsto specific operations of the bank, but is relatedto internal decision making on the expendituresof the institution. These are crucial decisions,constituting a more important issue, becausethose who initially support its implementationcontinuously demand improvements in theregistration of its operations.

In the absence of good planning, genebankmanagement can develop and evolve in manyways. In addition, local germplasm conditionsvary greatly, calling for several managementapproaches and producing a diversity of expe-riences. In developing countries, conservationissues and technological advancements are not

125


always a priority, and decisions regarding theseoften come from a political perspective. This hasbeen the case regarding the germplasm collectionof quinoa from Bolivia, where conditions havenot always been easy. The Bolivian collection hasthe greatest diversity in the world, particularlyin comparison to other countries in the Andeanregion. Quinoa is not merely an “Andean grain.”More than any crop in the region, quinoa encap-sulates the Bolivian culture. It is strongly rootedin our local customs, in indigenous consumptionand production. Not only does Bolivia have thegreatest genetic diversity of quinoa but it also hasthe highest acreage of quinoa grown in the world,making it the top exporter of quinoa. Theseaspects validate quinoa’s strategic importance forBolivia.

In this chapter, the center of origin and diver-sity of quinoa are discussed, together with thebeginnings of the Bolivian germplasm collection.The operations and the management process fol-lowed for more than 45 years since the first quinoaaccessions were collected, and critical timesthroughout the collection’s existence, are alsodiscussed. This chapter also provides a summaryof the work of the Promotion and Research onAndean Products (PROINPA) Foundation duringthe period when it was in charge of genebankmanagement and conservation by delegationof the Bolivian State, until the bank achievedrecognition at both national and internationallevels.

CENTERS OF ORIGIN AND DIVERSITYOF QUINOA

According to the Russian scientist Vavilov, thecenter of origin of a cultivated plant is the regionwith the greatest diversity of plant types, both cul-tivated and wild progenitors. The Andean regionis among the eight centers of origin of plantsgrown in the world (Vavilov 1951). It is also con-sidered as the center of one of the most importantAmerican civilizations (Gandarillas et al. 2001).By consensus, all scientists who have conductedmorphological, genetic, and systematic studiesconsider that quinoa originated in the Andes of

Peru and Bolivia (Gandarillas 1979). The Andeanregion has the highest genetic diversity of bothwild and cultivated quinoa occurring in naturalconditions and in cultivated fields. Consideringthe agroecological conditions under which thequinoa species develops, subcenters of diversityhave been identified. In these subcenters of diver-sity, quinoa ecotypes have developed and adapted,resulting in variability in botanical, agronomical,and species adaptation characteristics.

Five ecotypes of quinoa have been identifiedin the Andes region, based on genetic variability,adaptation, and several highly heritable mor-phological characteristics (Lescano 1989; Tapia1990). Four of the five major ecotypes or groupsof quinoa are found in Bolivia (inter-Andeanvalleys, highlands, salt flatlands, and Yungas).Only the sea level quinoas are not found in Boliviabut grow in Chile. The following are descriptionsof the ecotypes:

1. Quinoas of Inter-Andean Valleys have adapted togrow between 2500 and 3,500 meters above sealevel (masl) and grow up to 2.5 m or more inheight. They produce many branches with laxinflorescence and are usually resistant to downymildew (Peronospora farinosa). This group ofquinoas are typically grown intercropped withmaize in 5–6 transverse grooves, as edges ofother crops, or scattered in the same field.

2. Quinoas of the Highlands are able to growfrom 3,600 to 3,800 masl in the region of thePeruvian-Bolivian Altiplano, as pure or uniquecultures, and in larger areas. The plants growbetween 0.5 and 1.5 m, with the stem endingin a main panicle that is usually compact. Itis in this Altiplano region where the greatestvariability of the crop has been reported, andwhere grains with more specialized use areproduced. This group includes the largestnumber of improved varieties, and is suscep-tible to mildew when grown in areas of highhumidity.

3. Quinoas of the Salt Flatlands grow in the saltflat areas south of the Bolivian Altiplano.This is the driest area in the region, with200–300 mm of rainfall. In this region, it iscustomary to plant quinoa as a single crop

Ex Situ Conservation of Quinoa: The Bolivian Experience 127

at distances of 1 m× 1 m in holes to makebetter use of low humidity. These quinoas areknown as “Royal Quinoa,” with larger grainsize (>2.2 mm in diameter), characterized bya thick pericarp and high saponin content.

4. Quinoas of the Yungas or Edge of the Rainforestconsist of a small group of quinoas that haveadapted to the conditions of the Yungas or edgeof the Bolivian rainforest, mainly in the valleysof Cochabamba, at altitudes between 1,500 and2,200 m. They are characterized by somewhatbranched development, reaching heights of upto 2.20 m. The plants are green but the entireplant turns into a striking orange color when infull bloom.

5. Sea-level quinoas are found in the areas ofLinares and Concepción, Chile to 36∘ SouthLatitude. Plants of this type are more orless robust, 1.0–1.4 m tall, with branchedgrowth and cream-colored, transparent grains(Chullpi type). These quinoas share numer-ous similarities with Chenopodium nuttalliae(Huahzontle) grown in isolation in Mexico at20∘ North Latitude.

The quinoa genetic diversity conserved andavailable in the different countries from theAndean Region are classified in five majorgroups. Quinoa from Bolivia is distributed in theinter-Andean valleys, highlands, salt flatlands,and Yungas. Quinoa from Colombia and Ecuadoris distributed in the inter-Andean valleys, quinoafrom Peru is found in the inter-Andean val-leys and highlands, while quinoa from Chile isgrouped in the salt flatlands and sea-level quinoaecotypes (Fig. 8.1).

Rojas (2003) studied the genetic variabilityof the Bolivian germplasm collection and hasidentified seven subcenters of diversity in Bolivia:one subcenter in the salt flatlands of Potosi andOruro, two sub-centers in the northern Altiplanoin La Paz, one in the central Altiplano in La Pazand Oruro, one sub-center located geographicallyin the transition Salt Flatlands and Altiplano,and two subcenters in the Andean valleys ofCochabamba, Chuquisaca, and Potosi. Thesesubcenters comprise a wide genetic diversity ofthe crop, expressed in the variability of plant,

inflorescence, and seed color; variability of inflo-rescence types, culture cycle duration, nutritional(protein) and agroindustrial value; and variabilityin saponin and betacyanin content in leaves.This diversity of traits enables quinoa to adapt todifferent ecological and soil conditions such assalinity or acidity, rainfall, temperature, altitude,frost, and drought.

GEOGRAPHICAL DISTRIBUTIONOF QUINOA

Given the wide distribution of its center of origin,quinoa can be considered as an oligocentricspecies, with the Andean region as its center ofdiversity with multiple routes of diversification(Mujica 1992). Quinoa is grown throughout thevast Andean region that was once ruled by theIncas (Lescano 1994). It is found from Colombia(Pasto), to northern Argentina (Jujuy and Salta)and Chile (Antofagasta and Concepción). Itextends from 5∘ of North latitude in the southof Colombia, to 43∘ of South latitude in theTenth Region of Chile. It ranges from sea level inChile to 4,000 masl in the Peruvian and BolivianAltiplano. Thus, there are quinoas of the coast,valleys, inter-Andean valleys, salt flatlands, andAltiplano (Fig. 8.2). A considerable part of thegenetic variability of the species is associated withgeographical distribution (Rojas 2003).

Specifically, in Colombia, quinoa is grownin the Department of Nariño, in the towns ofIpiales Puesrés, Contadero, Cordova, San Juan,Mocondino, and Pasto. A department is a politicaldivision, each with a governor and an assembly.Colombia has 32 departments. In Ecuador, quinoais grown in the areas of Carchi, Imbabura, Pich-incha, Cotopaxi, Chimborazo, Loja, Latacunga,Ambato, and Cuenca. In Peru, quinoa is grownin the areas of Cajamarca, Callejon de Huayl-las, Mantaro Valley, Andahuayllas, Cusco, andPuno (Altiplano), which comprises 75% of thecultivated area. In Bolivia, quinoa is cultivatedin the Altiplano of La Paz, Oruro, and Potosiand in the inter-Andean valleys of Cochabamba,Chuquisaca, Potosi, and Tarija (Rojas et al. 2010b).In Chile, the quinoa-growing areas are the Chilean


4.000

3.500

3.000

2.500

2.000

1.500

0.000

Alti

tude

in m

asI

Sea level Yungas Inter-Andean Valleys Highlands Salt Flatlands

Major groups of quinoa diversity

Isolated plants

Intercropped with other crops

Isolated crops

Isolated and intensive cropsSpaced crops

Fig. 8.1 Profile distribution of the five major quinoa ecotypes in the Andean Region.

Altiplano (Isluga and Iquique) and Concepción.There are also reports of the Ninth and TenthRegions growing quinoa (Barriga et al. 1994).In Argentina, quinoa is produced in isolation inthe highlands of Jujuy and Salta. Cultivation alsoexpanded into Calchaquíes Valleys of Tucuman(Gallardo and Gonzalez 1992).

GENEBANKS OF THE ANDEAN REGION

To safeguard the phenotypic and genotypic vari-ability of quinoa in the Andean region, gene bankshave been established since the 1960s in severalcountries in the region. These genebanks are con-nected to the agricultural sector and universitiesof Argentina, Bolivia, Colombia, Chile, Ecuador,and Peru, and are responsible for their manage-ment and conservation.

According to Rojas et al. (2013), out ofthe 16,422 accessions conserved worldwide,14,502 are conserved in genebanks from theAndean region, with Bolivia and Peru managinggermplasm collections with the highest numberof accessions (Fig. 8.3). In Bolivia, there are

six genebanks which contains 6,721 accessionsof quinoa. These genebanks are located at theToralapa Center of the National Agriculturaland Forestry Research Institute (INIAF), at theUMSA Experimental Station in Choquenairaat the Centre for Research in Biotechnologyand Plant Genetic Resources of the UTO, atthe Tiahuanacu Academic Unit of UCB, at theKallutaca Experimental Center of UPEA, andat the Center for Community Research and Pro-motion. The genebank with the largest numberof accessions is the one managed by INIAF, with3,178 accessions, known in Bolivia as the nationalcollection of quinoa germplasm. Next in line arethe collections of UTO and UMSA with 1,780and 1,370 accessions respectively (Rojas et al.2010a, 2013).

In Peru, there are eight genebanks where6,302 accessions of quinoa are conserved. Thegenebanks are located in the experimental stationsof INIA in Illpa (Puno), Andenes (Cusco),Canaán (Ayacucho), Santa Ana (Huancayo),and Baños del Inca (Cajamarca). The followinguniversities also conserve quinoa germplasm:


Agroecological regions of quinoaproduction in South America

Sea Level Region

Inter-Andean Valleys Region

High Flatlands (Altiplano) Region

Salt Flatlands Region

W

N

E

S

Fig. 8.2 Geographic distribution of quinoa in the Andean Region. (See color insert for representation of this figure.)


0

7,000

6,000

5,000

4,000

3,000

2,000

1,000

Bolivia

Perú

Argen

tina

Ecuad

orChil

e

Colom

bia

N° Genebanks

N° Accesions

67216302

60 80 10 30 50 1028286492

673

Fig. 8.3 Number of accessions and genebanks conserving quinoa germplasm in the Andean countries.

Universidad Agraria La Molina in Lima, Univer-sidad Nacional de San Antonio Abad of Cusco,and the Universidad Nacional del Altiplanoin Puno (Mujica 1992; Bonifacio et al. 2004;Bravo and Catacora 2010; Gómez and Eguiluz2011). The most important collections of quinoagermplasm are those of Universidad NacionalAgraria La Molina, Universidad Nacional delAltiplano, and INIA Puno with 2,089, 1,910 and1,029 accessions.

In Argentina, the national network of seedgenebanks holds a total of 492 accessions ofquinoa conserved in the Base Genebank of theNational Institute of Agricultural Technology(INTA). These accessions are partially duplicatedin the Active Genebank of the ArgentinianNorthwest and at “La Consulta” Genebank.The collection of 492 accessions is a result ofthe joint efforts of the Faculty of Agriculture ofthe Universidad de Buenos Aires (UBA) and theINTA (Rojas et al. 2013).

In Chile, 286 accessions are conserved, out ofwhich 203 accessions are in the Base Genebank ofVicuña Experimental Center – from the NationalInstitute of Agricultural Research (INIA), and

the rest are in the genebank of the Facultyof Agrarian Sciences at UACH, in the ActiveGenebank of the Carillanca Regional ResearchCenter – INIA, in the Universidad Arturo Prat(UNAP) and in the Baer Seed Bank. In Ecuador,there are 673 accessions of quinoa conserved bythe National Department of Biotechnology andPhytogenetic Resources at the Santa CatarinaExperimental Station from the National Instituteof Agricultural and Livestock Research (INIAP).In Colombia, the genebank of the ColombianCorporation of Agricultural Research at Tibaitatáconserves 28 accessions (Rojas et al. 2013)

BOLIVIAN COLLECTION OF QUINOAGERMPLASM

History and management of the quinoagermplasm

According to Rojas et al (2010a), the first effortsto establish a germplasm collection of quinoaand other Andean crops date back to the early1960s, at the initiative of Humberto Gandarillaswho went on collection trips in the highlands,


salt flatlands, and inter-Andean valleys of Bolivia.With the material Gandarillas collected, thefirst quinoa genebank was established. Initially,the genebank was under the responsibility ofthe Patacamaya Experiment Station but waslater under the National Quinoa Program of theBolivian Institute of Agricultural Technology(IBTA) that operated in Bolivia until 1998.

After the closure of IBTA in the late 1990s,the Patacamaya Experimental Station becamedependent on the Prefecture of La Paz and thequinoa germplasm collection was in imminentdanger of being lost. The Prefecture of La Pazwas administered by the newly created Depart-mental Agricultural Services (SEDAG) – La Pazunit, and management of the quinoa germplasmcollection also became one of its responsibilities.Unfortunately, during this time, germplasm col-lection had no financial support. In the absenceof a clear policy regarding the collection, itsconservation and management was discontinued.

At the initiative of quinoa researchers and exec-utives of the Foundation for the PROINPA, everyeffort was made to maintain the plots of quinoagermplasm that had been sown in the northernAltiplano through the Durable Resistance Projectin the Andean Region (PREDUZA). During the1997–1998 crop year, the PREDUZA projectwas in full operation and managed by researchersfrom the former National Quinoa Program ofIBTA. The material was planted by the lakesideof Lake Titicaca mainly for accessibility and easein management. In addition, the environmen-tal conditions in the northern Altiplano wereconductive to assessment for mildew resistance.The germplasm had been divided into two lots,where 50% was assessed at the Belen ExperimentStation (Omasuyos province) while the other 50%at the Choquenaira Experimental Station (Ingaviprovince), to replicate the quinoa germplasmcollection at harvest. Both stations were managedby the Faculty of Agronomy, UMSA.

Under these circumstances, the authoritiesof the Ministry of Agriculture, Livestock andRural Development (MAGDER), later theMinistry of Rural Development, Agriculture andEnvironment (MDRAyMA) currently known asthe Ministry of Rural Development and Land

(MDRyT) through letter PDTA-2216-BO-CNo. 418/98, enabled the PROINPA Foundationto take over the conservation of the quinoagenebank. The PROINPA Foundation wasentrusted to administer, manage, and conservethe quinoa collection within the framework ofBolivia’s legislation. To fulfill its responsibilities,PROINPA on its own initiative raised fundsand received support from several agencies,including the Danish Cooperation for Develop-ment (DANIDA), International Plant GeneticResource Institute (IPGRI) currently knownas Bioversity International, Program of SmallDonations of the United Nations DevelopmentProgram (PPD/PNUD), International Fundfor Agricultural Development (FIDA), and theMcKnight Foundation. This marked a new begin-ning concerning the conservation of plant geneticresources of Bolivia. The PROINPA Foundationhas taken over the management and conservationof the quinoa genebank for more than 10 years.

Later, the quinoa genebank received finan-cial support from the national governmentin February 2001 through agreements signedbetween MAGDER, Agricultural ServicesProgram – Coordination Unit (UCPSA), andPROINPA. After the creation of the NationalSystem of Genetic Resources for Food andAgriculture (SINARGEAA) in 2003, six nationalgenebanks came into operation and MDRAyMAendorsed PROINPA as the entity in chargeof the National Genebank of Andean Grains,including the quinoa germplasm collection.During this period up to December 2008,PROINPA has managed and conserved thesegenetic resources under the SINARGEAAframework and with the support of projectsunder the Neglected and Underutilized Species(NUS) – IFAD and United Nations Environ-mental Program/Global Environmental Facility(UNEP/GEF) frameworks.

Subsequently, INIAF, an institution createdthrough a national decree in 2008 and desig-nated as the national competent authority inGenetic Resources, enabled funding for theSINARGEAA Transition Plan (2009–2010).Under this framework, INIAF and PROINPAsigned an interagency cooperation agreement,


through which the coordination and interactionmechanisms for the transfer of genetic materialand relevant equipment to the new competentauthority were established.

Current status of quinoa germplasm

In the crop year 2010, the quinoa germplasm col-lection and the Genebank of High Andean Grainswere transferred to INIAF. The transfer wascompleted on July 23, 2010 and was notarized,recording in detail the conservation status ofeach accession, along with related documentation(databases, publications, and other protocols),equipment and materials basis for conservation.The transfer also included a period of at least18 months of joint work between the two insti-tutions, including staff training and capacitybuilding to facilitate immediate management ofthe genebanks.

This moment closed a very important stage forPROINPA in the management of the NationalGenebank of Andean Grains, and, in particular,the administration of the Bolivian collection ofquinoa germplasm which lasted for 12 years. Itwas a labor of dedication to increase the number ofaccessions of the germplasm collection, improvethe quality of conservation, upgrade the collec-tion’s documentation, and generate a knowledgedatabase that can be used in different fields, fromgenetic improvement to agribusiness. All of thishas been made possible through complementaryprojects with which the genebank has beenarticulated with different users, from academic,scientific, and technical users to communitiesthat work with in situ conservation. This workand dedication has been recognized both nation-ally and internationally. Conservation farmers,government agencies, international cooperationagencies based in Bolivia, and entities outside thecountry, have lauded the genebank for its highconservation quality and possession of uniquematerials (Rojas et al. 2010a).

At present, the Bolivian quinoa germplasmcollection is part of the National Genebank ofAndean Grains, preserved in the INIAF ToralapaCenter. The collection has wide genetic vari-ability and conserves 3,178 cultivated and wild

accessions collected in highland communities,salt flatlands, inter-Andean valleys and alongthe edge of rainforests in the regions of La Paz,Oruro, Potosi, Cochabamba, Chuquisaca, andTarija. In addition, it includes germplasm fromPeru, Ecuador, Colombia, Argentina, Chile,Mexico, the United States, England, Holland,and Denmark.

STEPS FOR EX SITU MANAGEMENT ANDCONSERVATION OF QUINOA

Ex situ conservation is considered complementaryto in situ conservation as it is not possible toconserve all species ex situ or “off site.” It consistsof a set of activities towards the managementof plant genetic resources. It is carried out bycreating genebanks and germplasm collections,involving a series of steps and procedures thatrequire trained personnel.

Seed genebanks are viable options for ex situconservation of quinoa germplasm. Conditionsin these seed genebanks promote maximumstorage time with minimal physiological activityand negligible loss of viability and germination.Quinoa seeds have been classified as “orthodox”according to its behavior in storage (Ellis et al.1988). In “orthodox” seeds, one can managehumidity and temperature in order to keep seedsviable for longer periods of time, whereas in“recalcitrant” seeds this is not possible. Becausequinoa seeds are “orthodox,” their viability canbe maintained in a predictable manner withina range of environmental conditions throughtemperature and seed moisture reduction.

The “orthodox” behavior of quinoa seeds instorage makes it possible to devise a managementstrategy for the seed genebanks. The protocolsdeveloped and the results achieved with the Boli-vian quinoa seed germplasm collection, duringthe time that it was managed by PROINPA, arediscussed in this section. An effective protocolfor ex situ management has been developed byseveral specialists in Plant Genetic Resources inLatin America (Jaramillo and Baena 2000). Theprotocol has been adapted to quinoa germplasm,


including the collection, preliminary multipli-cation, storage, characterization, and evaluationof germplasm. It also includes the regenerationand multiplication of germplasm, plus theirdocumentation and utilization.

Collection of quinoa germplasm

“Collection of germplasm” is the process ofobtaining seed samples that represent wild plantpopulations or varieties of cultivated species.The collection of germplasm is performed forthe conservation of species diversity, to obtaingermplasm that can be used in breeding or tosearch for and find new populations not availablepreviously in the genebanks (Sevilla and Holle2004). Germplasm collections are necessary andfully justified in areas considered as centers oforigin and diversity because cultivated varietiesand wild relatives that coexist and evolve overtime can be found in such places. Germplasmcollection is the first stage or step that needs to becarried out in a management strategy for ex situconservation. Utmost caution and care shouldbe taken in technical and logistical planningand in job execution. For instance, seed samplescollected should be viable to ensure that thesewill germinate and develop into plants similarto the mother plants if grown in comparableenvironments.

Since 1964, when germplasm collections ofquinoa began in Bolivia, the Centralized Collectionmethod has been used. This method is based onthe work of a team of scientists and researcherswho visit various sites in the highlands, saltflatlands, inter-Andean valleys, and areas of cropdistribution in the country. The team collectsseeds to form the main quinoa germplasm collec-tion. Although the germplasm collection holdssignificant numbers of quinoa accessions, thevariability stored does not represent all the exist-ing diversity of quinoa in the country. For thisreason, quinoa germplasm was collected in areasthat had not been represented in the collection.

Since 2002, the Decentralized Collection me-thod for quinoa germplasm collection has beenimplemented in the country. This method entailscollaboration with local entities or groups such

as extension services, farmer organizations,NGOs and universities, among others. It isbased on itinerant collection of samples by ateam of scientists throughout different ecologicalregions. This collection method also involvesinteraction with local experts and constitutes apractical alternative to the Centralized CollectionMethod, because local experts have extensiveecogeographic and cultural knowledge of thearea. These local experts also know how to choosethe best collection time and can collect duringfruiting and later stages (Guarino et al. 1995).

Technical procedure for quinoagermplasm collection

For both the Centralized Collection and Decen-tralized Collection methods, it is critical thattechnical and logistical planning should be in syncto ensure the success of a quinoa germplasm col-lection trip. Technical planning involves definingwhat to collect and determining why, where, how,and when to collect. On the other hand, logisticalplanning means organizing the mission. Arrange-ments need to be made for the effective imple-mentation of the technical planning aspects, suchas forming the team or collection team, prepar-ing the itinerary, arranging the transportation,acquiring permits, and assembling the necessaryimplements for collection, such as instruments,equipment, and supplies (Guarino et al. 1995).

A protocol for quinoa germplasm collectionhas been adapted, and it can be applied to both thecentralized and decentralized collection methods.The protocol meets the minimum requirementsneeded for germplasm collection work. Someimportant points in the protocol are specified inthe following sub-sections.

Collection form

The collection form adapted for quinoa germ-plasm collection is shown in Annex 8.1; it is basedon the Germplasm Collection Form publishedby the International Plant Genetic ResourcesInstitute or IPGRI (Jaramillo and Baena 2000).The form has the minimum necessary informa-tion about the origin of the collected populations.


Unavoidable variables were included to recordmorphological and ethnobotanical information,used to compare qualitative characteristics at thetime of characterization and evaluation of quinoaaccessions (Rojas 2002b).

Sources of collection

Sources of collection are those sites where samplesof germplasm can be obtained. Farmers’ fieldsand storage facilities constitute the main sourcesfor quinoa collections because these providemore homogeneous seed samples. Moreover, theinformation needed on the collection form ismore reliable, often coming from the farmersthemselves. Nevertheless, rural fairs, markets, andother places of sale are also considered sourcesof collection, depending on available informationregarding the origin of the sample so it can berecorded in the collection form. Finally, wildlifehabitats are also considered sources of collectionfor the registration of wild populations, althoughwild populations of quinoa can also be found infarmers’ fields.

Sampling strategy

The objective of a collection trip is to gather agroup of accessions that would be a representativesample of the genetic diversity of a taxon. Thisrequires adequate knowledge of the area and ofthe target species. For this reason, informationon topography, geology, soil, climate, and vege-tation of the area must be collected. In addition,information on the distribution, phenology,reproductive biology, genetic diversity, storagebehavior, and ethnobotany of the species, that is,knowledge about their uses, must be gathered(Guarino et al. 1995).

The number of samples to be collected in ageographic area depends on the existing geneticvariability found in the area. The number ofsample plants to be taken per population woulddepend on the characteristics of the plot. Usually,a seed sample of 50 plants per population ofquinoa is recommended. The plants should berandomly selected (random sampling) in caseof homogeneous plots, and selected at small

intervals (stratified sampling) in case of variablesites (Genebank Standard 1994). In the case ofwild species, sampling should be done withoutcompromising the natural preservation of plantpopulations (Querol 1988).

From each plant, it is recommended thatthe glomeruli to the average height of the mainpanicle be cut on the glomerular basal axis with ascissor. A sufficient quantity of seed can be pro-duced with the material collected from at least 50plants, which may vary from 20 to 100 g of seed,depending on the plant structure. For quinoa, 3 gof seed on average equals approximately 1,000seeds. Therefore, the amount of seeds collectedwould exceed the recommended minimumamount of 1,500 to 2,000 seeds for autogamousand pollinated populations (Genebank Standard1994; Hawkes 1980). Consequently, the seedscollected from an accession could be consideredas representative samples.

Sample handling and documentation

Whenever possible, samples to be collectedshould be healthy, viable, and fresh. Plants shouldbe collected in the mature stage so it can toleratedesiccation without losing viability. The moisturecontent of the seed sample should be between10% and 12%. However, if the collection is doneimmediately after a rain, samples should be driedor exposed to the sun for the duration of theexpedition.

For each sample of quinoa germplasm, thecollection form described in Annex 8.1 mustbe completed. Information on origin, agromor-phological characteristics, and uses is generallyprovided by farmers through informal interviews.Both the collected seed and collection formshould be placed in paper envelopes identifyingclearly the expedition name and the samplenumber.

History and evolution of quinoagermplasm collections

Rojas et al. (2001) published a catalog on theBolivian quinoa germplasm collection andsummarized the history and progress of quinoa


collections. The first germplasm collection ofquinoa and Andean crops organized in theAndean region was in the Patacamaya Station in1966, at the initiative of Humberto Gandarillas.He went on collection trips throughout thehighlands and inter-Andean valleys of Bolivia,with financial support from the Project BoliviaII Oxfam-FAO and later from the Institute ofAndean Crops, Ministry of Agriculture of Bolivia(Tapia 1977).

Later, the germplasm collection was aug-mented with valuable donations received fromthe Technical University of Oruro (56 accessions)and IICA (239 accessions from Peru), expandingthe collection to 1,375 accessions. The geneticmaterial from the collection was evaluated atthe Patacamaya Station, and as a result, 17landraces of quinoa were developed and described(Gandarillas 1968). In the late 1960s and early1970s, 446 accessions were received from Peru asdonation and exchange, including 131 accessionsensuing from mass selections from the NationalUniversity of the Altiplano in Puno. In thesame period, a collection of 159 cultivated andwild accessions were received from the centralAltiplano of Bolivia (La Paz and Oruro) and65 accessions collected by the OAS, withoutregistration data and collection date.

By the mid-1970s, the accessions of quinoaand Andean crops numbered to 2,045. However,loss of genetic material and separation of thequinoa collection from the potato, oca, andullucus collections reduced the number to 1,458.Subsequently, Waldo Tellería made a collectionin the Department of Oruro and increased thegermplasm collection to 1,472. In 1978, the col-lection was expanded to 1,487 accessions througha donation of accessions from northern Argentina.In the same year, Humberto Gandarillas madecollections in the Altiplano and inter-Andeanvalleys of the country and the inclusion of threeaccessions from Mexico increased the collectionto 1,516 accessions. Later, in 1981, HumbertoGandarillas, Gualberto Espindola, and FlorencioZambrana undertook different collection tripsin the country, increasing the collection to 1,752accessions. In 1982, the entry of eight accessionsfrom Ecuador (INIAP) and northern Chile were

registered, increasing the collection to 1,761accessions.

Between 1983 and 1985, Humberto Gandaril-las, Gualberto Espindola, Raúl Saravia, AlejandroBonifacio, Emigdio Ballon, German Nina, andEstanislao Quispe embarked on several collectiontrips in the country and enlarged the collectionto 1,985 accessions. In the same period, quinoavarieties from Peru, Ecuador, Chile, and Mexicowere incorporated in the collection. A singleaccession from northern Argentina was receivedin 1987. In 1989, 15 accessions were collected byGuillermo Prieto, Raúl Saravia and AlejandroBonifacio in the central Altiplano, making thetotal number of accessions 2,001.

In 1992, the genebank recorded 2,012 germ-plasm accessions. In the same year, 20 acces-sions were incorporated from the southern andcentral Altiplano, through collections made byGualberto Espindola, Genaro Aroni, and JuanTupa. In 1993, 54 accessions were received fromCochabamba as a donation from the NGO WiñaySiway, Comprehensive Services CooperativePunata, Radio Esperanza, and Second Alandia.In addition, four accessions were received fromINIAP Ecuador, for a total of 2,090 accessions.In the same year, the Mañica Substation of IBTA(Potosí), through Severino Bartolome, collected147 cultivated and wild accessions. Furthermore,182 accessions (wild material and advanced linesclassified as bitter and sweet) from the breedingarea of the Quinoa National Program wereincorporated, increasing the collection to 2,419accessions.

In 1994, Wilfredo Rojas, Nicholas Monas-teries, and Gualberto Espindola collected nineaccessions from the South Altiplano and nineaccessions from the Pacajes province in La Paz.An exchange with the Caquiaviri TechnicalCollege resulted to 65 accessions incorporatedin the collection. INIA Peru donated nine acces-sions, bringing the collection to a total of 2,511accessions. In 1995, 24 accessions were added tothe collection, mainly varieties and breeding lines.By the time of the closure of IBTA, the number ofgermplasm accessions managed at the PatacamayaExperiment Station numbered at 2,535.


Through the work executed by the PROINPAFoundation, complementary and planned collec-tions were carried out. In 1998, 12 advanced linesfrom the breeding component were incorporatedin the collection, and 56 accessions collected in theSouth Altiplano by Alejandro Bonifacio were reg-istered and likewise included. In 1999, 13 acces-sions from the global quinoa test originating fromPeru, Ecuador, England, Holland, and Denmarkwere included, along with 85 accessions collectedin the northern, central, and southern Altiplano.By this time, the collection numbered a total of2,701 accessions (Rojas et al. 1999).

Between 2000 and 2002, through decentralizedcollections, 135 accessions were incorporated, fora total of 2,836 accessions in the collection (Rojas2002b). In the years 2002–2003, 113 accessionswere collected and the quinoa collection num-bered 2,949 accessions (Rojas et al. 2003a). In2003–2004, 172 accessions were collected for atotal of 3,121 accessions (Rojas and Pinto 2004).Finally, through complementary collection, 57accessions were collected, bringing the total countto 3,178 accessions. Table 8.1 shows the origin andnumber of accessions in the quinoa germplasmcollection in Bolivia.

Distribution of quinoa germplasmcollection

According to the distribution studies conductedwith the Bolivian collection of quinoa germplasm(Rojas 2002a; Rojas et al. 2009), the variabilityof quinoa is distributed from 15∘ 42′ of SouthLatitude in the Omasuyo province of the Depart-ment of La Paz, to 21∘ 57′ of South Latitude inthe M. Omiste province of the Department ofPotosi. Additionally, it extends from 64∘ 19′ ofWestern Latitude in the province Tomina of thedepartment of Chuquisaca, to 69∘ 09′ of WesternLongitude in the province Manco Kapac of theDepartment of La Paz. Its altitudinal distributionvaries from 2,400 to 4,200 masl (Fig. 8.4).

Fig. 8.4 shows a greater variability of quinoaalong the highlands (Altiplano), mainly in areasadjacent to the road that stretches from LakeTiticaca through La Paz, Oruro, Challapata,Sevaruyo and Uyuni, Salinas de Garci Mendoza,

Table 8.1 Origin and Number of Accessions in the QuinoaGermplasm Collection Preserved in the INIAF Genebank,Bolivia.

Department/ Number ofCountry Region Accessions Subtotal

Bolivia La Paz 1006 2,357Oruro 630Potosi 470Cochabamba 124Chuquisaca 108Tarija 19

Peru Ancash 5 675Junín 18Ayacucho 40Cusco 36Puno 567Ica 9

Ecuador Norte 11 28Centro 17

Chile Norte 1 18Sur 17

Argentina Jujuy 16 16Mexico Norte 3 6

Centro 3USA New Mexico 1 1Denmark 2 2Netherlands 2 2England 2 2OAS 60 60NIa 11 11Total 3,178

Source: Rojas et al. 2010a, 2013.aNI, Non-identified.

Daniel Campos, and Lipez. Equally importantis the geographical distribution of the accessionsthrough the Andean valleys of Cochabamba,Chuquisaca Potosí, and Tarija.

Preliminary multiplication of quinoagermplasm

During the initial stage of quinoa germplasmmanagement, there is a need to verify compli-ance with minimum conditions to ensure thatthe seed samples meet optimal quantity andquality standards for storage and conservation.Preliminary multiplication of germplasm must becarried out when the sample does not meet theseconditions. Preliminary multiplication consists of


N

Collection sites

Lakes and salt flatlandss

0 400

Kilometers

Fig. 8.4 Geographical distribution of the Bolivian quinoa germplasm collection.

increasing the sample size of germplasm underoptimal culture conditions to ensure sufficientand viable samples that have maintained theiroriginal genetic identity (Jaramillo and Baena2000).

There are two parameters that need to be takeninto consideration for the preliminary multiplica-tion of quinoa germplasm samples:

1. Number of Seeds Per Sample. According to theStandard for Genebanks (1994), the minimumamount required is from 1,500 to 2,000 seeds,which weigh an average of 4.5–6 g. However,at least 60 g of quinoa seed should be retainedunder short-term storage in order to havethe minimum required amount while at thesame time having enough seed needed for field


research tests or a plot of 70 m2 (Rojas andBonifacio 2001).

2. Germination of the Initial Sample. Quinoasamples should meet the germination levelsrequired by the Standard for Genebanks(1994), which are at least 85% for cultivatedsamples and 65% for wild samples. The higherthe germination percentage at storage, thebetter it would be for long term storage, asgermination potential decreases over time.

If the quinoa germplasm samples do notmeet one or both of these parameters, thesemust go through preliminary multiplication,which consists of meeting the target parameterunder optimum growing conditions (this willbe explained in detail in the “regeneration andmultiplication” stage). On the other hand, ifthe samples have optimal quantities of seedand germination rate, they are placed undershort-term storage. During this process, anaccession number is permanently assigned to thesample, and the passport information obtainedduring the collection of the quinoa germplasmsample is registered.

Storage and conservation of quinoagermplasm

The purpose of this stage of management is tokeep quinoa seeds viable and with the geneticidentity that represents the population. Thisrequires that storage be carried out under appro-priate conditions. According to Jaramillo andBaena (2000), the recommended procedure con-sists of three steps: preparation or conditioningof samples, packing of samples, and storage ofsamples.

1. Conditioning of the Sample. This procedureis performed to obtain a clean sample ofquinoa seeds, free of physical impuritiessuch as perigone residues, seed stalks of thepanicle, broken, infected, or foreign seeds.The conditioning process also includes theinitial measurement of moisture content of thesample to ensure longevity in storage. Thismeasurement can be determined by direct orindirect quantification of moisture content.

2. Packing of the Sample. After the conditioningprocess, the sample of quinoa seeds are packedand stored. A wide assortment of containers,of various shapes and materials, can be usedfor seed packing as long as the containers areairtight to isolate the germplasm and preventmoisture absorption and/or contamination.

3. Storage of the Sample. Storage conditionsmust be such that quinoa seed samples arekept viable. The packaging used and thesite of storage depend on the objective ofconservation and the projected duration ofstorage.

Short- and medium-term storage(1 to 20 years)

Short- and medium-term storage can last from1 to 20 years, and is used for quinoa germplasmthat will be used immediately or in the follow-ing years after collection. Weather conditionsin the highlands of Bolivia favor this kind ofstorage, with an average temperature of 10∘C,an average relative humidity of 45% and analtitude ranging between 3,700 and 3,900 masl.Since the establishment of the Bolivian quinoagermplasm collection, most samples have beenkept in short- and medium-term storage. For thiskind of storage, it is important to keep samplesin a dark environment with a simple ventilationsystem. The storage containers used for theBolivian germplasm collection are plastic bottles0.4 to 2 mm thick, with a double lid and a capacityof 1,000 g. These containers are well suited forshort- and medium-term storage at temperaturesranging from 8 to 20∘C and a relative humidityof 15% to 60% (IPGRI 1996). Under theseconditions, samples can be stored and maintainedfrom 1 to 20 years, depending on the geneticmaterial.

Long-term storage (80 to 100 years)

Seeds conserved under these conditions aremaintained for approximately 80–100 years.According to the Standard for Genebanks (1994),most orthodox seed species can be kept indefi-nitely at temperatures between −10 and −20∘C,


with a seed moisture content of 3–7% and aviability not lower than 85%. In order to imple-ment long-term storage of the quinoa collection,research on the use of silica gel and borax as seeddrying agents was conducted. However, thesedrying agents were ineffective, and moisturelevels failed to meet the requirements of theStandard for Genebanks (Rojas and Camargo2002). In the subsequent year, a protocol for theimplementation of long-term storage of quinoagermplasm was established (Rojas and Camargo2003) and described as follows.

Protocol for the implementation of long-termstorage

a. Analysis of Germination. The methodologyestablished by the ISTA (1993) is especiallyapplicable for the analysis of quinoa seedgermination, meeting the standards in termsof duration, number of seeds, drying levels,and incubation temperature. The formula forcalculating the germination percentage is

G% = No. germinated seeds ∕ No. total seeds

× 100

b. Initial Seed Moisture. Initial seed moisture canbe quantified directly or indirectly. Electronic

analyzers (moisture meters) can be used fordirect quantification of seed moisture, whilemethods described in the manual on seedtechnology for genebanks (Ellis et al. 1988) canbe used for indirect quantification. Using thedifferences in initial seed weight (wet weight)and final seed weight (dry weight), the initialhumidity of the seeds can be calculated usingthe following formula:

H % = Wet weight − Dry weight ∕ Wet weight

× 100

c. Reduction of the Moisture Content of Seeds.To reduce the initial moisture content ofseeds, a procedure using a dehumidifier hasbeen standardized. The dehumidifier is pro-grammed to 20∘C and seed moisture reachesa range of 3–7% after exposure for 24.5 h(Leon et al. 2007), thus meeting the humiditylevels required by the Genebank ManagementStandard (Table 8.2).

d. Seed Packing. Once moisture levels reach therequired levels (Genebank Management Stan-dard 1994), the quinoa seed must be packedimmediately and vacuum sealed in trilaminatedaluminum packs, which come in different sizes.These envelopes are airtight and well suited forlong-term storage, where temperatures range

Table 8.2 Initial Seed Moisture Content and Final Moisture Content in14 Accessions of Quinoa Exposed to 20∘C for a Period of 24.5 h.

Quinoa Initial Moisture, Achieved Moisture,Number Accessions % %

1 2350 12.40 4.902 2511 11.05 4.903 2857 11.10 3.654 2417 10.90 3.555 2401 12.00 4.306 1608 12.55 5.307 2840 12.40 5.108 1600 11.80 3.709 1462 10.90 4.6510 1289 11.00 4.2011 0550 10.40 4.5512 0577 11.20 4.2013 2237 9.70 4.7514 2374 10.05 4.85


from 8 to −20∘C and the relative humidity isfrom 10% to 20% (IPGRI 1996).

e. Storage. The aluminum packages should bestored in freezers at −20∘C, as indicated in theStandard for Genebanks (FAO/IPGRI 1994).

f. Germination Monitoring of Stored Samples. Tomonitor the germination rate of stored samples,the following steps are recommended: (i) openthe envelopes to remove seeds, and immediatelyvacuum seal the package to preserve the remain-ing seeds; (ii) rehydrate seed in a boiling waterbath for 50–60 min (Rojas and Camargo 2003);and (iii) perform a germination test followingthe procedure established by ISTA (1993).

Following this procedure, 247 germplasmaccessions of quinoa that belong to the “corecollection” were conserved for long term stor-age in 2003. This is the first experience withlong-term conservation of the Bolivian quinoagermplasm. After 5 years in storage, the firstmonitoring activity was performed in 2008 on the247 accessions that had been put on long-termstorage. Results were encouraging because thegermination percentage remained stable between90% and 98% when compared to the initialgermination percentage.

Characterization and evaluationof the quinoa germplasm

Characterization and evaluation of accessionsin a germplasm collection are complementaryactivities that involve describing the qualitativeand quantitative attributes of the accessions.These activities are undertaken to differentiateaccessions, determine their usefulness, structure,genetic variability, and relatedness, and findgenes of value in the production or breeding ofquinoa (Jaramillo and Baena 2000). Germplasmconservation goes hand in hand with its use,as experienced with the Bolivian collection ofquinoa. This is only possible if the characteristics,attributes, and potential uses of the accessionsare known. Information on the germplasm andits usefulness come from taking and analyzing aset of data on the germplasm sample in various

stages of its management, but mainly during thecharacterization and evaluation stage.

Theoretically, the quantity of data that can betaken during characterization and evaluation isinfinite. However, a good and useful descriptionof plants is not determined by the number of vari-ables used, but by its practical utility and accuracy(Querol 1988). Therefore, before describing anaccession, the data to be registered must be welldefined, although it also depends on the purposeand/or stage that is being followed in the process.

Stages of germplasm characterizationand evaluation

It is important to differentiate the stages involvedin characterization and evaluation of germplasmin order to carry out the work. These stages arecomplementary, based on data registration, andcan be performed simultaneously. The stages are(a) correct identification; (b) characterization; (c)preliminary assessment; and (d) evaluation.

(a) Correct Identification. Before describing agermplasm accession, the sample must haveaccurate botanical identification becausework is done through differentiations at theintraspecific level using the taxonomic clas-sification system. Furthermore, compliancewith passport data must be verified, a usefulprocedure for identifying duplicates amongaccessions that are often reintroduced to thegenebank (Valls 1992).

(b) Characterization. In a strict sense, this stageinvolves the systematic description of acces-sions using a set of highly heritable and per-sistent qualitative characters. Characters suchas growth habit, branching, plant color, mor-phology, etc., in addition to aiding the descrip-tion, help differentiate the accessions.

(c) Preliminary Assessment. This stage involves thedescription of agronomic traits of accessionsin a particular environment (space or time).The descriptors used are usually quantitativecharacters affected by the environment, suchas yield and resistance to biotic and abioticfactors, among others. It is recommendedthat a preliminary assessment be conducted


when evaluating the entire collection ofgermplasm accessions or significant amountsof the collection.

(d) Evaluation – Further evaluation of germplasmconsists of the description of agronomic orother traits of interest in the maximumnumber of possible environments (space ortime). These traits are usually quantitativeand affected by the environment, such asyield and resistance to biotic and abioticfactors, among others. The evaluation stage iscarried out after the preliminary assessmentand with those accessions that require furtherevaluation to assess their use. Unlike the pre-liminary assessment stage, the evaluation stageis similar to research trials and is establishedusing statistical experimental designs.

The characterization and preliminary eval-uation of quinoa germplasm can be performedsimultaneously. A representative sample of theaccessions is used, together with a list of cropdescriptors and the necessary tools to registerthe information. The genetic material mustbe established in properly identified plots, andwhenever possible, under uniform managementconditions. Depending on the number of acces-sions, it will require between 3 and 5 days of workper week from planting to physiological maturity.The data should be recorded systematically andconsistently to facilitate subsequent statisticalanalysis.

The procedure that must be followed to regis-ter each one of the target variables is in the list of“crop descriptors.” However, when conductingpreliminary characterization and evaluation ofquinoa germplasm, there are important things toconsider. First, sites with ecologies similar to theplaces of origin of the quinoa accessions must bechosen. Planting dates must match the naturalperiods of quinoa crop sowing, taking into accountthe area or place of origin of the accession. Toachieve a representative population, plots shouldhave four or six rows per quinoa accession andinformation should be gathered from the centralrows (registration of information). Recordingof qualitative variables and phenological phasesshould be performed according to the total

number of plants established from the accession.For the recording or registration of quantitativevariables, 10 plants randomly selected fromthe central rows during the “tipping panicle”stage are used. Moreover, it is recommendedthat information throughout the crop cycle berecorded.

In the over 40 years of its existence, the Boli-vian quinoa germplasm has been characterizedand evaluated with a focus on agromorphologicalinformation. The first catalog of the Boliviancollection of quinoa germplasm was published in2001 (Rojas et al. 2001). The catalog describesthe genetic variability of 2,701 quinoa accessionsusing 59 qualitative and quantitative variables.Although the information recorded was basedon the “Quinoa Descriptor” (IBPGR 1981),the catalog includes more variables identifiedin the various characterization and evaluationprocesses carried out since the 1980s. Later, a newversion of “Descriptor for Quinoa” was preparedand subsequently validated by researchers fromEcuador, Peru, and Bolivia (Rojas et al. 2003b).This document was the basis for the publicationof the new list of “Descriptors for Quinoa and itsWild Relatives” edition spearheaded by Biover-sity International and PROINPA (BioversityInternational et al. 2013).

Assessment of nutritional value of the quinoaaccessions began in 2001 and assessment ofagroindustrial variables began in 2006. Informa-tion on 555 accessions of quinoa was recorded toguide the use of germplasm in the developmentof products from processed quinoa. In addi-tion, most quinoa germplasm accessions werecharacterized at the molecular level.

Agromorphological variables

Starting in the 1980s, several characterizationand evaluation tasks were performed on thequinoa germplasm from Bolivia. As a result, thegenetic, morphological, and agronomic variabilityobserved during the crop cycle of the quinoagermplasm was studied. Although this informa-tion is published in the germplasm catalogs, theparameters of some variables of interest weresubsequently presented (Rojas et al. 2001, 2009;


Rojas 2003; Aroni et al. 2003; Rojas and Pinto2013):

1. Growth Habit. Although branching and growthhabit are influenced by planting density, fourdifferent clearly defined growth habits wereidentified in the quinoa germplasm collection(Fig. 8.5).

2. Plant Color. Between the stages of “tippingpanicle” and “first flower,” four colors typicalof the quinoa crop are expressed – green,purple, red, and a mixture of colors. However,as plants form grain and reach physiologicalmaturity, quinoa plants turn into differentcolors and combinations of colors includingwhite, cream, yellow, orange, pink, red, purple,brown, gray, black, wild green, and mixtures.

3. Shape and Density of the Panicle. In terms ofshape, there are three forms of panicles. The“amaranth-form” panicles are those with theglomeruli embedded directly in the secondaryaxis and have an elongated shape. “Glomeru-lated” panicles are those with the glomeruliinserted into the glomerulated axes and havea globular shape. “Intermediate” paniclesexpress the features of the “amaranth-form”and “glomerulated” (Fig. 8.6). Likewise, thereare two types of quinoa panicle in terms ofdensity – lax (loose) or compact. The panicledensity is determined by the length of thesecondary axes and pedicels, being compactwhen both are short.

4. Grain Color and Shape. When quinoa grainsreach physiological maturity they expressa wide diversity of colors, including white,cream, yellow, orange, pink, red, purple, light

(a) (b) (c) (d)

Fig. 8.5 Quinoa Growth habit: (a) simple; (b) branched to thelower third; (c) branched to the second third; and (d) branchedwith undifferentiated main panicle.

(a) (b) (c)

Fig. 8.6 Panicle shape: (a) glomerulated; (b) intermediate;and (c) amaranth-form.

(b) (c) (d)(a)

Fig. 8.7 Quinoa grain shapes: (a) lenticular; (b) cylindrical;(c) ellipsoidal; and (d) conical.

brown, dark brown, greenish brown, and black.In the quinoa germplasm, 66 grain colors hadbeen characterized (Cayoja 1996). Four grainshapes also exist in the germplasm (Fig. 8.7).

5. Grain Diameter. Grain diameter varies from1.36 to 2.66 mm. The famous “Royal Quinoa”falls within this range of variation. Its largegrains (2.20–2.66 mm) make it highly appreci-ated in the international market. On the otherhand, the weight of 100 grains ranges from0.12 to 0.60 g, and this variable is associatedwith grain size.

6. Vegetative Cycle. It is possible to find in thegermplasm collection accessions that reachphysiological maturity in 110 days and otheraccessions that reach maturity in 220 days.This feature is strongly dependent on thegenotype. Quinoas from the inter-Andean


valleys mature later than those from theAltiplano. This wide range of variation of thevegetative cycle is promising as adaptationto climate variability and climate change andcan be exploited further in quinoa breedingprograms.

7. Grain Yield Per Plant. Yields per plant wererecorded from 48 to 250 g. Yield is stronglydependent on both genotype and on yieldcomponent variables such as stem diameter,plant height, length and diameter panicle,grain diameter, etc.

Agro-food and nutritional value variables

A summary of the estimated statistical parameters(expressed on a dry basis) for each nutritionaland agro-food value feature of quinoa germplasmis presented in Table 8.3 (Rojas and Pinto 2006,2008; Rojas et al. 2007). The 555 accessionsevaluated show wide variability for most of thetraits studied, and is another indication of thegenetic potential of quinoa germplasm.

As seen in Table 8.3, the amount of proteinranged from 10.21% to 18.39%. These valuesare broader than the range of 11.6–14.96%reported by βo (1991) and Moron (1999) citedby Jacobsen and Sherwood (2002). While theamount of protein is a basic aspect of nutritionalvalue, its quality is also important and depends onthe content of essential amino acids. The proteinquality of quinoa is higher than that of cerealprotein. Fig. 8.8 shows the variation and proteincontent distribution among the 555 accessions

studied. It can be seen that majority of the acces-sions have a protein content ranging from 12% to16.9%, while 42 accessions had a higher range ofprotein content, 17% to 18.9%. The latter groupof accessions constitutes an important source ofgenes to drive the development of products withhigh protein content.

The fat content ranged from 2.05% to 10.88%with an average of 6.39% (Table 8.3). The upperrange of these results is greater than the rangeof 1.8–9.3% reported by βo in 1991 and Morónin 1999 (Jacobsen and Sherwood 2002). Quinoagrain has high fat content owing to its highpercentage of unsaturated fatty acids (Jacobsenand Sherwood 2002). The fat content of quinoacan be utilized to produce fine vegetable oils forcosmetic and culinary use.

The size of starch granule ranged from 1 to28 μ (Table 8.3). It is very important that thestarch granule is small to facilitate the processof texturing and insufflation because the spacesbetween granules allow more air to enter for theexchange and formation of air bubbles (Rojaset al. 2007). The size of starch granules is animportant variable in establishing the functionalcharacter of quinoa, as a component of differentmixtures with cereals and legumes.

The content of inverted sugars ranged from10% to 35%. This variable indicates the quantityof sugar that starts fermentation by splitting orinversion, which is the parameter for determiningthe quality of carbohydrates. In addition, it is alsoan important parameter through which quinoacan be classified as food suitable for diabetics.

Table 8.3 Nutritional and Agro-Food Characteristics and Statistical Parametersfor 555 Germplasm Accessions of Quinoa from Bolivia.

Component Minimum Maximum Mean SD

Protein, % 10.21 18.39 14.33 1.69Fat, % 2.05 10.88 6.46 1.05Fiber, % 3.46 9.68 7.01 1.19Ash, % 2.12 5.21 3.63 0.50Carbohydrates, % 52.31 72.98 58.96 3.40Energy, Kcal/100 g 312.92 401.27 353.36 13.11Starch granule, μ 1.00 28.00 4.47 3.25Inverted sugars, % 10.00 35.00 16.89 3.69Water filling, % 16.00 66.00 28.92 7.34

SD, standard deviation. Analyzed by LAYSAA, Cochabamba, Bolivia.


72

115126

89

67

33

9No.

acc

esio

ns

150

130

110

90

70

50

30

10

–10

Protein(%)

12

32

(10 – 10.9)

(11 – 11.9)

(12 – 12.9)

(13 – 13.9)

(14 – 14.9)

(15 – 15.9)

(16 – 16.9)

(17 – 17.9)

(18 – 18.9)

Fig. 8.8 Variation in protein content of 555 quinoa germplasm accessions.

The optimum percentage of “inverted sugar”content is ≥25%, and quinoa accessions havingthis optimum percentage can be used in flourblends to be used for breads, cereals, and otherflour-based products. As long as the saponinis removed from the outside of the grain, flourblends with quinoa have a pleasant mouthfeel.

The percentage of “water filling” shows a vari-ation range of 16–66%. This variable measuresthe water absorption capacity of starch for pastaelaboration and making of bread and pastries. Theideal value of this parameter for industrial appli-cation is ≥50%. There are quinoa germplasm inthe collection which meet this parameter and canbe an important source of genes to develop theseproducts.

The quinoa in the Bolivian germplasm collec-tion has a wide range of diversity as measured byagro-food and nutritive variables. This diversity isvaluable when incorporating quinoa in processedproducts to make appropriate use of the geneticpotential of quinoa. It is possible to select varietieswith higher protein percentages (≥18%) andobtain more attractive products. Varieties withsmall starch granule diameters (≤3 μ) can beused for expanded and homogeneous popping.Varieties with stable percentages of amyloseand amylopectin can be used for making pud-dings, gelatinised baby food, instant creams,and noodles, among others. Using quinoa in

processed products is congruent with the goals ofconservation and preservation of genetic diversity.

Molecular characterization

Two types of markers (SSR and ISSR) were usedto characterize 86% (2,701 accessions) of the Boli-vian collection. The markers revealed 3 to 13 poly-morphic alleles, generating a genetic fingerprintfor each quinoa accession. Furthermore, using theinformation generated, similar accessions can begrouped and related at a molecular level. In addi-tion, the DNA extraction method for quinoa wasstandardized.

Multiplication and regenerationof quinoa germplasm

Although the seeds from the quinoa germplasmare stored in optimum conditions, with thepassage of time they decrease in both quantity(because of use and distribution) and germinationpercentage. According to Jaramillo and Baena(2000), if the objective is to bring seed samples toan optimal number, the process is termed “mul-tiplication”; if the goal is to recover the initialgermination percentage, the process is called“regeneration” or “rejuvenation.” In any case,samples obtained from the multiplication and/orregeneration process must be viable, healthy, of


optimum size for storage, and genetically identicalto the original sample.

Monitoring of seed quantityand percentage of seed germination

A seed sample is in optimum condition when it isviable in terms of germination and in sufficientquantity. If the sample does not meet any ofthese requirements, it must be multiplied and/orregenerated, a decision that comes from moni-toring both the size and viability of accessions.Monitoring is governed by rules and proce-dures according to the Standard for Genebanks(FAO/IPGRI 1994).

Monitoring for sample size

The jars used to store the Bolivian collection ofquinoa have a capacity of 1,000 g. It is best tofill the container with seed to its full capacity.However, this amount of seed decreases with theuse of germplasm for research activities, cropbreeding, introduction or reintroduction to com-munities, and also with the distribution of seedsto meet requests received by the genebank. Thus,monitoring for sample size should be continuousto keep the amount of seed from reaching a levelbelow 60 g. It has been determined that 60 g ofseed is the minimum acceptable level while at thesame time keeping a sufficient quantity of seedreadily available for a research test or a plot of70 m2 (Rojas and Bonifacio 2001).

The monitoring process must record theuse and distribution of germplasm, and theinformation generated corresponds to the quinoagermplasm management data. Once the samplequinoa reaches a level less than 60 g, multiplica-tion of the sample must be programmed, wherebythe seeds are increased under optimal cultureconditions.

Monitoring germination of the sample

According to the Standard for Genebanks(FAO/IPGRI 1994), the interval between germi-nation tests depends on the species and storageconditions. For seeds that have been stored under

short and medium term conditions, a germinationtest every 5 years is sufficient. Another importantaspect to consider is the number of accessionsheld in the germplasm collection. In the case ofquinoa, if there are 100–200 accessions, it is bestto conduct annual monitoring of germination.However, for a greater number of accessions, agermination control test is recommended every3–5 years, although this will also depend on thenature of the genetic material.

For germination control tests, a seed sampleis subjected to germination tests according toISTA guidelines (1993). The results obtainedshould be compared with the initial germinationpercentage of the same sample collected duringthe “preliminary multiplication” period. If thegermination percentage is less than 85%, thesample must be regenerated. The decision toregenerate and/or multiply a sample should notdepend on the amount of the sample, whether ornot it is nearing the minimum quantity allowed.Germination percentage takes priority over theamount of seed. It will be more urgent to regener-ate a large sample whose germination is low thanto regenerate a small sample whose germinationis optimal. However, regeneration should notbe done often either because it is expensiveand may compromise the genetic integrity ofthe germplasm if the sample is contaminated(Jaramillo and Baena 2000).

Technical procedure for multiplicationand/or regeneration

Once the need to carry out regeneration and/ormultiplication work is determined, the quinoagermplasm must be established in field plots orgreenhouses and managed in the most optimalconditions for good crop development. Thiswill ensure that the quinoa samples obtainedare viable, healthy, in sufficient quantities, andgenetically identical to the original sample.

Field plots/greenhouses

Depending on the place of origin of the quinoaaccession and on the conditions of the siteintended for multiplication and/or regeneration,


it is recommended that this activity be done underfield conditions so quinoa plants can express theirgenetic potential in natural environments. In fieldplots, there should be six rows per accession, witha furrow 5 m long. Once quinoa plants reach phys-iological maturity, the four central rows shouldbe harvested, leaving 50 cm headers at both endsof the plot. If there is less available land, plotswith four rows per accession can also be planted.To facilitate management, the rows should bespaced uniformly. Crop management practicesusually carried out on the quinoa crop should beperformed in a timely manner. However, if anaccession has a small amount of seed or very lowlevels of germination, it requires more care toregenerate or multiply it. Therefore, the samplecan be grown in greenhouses or under controlledenvironments, where suitable substrates forsowing can be prepared, soil moisture controlledwith appropriate irrigation, and temperatureregulated with simple aeration systems.

Prevention of pollen exchange

Great care should be taken to prevent gene flowand contamination by pollen exchange betweentwo accessions, because quinoa is a partiallyallogamous species (10–15%). To overcome thischallenge, accessions with short phenologicalcycle can be planted alternately with accessionsthat have long phenological cycle, so that theirflowering phases do not coincide. Panicles canalso be bagged using paper envelopes immediatelybefore the quinoa plants enter the flowering phase.Another way to reduce allogamy and preventcontamination is to plant other crops in alternaterows with quinoa, preferably those similar inheight or architecture. It is also equally importantto avoid mechanical mixing of accessions, whichis common when handling quinoa germplasm,especially during threshing and venting. Carefuland correct management of the identification ofevery accession is recommended, from its estab-lishment in the field to harvest and postharvestoperations.

Finally, once the quinoa germplasm sampleis multiplied and/or regenerated, the germi-nation test must be redone. After fulfilling the

requirements established by the Standard forGenebanks (FAO/IPGRI 1994) and for quinoagermplasm, the sample must be conditionedfor the corresponding storage duration. Thepercentage of germination and the quantity ofseed both serve as points of reference for the nextmonitoring cycle.

Regeneration schedule

When a germplasm collection consists of thou-sands of accessions, such as the case of theBolivian quinoa germplasm collection, this stagein the genebank management requires consider-able attention to technical details. Because of thewide genetic variability of the accessions, differentgrowth traits and behaviors are expected whenevaluating germination percentage over time.

To develop a regeneration schedule of thegermplasm collection, the “monitoring of ger-mination behavior” has been implemented since2004 in a continuous manner in different groupsof cultivated and wild quinoa. This work beganwith the formation of nine groups of cultivatedquinoa and five groups of wild quinoa withsimilar germination percentages. Representativeaccessions were selected from each group, whiletaking into consideration the agromorphologicalvariability and passport data of these accessions.

Fig. 8.9 shows half-year results for the period2004–2010 from the four groups of cultivatedquinoa (Q-1, Q-2, Q-3, and Q-4) and two groupsof wild quinoa (QS-1 and QS-2), stored undershort and medium term conditions. As expected,the results indicate that there is a variation inthe levels of maintenance of seed germination.In general, an average reduction of germinationfrom 8% to 40% was observed for the studyperiod. From these results, it can be seen thatQ-1 seeds need to be regenerated after 2 years ofstorage, the Q-2 seeds after 4 years, and the Q-3seeds after 6 years, as germination levels are belowthe level required by the Standard for Genebanks(FAO/IPGRI 1994).

While this schedule of quinoa germplasmregeneration is still being developed, it clearlyindicates that generalizations cannot be made


I-200

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0

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0

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405060708090

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Q - 2 Q - 3 Q - 4 QS - 5 QS - 2Q - 1

Fig. 8.9 Germination behavior in four groups of cultivated quinoa and two groups of wild quinoa. Q-1, Q-2, Q-3 and Q-4 arethe cultivated quinoa groups, while QS-1 and QS-2 are the wild quinoa groups.

when managing a germplasm collection, partic-ularly at the stage of seed regeneration. Withoutdoubt, the wide genetic variability of the quinoagermplasm collection, as well as storage condi-tions, determines the internal moisture content ofthe seeds and the fat content of the seeds, amongothers.

Documentation and informationon quinoa germplasm

The management and conservation of quinoagermplasm in its various stages comprises a seriesof activities for which information is neededor where information is derived. Recording,organizing, and analyzing data all comprise the“documentation” stage of germplasm man-agement. Documentation is fundamental tothe exploration and characterization of thegermplasm, and in making decisions about itsmanagement. The value of a germplasm collec-tion increases as it is characterized and studied;hence, the importance of good documentation(Jaramillo and Baena 2000). The likelihoodthat a particular quinoa accession will be usedincreases to the extent that information on itscharacteristics and genetic potential is available.A quinoa accession cannot be considered for usewithout pertinent information, so it is essentialto document information as systematically aspossible, and with as much detail.

The information on the Bolivian quinoagermplasm is managed under a manual andelectronic documentation system. Manual doc-umentation consists of recording information infield books or record books, which are practicalto handle when gathering information duringcollection trips. These manually documented dataare transferred to electronic documentation sys-tems on Excel, pcGRIN, and SIRGEN databases(Table 8.4).

Information on the germplasm collectionis organized into three data sets consisting ofpassport data collection, characterization andevaluation data, and management data. Thepassport and collection data consists of 31 vari-ables recorded at the time of collection and/orreception of quinoa accessions. In the manualsystem, there is a book of “passport data” anda file of “collection forms” for the germplasmcollection. More information on the 31 variablesis presented in Annex 8.1.

For the characterization and evaluation data,agromorphological information is organized into59 qualitative and quantitative variables, both inthe manual and in the electronic system (Rojaset al. 2001; Pinto et al. 2009). The nutritional andagro-food value information of the quinoa grainis organized into six variables of nutritional value(protein, fat, ash, crude fiber, carbohydrates,moisture, and caloric energy) and three agro-food


Table 8.4 Quinoa Germplasm Information Documented in the Manual and Electronic Systems.

System Ex situ Conservation

Manual documentation Collection formsPassport Data BooksCharacterization and evaluation Data BookField BooksSeed movement logbookHerbarium specimens

Electronic documentation pcGRIN quinoaPassport data, characterization and evaluationData on nutritional and agro-food valueRegistration data on temperature and humidity of the storageroom BNGAData on the quantity of seed and percentage of germinationof the accessions

variables (size of starch granule, percentage ofinverted sugars, and water filling). Molecularinformation is organized in the electronic docu-mentation system and consists of DNA fragmentsof different sizes (base pairs) revealed with SSRand ISSR markers.

The quinoa germplasm management datacorresponds to the information generated frommonitoring of the percent germination, samplesize, initial seed moisture, number of regenera-tions and/or multiplications, temperature andhumidity recording in the storage chamber, anddistribution of seeds. Analysis of the informationthat has been generated and documented helpsin the decision making process to improve andoptimize the management of quinoa germplasm.In addition, using the genebank information,documents were produced and disseminated topromote the use of Bolivia quinoa germplasm.The following are some publications produced:document on the management strategy of theNational Genebank of Andean grains, germplasmcatalogs, technical bulletins, brochures, book-lets, calendars, banners, reading for secondaryschool biology books (conservation of our plantgenetic resources – genebanks), graduate andpost graduate theses, scientific articles, and presspublications.

Utilization of quinoa germplasm

The increasing population growth and reductionof land available for agriculture make it criticalto increase food production and attain a more

equitable distribution (FAO 1996). In orderto do this, plant genetic resources need to beutilized judiciously (Cadima et al. 2009). Theuse of germplasm depends on knowing where itcomes from, its characteristics and usefulness,and on keeping it viable and available (Jaramilloand Baena 2000). The strategy developed byPROINPA for the management of plant geneticresources involves three steps: direct use, indirectuse, and social use.

Direct use

The direct use of germplasm consists of identi-fying promising quinoa accessions with desirablecharacteristics, to introduce or reintroduce thesein their original form into other regions or com-munities. In the Bolivian quinoa genebank, directuse of germplasm began with the analysis of theresults of agromorphological characterizationand evaluation. Afterwards, quinoa accessionswith desirable traits (high yield, large grains,plant architecture, and place of origin) wereidentified and given to farmers for direct use.Training courses on the varied uses of quinoafor food processing were also developed by thegenebank for direct use by farmers and traditionalagro-food processors.

Procedure to apply participatory evaluationtechniques for quinoa

“Participatory evaluation techniques” are toolsthat allow farmers to be involved in the


decision-making process regarding one orseveral new technologies. These techniques wereapplied to the quinoa accessions. This form ofquinoa utilization requires direct work with farm-ers in communities where quinoa is produced(Pinto et al. 2010). Participatory evaluations wereperformed during the flowering stage and harvest.

The “participatory evaluation techniques”were implemented from first contact with farmersto delivery of seeds to participating families. First,quinoa accessions were identified on the basis ofthe analysis of results from the characterizationand evaluation of the germplasm collection.Then, communities where these accessionswould be produced were identified. Traditionallyconservative communities and/or those withthe potential to produce the crop were selected.The farmers’ level of motivation and interest inparticipating in the process was also consideredduring the selection process. Afterwards, whilerespecting the customs of each place, contactwas made with local communal authorities andfarmers in the selected communities and planningcommenced. With the active involvement offarmers, field evaluation plots were establishedand quinoa accessions planted. Throughout thecourse of the crop cycle, farmers and techniciansconducted crop management activities such astilling, weeding, fertilizing, roguing, and applyingphytosanitary controls. At the flowering stage ofthe crop, a participatory evaluation was conductedinvolving 10 farmers (men and women) who usedthe “absolute evaluation” method that evaluateseach alternative on a fixed or absolute scale.Afterwards, farmers from the local communitieshelped harvest and thresh the quinoa accessions.Harvest from each individual accession wasplaced in bags of the same size, for comparison ofquantities obtained. Participatory evaluation ofthe grain was then conducted, using the “order ofpreferences” method that facilitates a comparisonbetween the different alternatives. Again, 10hardworking and communicative farmers (menand women) who had superior knowledge ofthe quinoa crop were chosen for this activity.A participatory evaluation of food productswas also conducted to determine the culinarypotential of the accessions, and the “order of

preference” technique was again used, wherefarmers compare each technological alternativeagainst the others. Finally, seeds of the quinoaaccessions that were preferred and selected bythe farmers were distributed to the farmers in thepresence of technical staff and local communityauthorities.

Participatory assessments with quinoa germplasm

From the agricultural year 2002–2003 to2007–2008, participatory assessments wereconducted on 29 germplasm accessions and 4local varieties (Local, Wila Jupha, Wila Cayuniand Acujuira) in 22 communities in the centraland northern Altiplano of Bolivia (Table 8.5).

Two participatory evaluation techniqueswere applied, namely, the “absolute evaluation”technique in the flowering phase and the “orderof preference” technique during harvest (grain).The most frequent selection criteria used forquinoa accessions were tall plants, large panicles,resistance to frost, large grain size, white grain,good yield, and rapid maturation. Fourteenaccessions, namely, accessions 2527, 3130, 2522,2529, 2394, L320, 2943, 2031, 2857, 1667, 2516,1560, 1474, and 2401, were selected by farmers(60% male and 40% female). The seeds of theselected accessions were distributed in eachcommunity to the farmers who participated inthe whole process, so they could cultivate these intheir land and introduce these in their traditionalcrop systems for the next year.

The contribution of the farmer participatoryprocess is reflected in the introduction and rein-troduction of quinoa germplasm to communities.The flow of genetic material has strengthened thein situ conservation of crop diversity and its usein communities. Equally important, farmers havebecome aware of the existence of the Bolivianquinoa collection and the role of the genebank incase they deplete their seed stock.

Training courses on the varied uses of quinoa

From 2005 to 2006, training courses on foodpreparation based on quinoa germplasmaccessions were conducted in communitiessurrounding Lake Titicaca. These courses were


Table 8.5 Quinoa Accessions Evaluated Using Participatory Techniques Through-out Six Farming Years (2002–2008) and the Participating Communities.

Agricultural Quinoa Accessions andYear Communities Local Landraces

2002–2003 JalsuriSan Pedro – San PabloKalla ArribaChahuira ChicoVitu CalacachiPomposilloTacaca

05330547175016672031239023942411252225162527L-26

2003–2004 Salviani 16672031239023942516252225293130Local

2004–2005 AntaraniPataraniRosapataErbenkallaCoromata Media

0027057516411655165916671927203123902394251625222527252925613130Local

2005–2006 CachilayaCutusumaCutusuma altaTitijoniCariquina grandeJutilayaHuancaramaLlanga

1713002716672031239425112516252728572943


Table 8.5 (Continued)

Agricultural Quinoa Accessions andYear Communities Local Landraces

3130Wila jupaWila coyuni

2006–2007 PataraniCariquina Grande

14741560164123902401251625272857L320Acujuira

2007–2008 Santiago de Okola 14742511268928572943Local

developed to promote the varied uses of quinoa.For these courses, accessions 2943, 2637, 0081,0381, 1667, 2511, and 0027 were used. Thequinoa accessions were evaluated by farmers in aparticipatory process to determine their suitabil-ity for various culinary products. The followingfood preparations were promoted: quinoa cake,quinoa cookies, quinoa and apple juice blend,boiled quinoa Valencia style, quinoa bread, quinoafried buns, quinoa tamales, and quinoa pancake.The “order of preference” technique was usedto determine that accessions 1667 and 2943 weregood for making quinoa and apple juice blend,while accessions 2511 and 0027 were good forquinoa bread and cake.

The training courses were conducted incommunities where participatory evaluations ofthe quinoa crop had been conducted previously.This was done in order to promote the use ofquinoa in food preparations in communitieswhere selected accessions of quinoa had beendistributed to farmers. A total of 18 trainingcourses in eight communities of five provincesfrom the department of La Paz were conducted,attended by 397 male and female farmers. Therewere more women who participated than men,

because of the role of women in home foodpreparation (Table 8.6).

Indirect use

The indirect use of quinoa is linked to crop breed-ing. As with any crop improvement program,quinoa breeding objectives are to (i) increaseproduction through yield, agronomic traits and,resistance to pests and diseases; and (ii) increasethe quality of products through nutritional andagribusiness characteristics, such as grain shape,grain color, and storage life attributes.

In Bolivia, research on quinoa breeding beganin the early 1960s in the Patacamaya ExperimentalStation, initially under the administration of theInstitute of Andean Crops, which was underthe Ministry of Agriculture, and then under theadministration of the IBTA. During this period,Bolivia consolidated a quinoa breeding program,which was a pioneer in the Andean region, todevelop not only quinoa varieties but also thetechnical skills of its workforce. Later, PROINPAcontinued the quinoa breeding program, makingcrosses and monitoring generations to obtain newquinoa varieties.


Table 8.6 Number of Communities, Courses and Participants in Training Events on New Ways of PreparingQuinoa Food Products (2005–2008).

Agricultural Number ofYear N∘ Community Province Courses Participants

2005–2006 1 Antarani Pacajes 1 152 Cariquina Grande Camacho 1 233 Titijoni Ingavi 1 394 Cachilaya Zone A Los Andes 1 625 Jutilaya Camacho 1 376 Cachilaya Zone B Los Andes 1 487 Cutusuma Los Andes 1 478 Coromata Media Omasuyos 1 40

2006–2007 1 Titijoni Ingavi 2 272 Cachilaya Los Andes 2 223 Cariquina Grande Camacho 2 37

2007–2008 1 Titijoni Ingavi 1 112 Cachilaya Los Andes 2 343 Cariquina Grande Camacho 1 11

Total 18 453

In Bolivia, the initial focus of the quinoa breed-ing program was to develop high-performingvarieties with large grain size, white color, andsaponin free. In the course of time, changesin the quinoa market and weather patternshave adjusted priorities for crop improvement,without neglecting productivity. In the late1990s, brown and black quinoa grains, knownin the international market as “red quinoa” and“black quinoa,” were included in the breedingprocess. At the end of the 1990s, the earlinesstrait was also considered in the breeding processto cope with delayed rains, thus introducing thepossibility of planting crops until November andharvesting within a shorter growing cycle. Thereare 24 varieties of quinoa in Bolivia obtained bybreeding through hybridization and/or selection(Table 8.7). There is also a complex of at least54 known bitter varieties with the name “RoyalQuinoa” (Bonifacio et al. 2012), of which thevarieties Real Blanca, Toledo, Pandela, K’ellu,and Black Pisankalla dominate the export market.

Quinoa core collection

When germplasm collections are composed of alarge number of accessions, such as the case of theBolivian quinoa germplasm, the selection of a core

collection is necessary to facilitate managementand encourage the use of quinoa germplasm.Core collections are a subset of the completecollection, representing between 10 and 15%of the accessions, and have the highest possiblegenetic variability (70–80%) in the germplasmcollection. It is important to highlight that corecollections do not replace the total collection,yet are accepted as effective tools to improve theconservation and use of germplasm collections(Rojas 2010).

The quinoa core collection was selectedthrough statistical analysis of 2,514 accessionsusing 18 quantitative variables. The core col-lection consists of 267 accessions, representing10.6% of the accessions analyzed (Rojas 2010).The quinoa core collection has guided the workof the crop breeding program and has facilitatedthe selection of progenitors. The accessions thatcomprise the core collection are currently inhybridization and selection processes to developvarieties tolerant and/or resistant to biotic andabiotic factors.

Social use

Genetic resources are the basis for the survivalof humanity. They are vital for developingcountries, to be utilized for the benefit of current


Table 8.7 Bolivian quinoa varieties obtained through breeding.

Number Variety Material of origin Year

1 Sajama 0547 0559 19672 Samaranti Individual selection 19823 Huaranga Selection S-67 19824 Kamiri S-67 0005 19865 Chucapaca 0086 0005 19866 Sayaña Sajama 1513 19927 Ratuqui 1489 Kamiri 19938 Robura Individual selection 19949 Jiskitu Individual selection 199410 Amilda Individual selection 199411 Santa Maria 1489 Huaranga 199612 Intinayra Kamiri F4(28)xH 199613 Surumi Sajama Ch’iara 199614 Jilata L-350 1493 199615 Jumataqui Kallcha 26(85) 199616 Patacamaya Samaranti Kaslala 199617 Mañiqueña Selection 1489 199918 Caraquimeña Selection DC 200319 Jacha Grano 1489 Huaranga 200320 Kosuña 1489 L-349 200521 Kurmi 1489 Marangani 200522 Horizontes 1489 L-349 200723 Aynoq’a Selection L-118 200724 Blanquita Selection L-320 2007

Source: Personal elaboration based on Espindola and Bonifacio (1996), Bonifacio et al.(2006), and Rojas-Beltran et al. (2010).

and future communities. Therefore, there is greatvalue in increasing awareness among the generalpopulation, especially the younger generation,about the importance of conservation and sus-tainable use of genetic resources. Based on theexperience of PROINPA, the social use of quinoaare in distinguished advocacy and disseminationcampaigns, participation in formal and informaleducation, and empowerment of local populationsand authorities (Cadima et al. 2009).

Promotion and dissemination

As a key element in supporting the conservation ofgenetic resources, promotion and disseminationactivities are aimed at encouraging the consump-tion and use of native species and crops. In thissense, information gathered from the geneticmaterial in the quinoa germplasm collection canbe the basis for advocacy and dissemination.

A key promotion activity of the genebankis participation in biodiversity fairs, as wellas dissemination of information through massmedia. To promote the benefits of quinoa,the genebank participated in urban and ruralfairs with banners containing information onthe ex situ conservation of quinoa germplasm.Germplasm samples were also exhibited, togetherwith samples of quinoa biscuits and cakes, tohighlight quinoa diversity (Table 8.8). Publica-tions about the management and conservationof quinoa germplasm were also distributed tobooth visitors. Information about the geneticwealth of quinoa and its nutritional valuewas promoted and disseminated throughthe newspapers “La Prensa” and “NuestrosPueblos,” in concert with genebank activities.The germplasm collection was also promotedthrough mass media such as Radio San Gabriel,which has urban and rural outreach. Radioscripts were also developed on topics such as

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“Quinoa Germplasm Bank,” “First Meetingof Farmers,” “Diversification of Quinoa-basedFood Uses,” “Participatory Evaluations,” “CropCultivation of Quinoa,” “Quinoa Seed Flowsin Fairs,” Diversity Contests,” “Testimonialson Diversity Contests,” “Biodiversity Fairs,”“Quinoa Planting,” “Quinoa Pest and Dis-ease Control,” “Quinoa Harvest,”“MedicinalValue of Quinoa,” Quinoa Nutritional Value,”and “Cultural Value of Quinoa,” for a totalof 28 scripts. The booklets were disseminatedthrough the “Agricultural” program in RadioSan Gabriel. Additionally, through the program“Palabra Rural” aired by Bolivia TV, documen-taries entitled “Quinoa germplasm bank andits role in the conservation of strategic geneticresources for the country” and “Diffusion ofquinoa varieties and accessions” were broadcast(Table 8.8).

Formal and informal education

More than 30 lectures and talks were given tofarmers; students and teachers from schools,colleges and, public and private universities; aswell as technicians and researchers from differentresearch institutions dedicated to Andean grains.Depending on the target audience, the lecturescovered the following topics: “Origin and Dis-tribution of Quinoa,” “Quinoa of Nutritional,Economic, Medical and Adaptive Importance,”“Training Quinoa Germplasm Bank,” “Con-ditions of Conservation of Genetic Material,”“Conservation ex situ,” “In situ Conservation,”and “Use of Genetic Material and Its NutritionalValue” (Table 8.9).

At conferences and lectures, seed samples ofthe quinoa germplasm collection were used toillustrate variation in shape, size, and color ofgrains. Quinoa panicles and plants were displayedto show differences in panicle shape and color,plant architecture, and other morphologicaltraits. Toward the middle part and end of thetalk, quinoa-based products such as biscuits,juice, pancakes, and nougats were tasted andappreciated by the audience.

CONCLUSIONS

Plant genetic resources are essential for foodsecurity and sovereignty of people groups world-wide, and contribute substantially to humanity’sbasic needs. These genetic resources are part ofthe ancestral and cultural heritage of countries.Their conservation and use is a responsibility thatmust be assumed by society in general, with theleadership of governments and the state. Thosetimes when the responsibility of managing geneticresources fell solely on particular institutions ororganizations are over. Now, all segments of theBolivian society must assume the responsibility,because it concerns everyone. We must start byvaluing this genetic heritage, recognizing that it ispart of our cultural identity, and be proud of thegenetic diversity under our stewardship. We needto teach our children the value and role played byplant genetic resources for the benefit of societyas a whole.

The conservation of plant genetic resourcesrequires institutional support through solidinfrastructures backed by clear policies andheaded by governments. State governments haveto provide sustained financial resources for vitalconservation activities. According to studies, theconservation of a sample of germplasm costsbetween 5 and 10 USD per year. No effort shouldbe spared when allocating annual budgets becausethese are valuable resources that should be passedon from generation to generation to support ourvery existence. Governments must also play aleading role in the specialized training of person-nel while ensuring work stability. At the sametime, governments must establish infrastructuresthat meet the minimum equipment conditionsrequired to manage and conserve germplasmcollections.

Management of the Bolivian quinoa germplasmcollection has allowed us to experience variedtechnical, social and financial situations. Vocationand commitment to work were the key elementsthat enabled us to make the Bolivian quinoagenebank the most important quinoa genebankin the world, with the greatest diversity andlargest number of accessions (FAO 2010). Thisis an exceptional achievement, especially in a

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156


EXPEDITION:

1.NAME(S) OF COLLECTOR(S):

2. NAME OF FARMER:

:REBMUN NOISSECCA .4 :REBMUN ELPMAS .3

5. DATE OF COLLECCTION (DD/MM/YYYY): 6. REGISTRATION DATE:

7. GENUS:

8. SPECIES:

9. LOCAL NAME(S):

10. ETHNIC GROUP OF THE RESPONDENT:

:TNEMTRAPED.21 :YRTNUOC .11

:YTILAPICINUM .41 :ECNIVORP .31

:YTINUMMOC .61 :NOTNAC .51

17. LOCATION: at Km, fromin direction (North / South / East / West)

18. LAT (° ' ") N/S 19. LONG (° ' ") E/O 20. ALT (m.a.s.l.)

21. TYPE OF SAMPLE

1. Wild 4. Breeding line

2. Undergrowth 5. Advanced crop (variety)

3. Native crop 6. Other (specify)

22. SITE / SOURCE OF COLLECTION

1. Habitat: Wild Prairie Desert Salt Flatlands

2. Farm:Field plot Huerto / Garden Crop Bordure Intercropping Storage

3. Market/Fair:City Town Community

)yficeps( rehtO .5 nóicagitsevni ed otutitsnI .4

23. USES OF THE PLANT / PARTS 1. Food: Grains

LeafStem / branches Root

2. Medicinal: Grains Leaf Stem / branches Root

3. Beverages: Grains Leaf Stem / branches Root

4. Crafts: Grains Leaf Stem / branches Root

5. Foliage: Grains Leaf Stem / branches Root

6. Ornamental: Grains Leaf Stem / branches Root

)yficeps( rehtO .7

24. INFLORESCENCE COLOR ( :ROLOC METS .52 :)ELCINAP

:)ELCINAP( EPAHS ECNECSEROLFNI .62

etaidemretnI .3 mrof-htnaramA.2 detaluremolG .1

27. GROWTH HABIT

elcinap niam denifednU .4 sehcnarB gnoL .3 sehcnarB trohS .2elpmiS .1

dexiM .2 mrofinU .1 :NOITALUPOP ELPMAS .82

:DELPMAS STNALP FO REBMUN .92

?ynam woH oN seY ?NEKAT SERUTCIP EREW .03

31. OBSERVATIONS:

ANNEX 8.1QUINOA GERMPLASM COLLECTION FORM


developing country such as Bolivia, where con-servation of genetic resources and technologicaladvancements are not always a priority. We havelearned many valuable lessons from the wholeprocess of managing the quinoa collection. Thereare still many goals to be accomplished, and weshould be motivated to continue studying quinoaand other plant species, especially underutilizedspecies, such as cañahua, amaranth, and lupine.These species, owing to particular characteristics,can be grown for food in places of extreme povertyand adverse weather conditions. Thus, utilizationof these plant species should be a priority for allcountries worldwide.

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[FAO/IPGRI] Food and Agriculture Organization of the UnitedNations/International Plant Genetic Resources Institute.1994. Genebanks standards. United Nations Food andAgriculture Organization & International Plant GeneticResources Institute, Rome, 1–13.

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Jaramillo S, Baena M. 2000. Material de apoyo a la capacitación enconservación ex situ de recursos fitogenéticos. Instituto Inter-nacional de Recursos Fitogenéticos, Cali, Colombia. 1–210.

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Lescano JL. 1989. Avances sobre los recursos fitogenéticosaltoandinos. En: Curso: cultivos altoandinos. Potosí, Bolivia.17–21 de abril de 1989, pp. 19–35.

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Rojas W, Bonifacio A, Aroni G, Aroni JC. 1999. Recolección denuevas accesiones de quinua y otras Chenopodiaceas. InformeAnual 1998–99. Fundación PROINPA, pp. 1–5.

Rojas W, Bonifacio A. 2001. Multiplicación de accesiones tardíasde quinua bajo condiciones de invernadero. Informe Anual2000/2001. Fundación PROINPA, pp.. 1–4.

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Rojas W. 2002a. Distribución geográfica de la colección de germo-plasma de quinua. Informe Anual 2001/2002. Proyecto Mck-night. Fundación PROINPA, pp. 1–5.

Rojas W. 2002b. Recolección de germoplasma de cañahua yquinua. Informe Técnico Anual 2001–2002. Año 1. Proyecto“Elevar la contribución que hacen las especies olvidadas ysubutilizadas a la seguridad alimentaria y a los ingresos dela población rural de escasos recursos”. IPGRI – IFAD. LaPaz, Bolivia: Fundación PROINPA, pp. 13–21.

Rojas W, Camargo A. 2002. Reducción de la humedad del granode quinua para almacenamiento a largo plazo. Informe anual2001–2002 Proyecto Mcknight. Fundación PROINPA, pp.1–6.

Rojas W. 2003. Multivariate analysis of genetic diversity of Boli-vian quinoa germplasm. Food Reviews International 19:9–23.

Rojas W, Camargo A. 2003. Establecimiento de un método dereducción del contenido de la humedad del grano de quinua.Informe Anual 2002/2003. Proyecto Mcknight. FundaciónPROINPA, pp. 1–4.

Rojas W, Pinto M, Camargo A. 2003a. Recolección descentral-izada de germoplasma de cañahua y quinua. Informe TécnicoAnual 2002–2003. Año 2. Proyecto IPGRI - IFAD “Elevar lacontribución que hacen las especies olvidadas y subutilizadasa la seguridad alimentaria y a los ingresos de la población ruralde escasos recursos.” La Paz, Bolivia: Fundación PROINPA.9–18.

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Chapter 9

Quinoa Breeding in Africa: History,Goals, and Progress

Moses F.A. Maliro1 and Veronica Guwela2

1Department of Crop and Soil Sciences, Bunda College Campus, Lilongwe University of Agricultureand Natural Resources, P.O. Box 219, Lilongwe, Malawi

2International Crops Research Institute for the Semi-Arid Tropics, P.O Box 1098, Lilongwe, Malawi

INTRODUCTION

Origin of quinoa

Quinoa (Chenopodium quinoa Willd.) is an Andeancrop belonging to the family Chenopodiaceae. It isa highly nutritious grain-like crop that has beena staple for centuries in South America, amongpre-Columbian Andean farming communitiesfrom Colombia to Ecuador (Wilson 1990; Schlickand Bubenheim 1993; Bhargava et al. 2007). It isnative to several countries of the Andean region,from Colombia to the north of Argentina andthe south of Chile. History shows that the crophas been cultivated for at least 5,000 years inLatin America and was the staple food of theInca Empire for many centuries (Schlick andBubenheim 1993). In the 1500s, the Spanishconquerors banned quinoa cultivation in SouthAmerica (Cusack 1984) and, hence, it became aminor crop, grown only by small-scale farmersfor local consumption in remote areas of Bolivia,Peru, and Colombia (Jacobsen and Stølen 1993).

At present, the major producers of quinoaare Bolivia, Peru, and the United States. Quinoacultivation has today transcended continentalboundaries; thus, it is now grown in France,


England, Sweden, Denmark, Holland, and Italy.In the United States, it is grown in Colorado andthe Pacific Northwest, and in Canada, it is grownin Saskatchewan. Quinoa has shown high yieldsin Kenya and has also been grown successfully inthe Himalayas and the plains of northern India(Jacobsen et al. 2003a, b).

Introducing quinoa in Africa

Food security in Africa

The nutritional superiority of quinoa comparedto other crops has been recognized in recentyears (Jacobsen et al. 2003b), and demand forquinoa has soared in developed countries wherethere is more consciousness about wellnessthrough healthy diets. The increasing popularityof quinoa has triggered intensive research andbreeding to promote its production and meet thegrowing market demand. In developing countries,particularly in Africa, the introduction of quinoainto the diet has the potential to contribute tofood and nutritional security.

While food insecurity in some African coun-tries may be attributed to political instabilities andcivil wars, in the majority of African countries,

161


food insecurity is due to natural disasters.Recently, droughts and unpredictable rainfallpatterns have been exacerbated by climate changeeffects. Even in times when food production hasbeen adequate, many children and adults are stillmalnourished because maize is the predominantstaple food and the main source of energy inthe African diet. Protein-rich crops such ascommon bean and cowpea are grown as minorcrops by most of the small-scale farmers whodominate African agriculture. Consequently,malnutrition has been one of major causes ofinfant mortality among children under 5 years ofage (Table 9.1, FAO 2012a; Babatunde et al. 2011)and stuntedness among adults.

Prevalence of malnutrition

Quinoa production in Africa has the potentialto contribute to reducing malnutrition, which isa problem among both rural and urban peoplein Malawi and other African countries. On thebasis of three anthropometric indices, resultsof the 2010 Malawi Demographic and HealthSurvey (NSO 2010) showed that malnutrition

is still high among children under 5 years ofage. Height-for-age is the measure of lineargrowth and used as a measure of the nutritionalstatus of a child. Children who are below −2standard deviations from the reference meanfor height-for-age are considered stunted orshort for their age. Stuntedness is a reflection ofthe cumulative effect of chronic malnutrition.In 2010, the percentage of children who werestunted (below −2 SD) was 47%. In rural areas,48% of children were stunted, whereas in urbanareas, 41% of children were stunted.

Another index of malnutrition is theweight-for-height ratio, wherein childrenwho are below −2 standard deviations from thereference mean are considered too thin for theirheights or considered “wasted,” a condition thatreflects acute or recent nutritional deficit. Theresults of NSO 2010 showed that 4% of thechildren were wasted and half of them severelywasted. Rural areas had 4% of children wasted,whereas urban areas had 2% of children wasted.

The weight-for-age ratio is an overall indica-tor of a population’s nutritional health; 13% of allchildren were underweight and 3% of these were

Table 9.1 Prevalence of undernourishment in selected African countries and in comparison with world overall levels (FAO2012a).

Proportion of undernourished in total population, %

Country 1990–1992 1999–2001 2004–2006 2007–2009 2010–2012 Change so far

World 18.6 15.0 13.8 12.9 12.5 −32.8Developed countries 1.9 1.6 1.2 1.3 1.4 NADeveloping countries 23.2 18.0 16.8 15.5 14.9 −35.8Morocco 7.1 6.2 5.2 5.2 5.5 −22.5Angola 63.9 47.5 35.1 30.7 27.4 −57.1Benin 22.4 16.4 13.1 10.8 8.1 −63.8Burundi 49.0 63.0 67.9 72.4 73.4 49.8Cameroon 38.7 29.1 19.5 15.6 15.7 −59.4Ethiopia 68.0 55.3 47.7 43.8 40.2 −40.9Kenya 35.6 32.8 32.9 32.4 30.4 −14.6Madagascar 24.8 32.4 28.1 29.1 33.4 34.7Malawi 44.8 26.8 24.7 23.0 23.1 −48.4Mali 25.3 21.5 14.7 9.5 7.9 −68.8Mozambique 57.1 45.3 40.3 39.9 39.2 −31.3Namibia 37.5 24.9 26.8 32.7 33.9 −9.6South Africa < 5 < 5 < 5 < 5 < 5 NATogo 32.8 25.2 20.4 19.8 16.5 −49.7Zambia 34.3 43.9 48.3 47.5 47.4 38.2Zimbabwe 44.1 43.1 38.2 33.9 32.8 −25.6

Quinoa Breeding in Africa: History, Goals, and Progress 163

severely underweight, and 13% of rural childrenwere underweight as compared with 10% of urbanchildren. In addition, the impact of weaning couldbe seen in younger children where data on all threeindices showed that the nutritional status of chil-dren deteriorated after 6 months of age, when chil-dren were being weaned. This case of malnutritionis prevalent across Africa as shown in Table 9.1(FAO 2012a).

Malnutrition compromises the body’s immu-nity, rendering children, pregnant women, andlactating mothers, as well as the elderly, vulnera-ble to diseases. Malnutrition contributes heavilyto the high mortality rates in Africa, especiallyin children. Therefore, introducing quinoa andpromoting its production and consumption inAfrica would be one of the interventions to solvethe malnutrition crisis.

Nutritional value of quinoa

Quinoa grain has an excellent balance of oil, fat,and protein content and has a unique compositionof amino acids. The protein in quinoa containsall eight essential amino acids needed for humangrowth and development. It is exceptionally highin lysine, cystine, and methionine, amino acidsthat are typically low in other cereals (Schlick andBubenheim 1993). Such nutritive value makesquinoa a relatively cheap yet excellent alternativegrain used in people’s diets and to fortify variousfood products. Quinoa grain ground into flour canbe used for biscuits and cakes, added directly intosoups, and can also be fermented with millet tomake beverages (Schlick and Bubenheim 1993).New promising products from the grain includemilk, protein concentrates, and natural colorants.The fresh leaves and tender shoots are eaten rawin salads or cooked and eaten as a vegetable inAfrican dishes.

Quinoa as alternative crop in Malawi

Quinoa can grow in a wide range of climaticconditions and potentially can be grown almostanywhere in the world. It has been reportedthat some quinoa varieties can tolerate salinitylevels as high as those present in sea water, with

electrical conductivity (EC) 40 dS% to 400 mMNaCl high salt tolerance (Jacobsen et al. 2001,2003a; Koyro and Eisa 2008; Hariadi et al. 2011;Adolf et al. 2012) and can grow under extremelydry conditions. It is a potential alternative cropin drought-prone areas of Africa, as it can growin areas with as low as 200 mm annual rainfall inpure sand. In areas where frost occurs, quinoa cansurvive night frost (−8∘C for 2–4 h) (Jacobsenet al. 2007). With the growing demand for quinoagrain in the United States, Europe, and Asia,the crop is a potential alternative export crop formany African countries such as Malawi. For somany years, Malawi has depended on tobaccoas its main source of foreign income, but lately,international demand for tobacco has dwindleddue to anti-smoking lobbies in many importingcountries. Thus, Malawi needs an alternativeexport crop and quinoa could well be it.

Increasing awareness about quinoa

In recognition of its excellent nutritional proper-ties and high adaptability, FAO selected quinoaas one of several promising crops with thepotential to sustain food security in the nextcentury (Jacobsen et al. 2003b). The FAO andUnited Nations also declared 2013 as the Yearof Quinoa (FAO 2012b; UN 2012) to recognizethe Andean indigenous peoples who have main-tained, protected, and preserved quinoa as foodfor present and future generations. Owing tothe recognition given by the FAO and UnitedNations to quinoa, more African agricultural andnutritional scientists have become aware of itspossible role in alleviating African food insecurity.

Ecological adaptation of quinoa

The high and balanced nutritive value of quinoa,in addition to other desirable attributes suchas tolerance to adverse growing conditions(Jacobsen et al. 2007), sparked a growing interestto introduce this crop into other regions of theworld. According to Jacobsen et al. (2003b),there is a good potential of growing quinoa whereenvironmental conditions are similar to thoseof the Andean region, specifically in parts of


southern Europe, the United States, Africa, andAsia. Studies on quinoa adaptability conductedin Europe produced promising results (Geertset al. 2008; Jacobsen et al. 1996; Jacobsen 1997,2003) such that in Denmark and certain areas inEurope, quinoa had been considered a future foodand fodder crop (Sigsgaard et al. 2008). Quinoaalso has a growing popularity in Canada (AAFRD2005). Africa can therefore take advantage of thegrowing world demand to produce quinoa forexport in addition to contributing to its own foodsecurity. The prospects of introducing quinoainto African farming systems are high as the cropis adapted to a wide range of ecological zones inthe Andean region where it originates. Quinoa canproduce grain yields even in unfavorable soil andclimatic conditions (Garcia et al. 2003). Quinoa’stolerance to arid conditions makes it an attractivecrop for farmers in drought-prone areas; hence,its cultivation has been expanding to Kenya,India, North America, and Europe. Most quinoagrowers are small farmers and the crop holds thepromise of improved income. Some of the poorestAndean indigenous farming communities havealready benefited greatly from the rising pricesdriven by demand for quinoa in world markets.

GOALS OF QUINOA BREEDING IN AFRICA

Quinoa was first introduced to Africa in the late1990s in Kenya and recently in Malawi in 2012.Quinoa cultivars from the Andean region andcultivars bred in the United States, Canada, andDenmark were supplied by the InternationalPotato Centre (CIP) and Washington StateUniversity (WSU) for adaptability studies. Thegoal of these initial breeding experiments wasto identify cultivars and varieties of quinoa thatcould grow well and yield grain for productionand consumption by African communities. Theultimate goal of these experiments is to contributeto efforts in reducing malnutrition problems inAfrica. From the breeding work, it is also expectedthat quinoa varieties will be developed and grownfor the domestic and export market, therebypresenting alternative cash crops, especially forsmall-scale farming communities of Africa. The

breeding experiments that have been carried outso far have focused on evaluation of introducedvarieties for adaptation to local ecological andclimatic conditions of Africa, specifically inMalawi and Kenya.

Quinoa studies under Malawi conditions

Cultivars introduced

Quinoa was first introduced in Malawi in 2012with 13 cultivars that originated from SouthAmerican countries and those that have been bredfor US and Denmark conditions (Table 9.2) andfor which seeds were supplied by WSU. Testingcultivars of diverse origin increases the likelihoodof selecting cultivars that can perform well underlocal conditions.

General climate conditions

Malawi has a diverse range of agroecologicalzones ranging from cool, highland areas towarm, low-lying areas. Its climate is described assubtropical, which is relatively dry and stronglyseasonal. The warm-wet season runs fromNovember to April, during which 95% of theannual precipitation occurs. Annual average rain-fall varies from 725 to 2,500 mm with Lilongwe inthe Central region having an average of 900 mm,Blantyre in the Southern region with 1,127 mm,Mzuzu in the Northern region with 1,289 mm,and Zomba in the Eastern region with 1,433 mmrainfall.

A cool, dry winter season runs from May toAugust with mean temperatures varying between17 and 27∘C, with temperatures falling between4 and 10∘C. Frost occurs in isolated areas in Juneand July. A warm, dry season lasts from Septem-ber to October with average temperatures varyingbetween 25 and 37∘C. Relative humidity rangesfrom 50% for the drier months of September andOctober to 87% for the wetter months of Januaryand February (MoNREE 2013) (Fig. 9.1).

Malawi has landforms that include highlands,escarpments, plateau and low-lying areas of thelakeshore, and the lower Shire valley. The high-lands consist of isolated mountainous areas with


Table 9.2 Quinoa varieties introduced in Malawi in 2012 for testing and their background information.

No. Variety Origin Background information

1 Ecuadorian Ecuador Not provided2 Black-seeded Colorado, USA Developed from cross between Chenopodium

quinoa and Chenopodium berlandieri, very tallvariety (>2 m tall)

3 Inca Red (a.k.a. Pasankalla) Bolivia Member of the “Salares” ecotype of quinoa4 Brightest Brilliant Rainbow Oregon, USA Not provided5 Bio-bio Chile Not provided6 Cherry Vanilla Oregon, USA Not provided7 Multi-Hued British Columbia, Canada Not provided8 Red Head Oregon, USA Not provided9 QQ74 Chile Chilean landrace10 Puno Denmark Bred by Sven-Erik Jacobsen11 Titicaca Denmark Bred by Sven-Erik Jacobsen12 QQ065 Chile Originally from extremely rainy region of southern

Chile (>2,500 mm annual precipitation); shortestvariety observed (∼0.8 m) and has shown highresistance to postharvest sprouting in Malawi trials

13 Rosa Junin Peru Not provided

elevations between 1,320 and 3,000 masl such asthe Nyika, Viphya, and Mulanje, whereas Dedzaand Zomba are between 960 and 1,600 masl. Theescarpments are areas that are around the high-land plateaus and mountains. The plateaus areat elevations of 750 to 1,300 masl. The low-lyingareas along the lakeshore are at 465–600 maslwhere the land is flat to gently undulating fromthe north to the south along the main outlet ofLake Malawi. The lowest lying areas are in theShire valley at the southernmost part of the coun-try with most elevations at less than 180 masl.The climate for each specific agroecologicalarea of the country is moderated by variationin the landform, thereby giving a wide range ofconditions across the country, from cool to warmto hot areas and from wet to drier areas (Fig. 9.1).

Plant growth performance

A wide range of crop species can be grown in acountry with a diversity of geographical areas,precipitation, and temperature. Thus, it shouldbe possible to grow quinoa quite well in Malawi.For instance, there are varieties of maize, a staplefood crop for the country, that have been bred andperform well in each specific agroecological zone.Adaptation trials that include quinoa cultivars and

ZAMBIA

ZAMBIA

Mzuzu

Lilongwe

MOZAMBIQUE

MOZAMBIQUE

Blantyre

S

EW

N

TANZANIA

Lake

mal

awi

Fig. 9.1 Map of Malawi showing temperature variationacross the country and these mainly influenced by mountainsand low-lying areas that characterize the country.

genotypes collected from diverse geographicalsources should generate information on whichspecific quinoa varieties will do well in variousagroecological zones of Malawi.

Eleven varieties/cultivars were evaluated fortheir adaptation in two ecological areas of thecountry using indices such as plant growth,


flowering, and grain yield. The first site wasBunda (1,200 masl) in Lilongwe district, repre-senting the mid-altitude agroecological zones.The second site was Bembeke (1,560 masl) inDedza district, representing higher altitudeagroecological zones. The experiment was con-ducted from July through the warmer months ofAugust, September, and October under irrigationconditions. The cultivars were also evaluatedunder warm rain-fed conditions during theDecember to April 2012/2013 cropping season atthe Bunda site.

Results in the Bunda and Bembeke sites and therain-fed site at Bunda showed promise for quinoaintroduction in Malawi. In the mid-altitude site(Bunda), all cultivars grew slowly for the first21 days after sowing but grew rapidly when theweather started to warm up in mid-August. In theBembeke highland site, quinoa grew extremelyslowly for the first 2 months, probably due tothe prolonged cold period experienced duringthe trials. By the time the weather warmed up,the plants were close to physiological maturity.Consequently, quinoa plants at the highland sitewere short, reaching only 50 cm in height, whileall the 11 cultivars at the mid-altitude site grew toheights of 90–100 cm. Plant height significantlyaffected panicle length that in turn affected thenumber of inflorescence, ultimately determininggrain yield. The results suggested that therewill be severely reduced grain yield if quinoa isgrown in the highland areas of Malawi duringthe winter season. The results also highlight theneed to continue evaluating a diverse numberof cultivars to select for genotypes adapted tospecific agroecological areas across seasons inMalawi.

The slow plant growth attributed to very lowtemperatures also affected the period to maturity.At the mid-altitude or warmer site, the plants had100% flowering by the end of 30 days, whereasat the highland or cooler site, the plants took51 days to attain 100% flowering. The differentquinoa varieties at the cooler site (Bembeke) tooklonger to reach maturity (102–119 days), whereasthe quinoa genotypes at the warmer site (Bunda)reached maturity earlier (90 days) correspondingto earliness to flowering.

Genotype performance

The performance of the different genotypesshowed variation in plant height at harvest, num-ber of days to harvest (maturity period), paniclelength, grain yield (kg/ha), and harvest index(HI) (Fig. 9.2). Promising high yielding varietiesand genotypes that yielded up to or about 3 tonsper hectare (t/ha) were “Brightest Brilliant”and “Cherry Vanilla” (both bred in Oregon,USA), “Multi-Hued” (bred in British Columbia,Canada), “Titicaca” (bred in Denmark), andQQ74 (from Chile). These promising quinoacultivars could be recommended for commercialproduction under the climatic conditions ofMalawi. The 3 t/ha quinoa grain yield was higheror comparable to the maize yields that small-scalefarmers get (2 t/ha) under rain-fed conditions inMalawi. Moreover, the quinoa yields in Malawidid not differ from those reported in other regionsof the world (Bertero et al. 2004). This impliesthat if farmers allocate a piece of land to quinoaproduction in place of maize, they are likely toharvest the same or higher quantity of quinoagrain, with the added benefit that quinoa is morenutritious than maize.

Quinoa studies in Kenya

Experimental sites and climatic conditions

Quinoa breeding studies in Kenya were firstconducted as part of a multienvironment trialthat involved a diverse set of 24 cultivars tested in14 sites under irrigation conditions from 1999 to2000 (Bertero et al. 2004; Oyoo et al. 2010). Theother 13 sites were in Peru, Brazil, Bolivia, andVietnam. In Kenya, the cultivars were plantedat the Kabete Field Station of the University ofNairobi to determine their adaptability and yieldperformance. The site is located at an altitudeof 1,820 masl, with temperatures ranging from13 to 23∘C, and a bimodal rainfall pattern witha mean annual rainfall of 970 mm. The soilshave an average pH of 5.0–6.8, classified ashumic nitisols (Siderius and Muchena 1977). Thequinoa accessions were evaluated under both thelong rainy seasons of 1999 (March–June) and theshort rainy seasons of 1999 to 2000.


0

3500

3000

2500

2000

1500

1000

500

Gra

in y

ield

(kg

/ha)

Bio-bio

Black-

seed

ed

Bright

est B

rillian

t Rain

bow

Chery

vanil

la

Ecuad

orian

Inca

Red

(Pas

anka

la)

Mult

i-Hue

dPun

o

QQ74

Red H

ead

Tritica

ca

Bunda

Bembeke

Genotype

Fig. 9.2 Yield (kg/ha) of 11 quinoa genotypes and cultivars grown under irrigation from July to October 2012 at the Bunda andBembeke sites in Malawi.

Plant growth and grain yield

The cultivars tested in Kenya showed varyingperformance in terms of plant growth and grainyield. The cultivars had shorter growth andmaturity periods at 65–98 days during the 1999season and 72–123 days in the 2000 growingseason (Oyoo et al. 2010) compared to the matu-rity periods ranging from 110 to 190 days whenquinoa is grown under Andean climatic condi-tions (Jacobsen and Stølen 1993; Bertero et al.2004). The earlier maturity periods of quinoa inKenya has been attributed to temperature effectsimposed by the lower altitude of 1,820 maslcompared to altitudes of over 3,000 masl in theAndean region where quinoa originated.

The overall grain yields of the cultivars eval-uated (1.583 to 2.097 t/ha) were comparableto the yield obtained in the Andean and otherregions of the world, and some cultivars even hadhigher yield. Some genotypes had yields up to4 t/ha in the Nairobi sites, presenting one of thehighest yields of quinoa obtained from quinoaintroduction studies around the world (Jacobsen2003). These results strongly suggest that quinoaproduction under Kenyan conditions is possible.However, these results cannot be generalized for

the entire country as plant growth and yield areinfluenced by several environmental factors.

Latitude is one of the factors that influ-ence crop introduction in a new environment.Latitude determines day length, which is criticalfor crops that are either long-day or short-daysensitive. The photoperiod sensitivity of quinoafor seed filling plays an important role in thecrop’s adjustment to new environments (Berteroet al. 2004), as it permits an accelerated seedfilling when photoperiod shortens. However, thischaracteristic limits the adaptation of quinoato higher latitudes. South Chilean cultivars areknown to have less sensitivity to photo period inseed filling. Thus, adaptation of quinoa to highlatitudes has been used as a selection index forthe lack of or for less sensitivity to photoperiod inseed filling.

Cultivar performance also varied significantlyfrom year to year even when grown during thesame cropping season, as influenced by variationin temperature and precipitation. The growthrange among cultivars has been reported to bealmost the same, but the actual length of thegrowth period (longer or shorter) and the speedof plant growth (faster or slower) are highly


dependent on the actual conditions during theseason – on how cold or warm or how wet or drythe season is.

Quinoa introduction studies in Africa needto include analysis of day length data (variationin sensitivity to photoperiod and its geneticbase) and how it affects performance of quinoacultivars of diverse origins. There is a needto screen or evaluate a large sample of quinoagermplasm that exists in genebanks for growthand yield stability across sites and seasons. TheKenyan studies showed a reduction in grainyields of quinoa for all genotypes evaluated in2000 compared to 1999. This yield reductionwas attributed to lower rainfall received duringthe latter season compared to the first. Otherparameters such as plant height, panicle length,and HI, which is strongly associated with biomassand grain yield, varied among cultivars tested andwere also significantly affected by the croppingseason. From the initial trials, three cultivarshave performed best in terms of yield and showpromise of commercial cultivation under Kenyanconditions – “Narino” (from Colombia, adaptedto the altiplano), CICA-127 (from Peru, adaptedto the valley areas), and ECU-420 (from Ecuador,adapted to the valley areas).

Harvest indices are useful in selecting geno-types with high grain production. The capacity ofcultivars for high grain production as measuredby HI varied from 0.24 to 0.47 and 0.15 to 0.49for the 1999 and 2000 seasons, respectively. SuchHI showed that the genotypes and cultivars testedwere as productive in Kenya as in the areas wherequinoa is traditionally grown (Bertero et al. 2004;

Oyoo et al. 2010). However, genotypes with highHI did not necessarily have high grain yields perhectare (kg/ha). For instance, the lowest HI inthe 1999 season were recorded in the cultivars“Canchones” (0.24) and “Narino” (0.25). In the2000 season, the lowest HI were recorded in“Real” (0.15), “Narino” (0.17), and “Kamiri”(0.17). On the other hand, highest HI wererecorded in ILPA (0.47), RM-072 (0.41), andHUA (0.41) in 1999 and in EDK-4 (0.49) andBB-079 (0.48) in 2000 (Table 9.3). Therefore,when selecting varieties for commercial produc-tion, both HI and grain yield per unit area needto be considered. In Africa, where the fresh leavesof quinoa are considered as a delicious vegetable,both as salad and when cooked, cultivars with lowHI may be selected for both leafy vegetable andgrain production, whereas those with high HI canbe selected for grain production only (Rojas et al.2000).

International quinoa trials comprising 14sites (Kenya included) across three conti-nents investigated the implication of genotype(G)× environment (E) interaction for geneticimprovement of grain yield and grain size in lowaltitude areas. The studies focused on examiningthe relative size of components of variance forG and G×E interaction for grain yield, time tophysiological maturity, above-ground biomass,HI, and grain size to group quinoa cultivarsaccording their relative responses to testingenvironments (Bertero et al. 2004). Results fromthese studies showed a strong across-cultivar andacross-environment variation for grain yield andits physiological determinants and grain yield.

Table 9.3 An extract of the mean performance of 24 cultivars of quinoa in Nairobi, Kenya, evaluated under the 1999 interna-tional quinoa trials.

Location LatitudeAltitude,masl

Meantemperature,

∘C

Meanphotoperiod,

hSowingmonth

Days tocropmaturity

Grainyield,gm−2

Grainsize,mm

Above-groundbiomass,

gm−2Harvestindex

Nairobi L 1∘15′S 1,819 18.9 12.4 October 77.1 209.7 2.1 698.7 0.31Nairobi S 1∘15′S 1,819 18.2 11.7 March 84.5 158.3 2.0 806.5 0.25

Source: Bertero et al. (2004).Note: Nairobi L and Nairobi S are crops grown during the long (L) and short (S) rainy seasons in that environment (Maurice 2001).Crop duration is expressed as days from sowing to maturity. Temperature and photoperiod data are means for that period.


Both yield determinants, that is, HI and biomassalso showed large G×E interaction to the Gcomponent of variance ratio. From this study, theinvestigators classified the sites into four groupsof environments based on grain yield and Kenyawas in the group of warmer and low-altitudeenvironments. The Kenya sites were also reportedto be in the shortest crop duration areas. In termsof cultivar performance, it was reported that allthe valley type of cultivars showed their bestperformance in the valley sites, that is, Kenyasites, above the mean yields in the Atiplano sitesand below mean yields in other environments.These results suggest that these cultivars arebetter adapted to the warmer and low altitudeareas and can thus be adaptable in most of thetropics in Africa.

Pests and diseases

The varieties tested in Malawi did not have seri-ous infestation of pests and diseases. Insect pestsobserved during the trials were sucking insectssuch as aphids and shield or stinkbugs, but atlevels that did not warrant spraying of chemicalsto control them. The aphids seemed to be moreprevalent under dry weather as is the case in othercrops, though the infestation was light and did notseem to attract new waves of infesting aphids. Itmay be too early to conclude that quinoa does nothave serious pests and diseases under Malawianconditions until adaptation studies have beenconducted over several agroecological zones andseasons. Future trials need to include studies onquinoa pests and diseases to substantiate theseinitial observations.

CHALLENGES AND CONSIDERATIONS FORFUTURE RESEARCH

Plant lodging

Both irrigated and the rain-fed experimentsunder Malawi conditions showed that most ofthe quinoa varieties tested are susceptible tolodging, resulting to grain yield losses. Africanclimates are characterized by the occurrence of

heavy rain storms that may make the lodgingworse. Therefore, selecting and breeding forlodging-resistant varieties should be one of thegoals of quinoa breeding in Africa.

Acceptability

Acceptability of quinoa into African diets is a keyfactor for the successful introduction of the crop.Maize has been the staple food of Malawiansfor centuries. They do not consider that theyhave had a meal until maize-based food is eaten;other crop-based food products are consideredmerely as snacks. Such an attitude is reflectedeven at the national level, where the country isconsidered to have a food shortage whenevermaize harvests are lean, even if other food cropsare available. It is only in recent times that theurban populations are changing their eatinghabits and have begun to accept potato, rice, andwheat-based food products in their main meals.Malawians will likely have an attitude to quinoasimilar to their attitudes toward other food crops.Hence, in conjunction with quinoa breeding andadaptability studies, there should be studies inthe acceptability and incorporation of quinoain the Malawian and African diet. Recipes andquinoa-based products should be developed topromote quinoa consumption in Africa.

The majority of African farmers are small-scalefarmers who consider maize as the main foodcrop and allocate most or all of their resources ingrowing maize. The farmers’ priority is to plantmaize when the first rains come, as is the casefor tobacco in regions where it is grown as themain cash crop. Under rain-fed cropping con-ditions, maize and other cash crops are plantedfirst, followed by other important crops such asgroundnut, soybean, and millet. Crops with lessmarket value are planted last. However, withoutthe application of inorganic fertilizers, cropsplanted late in the season usually do not have avigorous take off compared to crops planted earlywith the first rains. In order to apply inorganicfertilizers to late-planted crops, farmers have tobe convinced that the new crop has a potential ofearning them income as well as being valuable intheir diets.


Agronomic practices

The farming systems of Africa are dominated bysmall-scale farms characterized by land holdingsof less than 2 ha, almost no mechanization, andwith few input resources (Jayne et al. 2003).Successful promotion of quinoa as a new crop willneed technologies adapted to small-scale farmingconditions. For instance, most farm operationsare manually done and sowing of quinoa seed atvery close plant spacing of 10 cm would be timeconsuming. Farmers might opt to use the broad-cast sowing method to save time, but this sowingmethod is impractical as quinoa has extremelysmall seeds. Investigations on optimal seed ratesneed to be conducted and recommended tofarmers. Application of fertilizers in cereal cropsis recommended to boost productivity, but mostsmall-scale farmers can hardly afford inorganicfertilizers. Most of the inorganic fertilizers thatthey do manage to obtain are reserved for theirstaple crops such as maize. Alternative methodsof improving soil fertility for quinoa production,such as application of animal manure or greenmanure, need to be investigated.

Rain-fed versus irrigated croppingsystems

Crop production in small-scale farms is mostlyunder rain-fed conditions. In regions of Africawhere rains are limited to one season and only fora few months, quinoa may need to be producedunder irrigated conditions. Results from on-goingexperiments suggest that irrigated quinoa grownshortly after the end of the rainy season gives a bet-ter grain yield than under the rain-fed conditionsin Malawi. However, irrigation as practiced bymost small-scale farmers is with the use of water-ing cans. Irrigation technologies that would con-serve soil moisture (such as mulching) would makequinoa production more feasible and affordable.

CONCLUSION

Results of initial experiments in Malawi andKenya have shown that quinoa can grow well

under varying agroecological zones, from warmerto cooler areas. However, more genotypes fromthe Andean region and those that have been bredelsewhere need to be evaluated under the variousagroecological zones and seasons of Africa. Suchevaluations will allow selection of more cultivarsadapted to specific ecological zones and croppingseasons that prevail in the region. Studies haveshown that cultivars from South America andthose bred in North America can give the sameor higher grain yields (3–4 t/ha) when grown inMalawi and Kenya, comparable to the yields of thesame cultivars when grown in areas where quinoais traditionally grown. Such varieties can beadopted in Africa and promoted to alleviate foodinsecurity common in many African countries.

To facilitate the introduction and adoption ofquinoa in Africa, there should be more researchon cropping technologies relevant to small-scalefarms that characterize a large section of Africanagriculture. Aside from agronomic factors, socioe-conomic factors that affect the adoption of newcrops also need to be considered. For instance, theacceptability of a new grain crop can be influencedby grain color, taste, or the ease of processing ofthe grain for local dishes, even though the cropmay be high yielding and nutritious. Acceptabil-ity of quinoa into the African diet, and the fac-tors that influence the adoption of change, shouldalso be studied. Plant breeders and agronomistsshould work hand-in-hand with farmers, exten-sion agents, nutrition experts, government agen-cies, and relevant stakeholders to introduce quinoato Africa, taking into account not only the agro-nomic challenges but also the social, market, andpolitical challenges of introducing a new crop intothe African landscape and psyche.

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Wilson HD. 1990. Quinoa and relatives (Chenopodium sect.chenopodium subsect. cellulata) Econ Bot 44Supplement3:92–110.

http://www.fao.org/fileadmin/templates/aiq2013/res/en/

http://www.metmalawi.com/

http://www.un-ngls.org/IMG/pdf/IYQ.pdf

Chapter 10

Quinoa Cultivation for Temperate NorthAmerica: Considerations and Areas for

Investigation

Adam J. Peterson and Kevin M. MurphyDepartment of Crop and Soil Sciences, Washington State University, Pullman, WA, USA

INTRODUCTION

Quinoa has a relatively recent history of commer-cial cultivation in North America. The first majorefforts at commercial cultivation were begun in1983 by a partnership between Colorado StateUniversity and Sierra Blanca Associates, focusingon growing quinoa in high altitude locations ofColorado (Johnson 1990). In addition, privateefforts to test and grow quinoa varieties inNorth America were begun by John Marcille innorthern Washington state and Emigdio Ballón innorthern New Mexico (Ballón 1990; Wilson andManhart 1993). Quinoa production expandedoutside Colorado to Wyoming and Northern NewMexico (Ward 1994). By the late 1980s, efforts togrow quinoa in Canada were underway (NationalResearch Council 1989; Tewari and Boyetchko1990; Small 1999).

Cultivation of quinoa in North America iscurrently centered in the San Luis Valley of Col-orado and in the Canadian Prairies through theNorthern Quinoa Corporation, with headquartersin Saskatoon, Saskatchewan. Despite efforts tocultivate quinoa in North America and other partsof the world, the majority of worldwide quinoa


cultivation is still concentrated in South America.In recent years, the large gap between the supplyof quinoa and the growing demand for it has ledto high prices and mounting concern about thesocial and environmental impacts of quinoa pro-duction in the major quinoa-producing countries(Jacobsen 2011; Romero and Shahriari 2011).These concerns, along with the desire in manyareas for regionally sourced food and interest inquinoa as a crop for improving food security, haveled to efforts to adapt and grow quinoa in variousparts of the world (Jacobsen 2003).

TOLERANCE TO ABIOTIC STRESSES

Heat tolerance

Quinoa production in North America has so farbeen limited to regions with cool summers, wheremaximum temperatures do not exceed 35∘C(95∘F). Initial trials in Colorado showed thatquinoa was unsuccessful at elevations lower than2,100 m (7,000 ft) due to pollen sterility and plantdormancy caused by high temperatures (Johnsonand Croissant 1985; Johnson 1990).

173


Multiple reports exist indicating that high tem-peratures pose a constraint to quinoa productionin North America, namely in Minnesota (Oelkeet al. 1992), New York (Dyck 2012), Virginia(Bhardwaj et al. 1996), and Alberta (AAFRD2005). Oelke et al. (1992) suggested that heatsusceptibility would limit the expansion of quinoacultivation to coastal areas in central California,high altitude locations in central and northernWashington state, and parts of the Canadianprairies. High temperatures have been noted ashaving a detrimental effect on yield and seedfilling in locations outside of North Americasuch as Morocco (Benlhabib et al. 2004), Chile(Fuentes and Bhargava 2011), Greece (Iliadiset al. 2001), and Italy (Pulvento et al. 2010).

Chronic heat stress can also affect quinoa, incontrast to the acute heat stress events that canoften occur under field conditions. In an earlystudy of a variety of unspecified origin, Aguilar(1968) found that quinoa subjected to a constanttemperature of 32∘C (90∘F) had greatly reducedheight, biomass, and seed yield compared tomore mild temperature treatments. Overalldevelopment time was shortened, and red stemcolor present in the tested variety was enhancedat hotter temperatures.

Current work at Washington State University(WSU) has found maximum summer tempera-tures to be a major limiting factor for successfulseed set in quinoa. While temperatures did notexceed 35∘C (95∘F) during anthesis in a 2011 fieldexperiment, high temperatures during the seedfill stage may have caused significant reductions inyield. Many of the inflorescences lacked seeds orcontained empty seeds (Peterson 2013). Despitethe large reduction in yield in 2011, several vari-eties, namely Colorado 407D, QQ74, and Kaslaea,exhibited greater heat tolerance than others.

Variation in adaptation to hot, dry conditionshas also been observed among Chilean highlandvarieties grown in a field experiment in AtacamaDesert of northern Chile (Fuentes and Bhargava2011). The effect of heat stress on quinoa wasreviewed in detail by Bonifacio (1995), whonoted that heat stress could cause reabsorptionof the endosperm, a phenomenon recognizedby Bolivian farmers as “phuna” or “puna.” As

the endosperm of the quinoa seed is of minimalsize and the perisperm and embryo are the twolargest components of the seed (Prego et al.1998), this reabsorption likely extends to moreseed components than the endosperm. Bonifacioalso observed that high temperatures inhibitedanther dehiscence in outdoor plantings in Provo,Utah in 1993 and found varietal differences inheat tolerance.

Irrigation may be an important tool in quinoacultivation by ameliorating the effects of heatstress. Preliminary results from a WSU irriga-tion trial showed that irrigation substantiallyincreased yields under heat stressed growingconditions in eastern Washington state (HannahWalters, personal communication, 2013). Furtherinvestigation into the role of heat stress, wateravailability, and the interaction of these factors inquinoa is warranted.

As most areas of temperate North Americahave summer temperatures in excess of quinoa’sthreshold of tolerance (NCDC 2011), the devel-opment of heat tolerant varieties could greatlyexpand the area suitable for quinoa productionand increase harvest security in areas with damag-ing heat waves. Despite the heat susceptibility ofquinoa, closely related Chenopodium spp. inhabitparts of North America that experience intensesummer heat (Jellen et al. 2011). In addition,archeological evidence indicates the existence ofa domesticated chenopod pseudograin, analogousto quinoa, in the prehistoric Eastern NorthAmerican agricultural complex (Smith 1985).This implies the possibility of developing aheat-tolerant chenopod pseudocereal for NorthAmerica outside of high altitude or cool maritimelocations. If the existing variation for heat tol-erance within quinoa proves insufficient, relatedChenopodium spp. such as C. berlandieri and C.bushianum to which quinoa can hybridize mayprovide a promising source for introgression ofgenes for heat tolerance.

Drought tolerance

Quinoa is considered to have remarkable droughttolerance. It has been reported to grow with aslittle as 200 mm (8 in) annual precipitation in

Quinoa Cultivation for Temperate North America: Considerations and Areas for Investigation 175

pure sand (Aguilar and Jacobsen 2003). Yieldsexceeding 1,000 kg/ha (890 lbs/acre) have beenreported with as little as 50 mm (2 in) irrigation inthe Atacama Desert of northern Chile. However,yields are much improved in arid regions underirrigation (Martínez et al. 2009). Initial researchin Colorado found that quinoa had highest yieldswith 208 mm (8.2 in) of combined irrigation andrainfall on a sandy loam soil (Flynn 1990). Laterrecommendations to growers in the San LuisValley were 25–38 cm (10–15 in) of combinedirrigation and rainfall (Johnson and Croissant1985). The addition of organic matter has beenshown to be effective in increasing quinoa yieldunder arid conditions (Martínez et al. 2009).

The effect of drought on yield varies depend-ing on the stage of plant development. Geertset al. (2008) found that water use efficiencyimproved when there was adequate water supplyduring the initial germination phase and duringflowering and seed fill, even though droughtoccurred during vegetative growth. In contrast,there were severe negative effects on yield whendrought occurred during flowering and duringseed fill stages. Jensen et al. (2000) also foundyield decreases when drought was simulatedduring the flowering stage and during the seedfill stage. When drought was instead simulatedduring the early vegetative phase, yield increasedcompared to the control.

Sensitivity to drought in later developmentalstages may be responsible for the reported lackof seed set in cool growing locations. Quinoatrials in Sweden showed a total failure of seed setduring a year with a near absence of precipitationin July (Ohlsson 2000). This contrasts withfavorable performance the previous year, whenrainfall was more equally distributed (Ohlssonand Dahlstedt 1999). Some Chilean lowlandvarieties grown in cool locations at sites in mar-itime western Washington state failed to set seedin 2013 (unpublished data). As these sites arecharacterized by a mild oceanic Mediterraneanclimate with seasonal summer drought that wouldcoincide with later growth stages of quinoa, theimpact of drought on seed set deserves furtherinvestigation, as well as the variability for seed setamong Chilean lowland varieties.

In contrast, some reports indicate greaterdrought tolerance in later growth stages. Jacobsenand Stølen (1993) noted that in Denmark, thegreatest impact from drought occurs during thevegetative stage. Likewise, Darwinkel and Stølen(1997) reported greater drought tolerance inlater growth stages. Razzaghi et al. (2012) foundthat yield did not significantly decrease whensimulated drought was applied during the seedfilling stage.

Cold tolerance

Cold temperatures are an important limiting fac-tor for quinoa cultivation in many areas of NorthAmerica. The occurrence of frosts places limits onthe planting date of spring planted quinoa, whichis of particular importance where the long timeto maturity for quinoa is an issue. At high alti-tude locations, cooler temperatures favor quinoacultivation, although the frost-free growing periodis shorter. This limits cultivation to the earliestmaturing varieties and can place plants in the fieldat risk to early frosts during sensitive growth peri-ods (Johnson and Croissant 1985).

One untested possibility is the cultivationof quinoa as a winter crop in extreme southernlocations of the United States. Although heatwould not be an issue over the relatively coolwinters, the potential occurrence of damagingfrosts in many of these locations would likely limitany cultivation of quinoa to locations that do notexperience temperatures lower than the reportedlimits for quinoa, such as areas of southernFlorida that experience a tropical climate.

There are varying reports on the frost toler-ance of quinoa under field conditions. Risi andGalwey (1984) reviewed contradictory reportsregarding the frost tolerance of quinoa in SouthAmerica, with some sources indicating little or nofrost resistance and others reporting high frostresistance.

In a study by Jacobsen et al. (2007), frost toler-ance measured under controlled conditions variedbetween an Altiplano and a Valley-type variety.In addition, frost tolerance was found to correlatewith the ability of quinoa to produce more solublesugars and, to a lesser extent, proline, with


exposure to cooler temperatures (Jacobsen et al.2007). Growth stage also affects tolerance to frost.Exposure to frost after the initiation of floweringproved far more damaging than exposure duringearlier growth stages. A 66% reduction in yieldwas seen when plants in anthesis were exposed to−4∘C (25∘F), whereas seedlings at the two-leafgrowth stage exposed to the same conditions onlyhad a 9% reduction in yield. Humidity also inter-acted with the impact of frost on quinoa, withdrier conditions resulting in lower percentage ofplant survival (Jacobsen et al. 2005).

There are a few accounts of frost tolerancein Chilean lowland varieties. In England, Risiand Galwey (1984) found that several Chileanvarieties tolerated several frosts in spring, oneof which reached −5∘C (23∘F). In Colorado,reports indicate that quinoa could withstand lightfrosts of −1 to 0∘C (30–32∘F). In accordancewith Jacobsen’s findings, a heavy frost of −4.4∘C(24∘F) during flowering caused losses exceeding70% (Johnson and Croissant 1985). Oelke et al.(1992) suggested that temperatures below −2∘C(28∘F) during flowering would cause significantlosses. However, once seeds are in the softdough stage, frost resistance increases and plantswere reported to withstand temperatures downto −7∘C (20∘F). Darwinkel and Stølen (1997)reported varietal differences in frost tolerance andnoted −3∘C (27∘F) as the threshold for quinoa.

Salinity tolerance

Soil salinity is a significant agricultural problemfor large parts of temperate North America. In theUnited States, there are 2.2 million hectare (Mha)(5.4 million acres (Mac)) of saline agriculturalland, with a further 30.8 Mha (76.1 Mac) of agri-cultural land under threat of salinization (USDA2011). The majority of these saline-affected soilsare confined to arid and semi-arid regions ofthe West (USDA 1989). In Canada, salinity is asignificant problem in the Prairie provinces ofAlberta, Saskatchewan, and Manitoba, affectingan estimated 2.19 Mha (5.4 Mac) (ARD 2004).

Quinoa is generally recognized as one of themost saline-tolerant crops known (Jacobsen 2007).In its native range, quinoa is cultivated in areas

with highly saline soils. For example, varieties ofthe Salares ecotype are grown around salt flats inSouthern Bolivia (Risi and Galwey 1984).

Quinoa has exhibited unparalleled levels ofsalinity tolerance under controlled conditions.Koyro and Eisa (2007) and Hariadi et al. (2011)demonstrated the ability of quinoa to survive andproduce seed under 500 mM NaCl, an equiva-lent concentration to that of seawater. Jacobsenet al. (2003) found that seeds of the variety“Kanckolla” were able to germinate at 57 mS/cm,a level exceeding that of seawater.

The salt tolerance of quinoa has been demon-strated to vary significantly within and betweenecotypes. In an analysis of Peruvian quinoagermplasm, Gómez-Pando et al. (2010) foundsignificant variation for saline tolerance at boththe seedling and the adult stages. Tolerance at theseedling stage was not necessarily correlated withtolerance during the adult stage (Jacobsen et al.1999b).

Adolf et al. (2012) investigated the response ofDanish, Bolivian, and Peruvian varieties to salin-ity and noted a considerable range in physiologicalresponses and relative salinity tolerance. Despitethe complex variation exhibited in the study, Dan-ish varieties of Chilean lowland background wereof average or lesser salinity tolerance as measuredby relative declines in height and biomass, whereasthe “Real”-type quinoa varieties from SouthernBolivia rated more tolerant for these measures.

Investigation of salinity tolerance withinChilean lowland germplasm will prove importantin the use of quinoa as a salt tolerant crop. Thesevarieties are most adapted to the conditionsfound in areas of North America affected bysoil salinity. Many salt-affected areas in westernNorth America experience high summer tem-peratures characteristic of a continental climate.Breeding varieties with greater heat tolerancewill be necessary as the susceptibility of quinoato heat precludes its cultivation in these areas.Chilean lowland varieties have the greatest heattolerance and characterizing their levels of salinitytolerance will be crucial in developing quinoa as asuccessful halophytic crop for these areas.

Two germination studies conducted withChilean germplasm provided evidence for a


significant geographical trend in salinity tol-erance (Delatorre-Herrera and Pinto 2009;Ruiz-Carrasco et al. 2011). Delatorre-Herreraand Pinto (2009) found higher tolerance among aChilean highland variety compared to a Chileanlowland variety, measured in terms of seedgermination, and related this to adaptationto the saline soils found in the highlands ofnorthern Chile. Ruiz-Carrasco et al. (2011)tested varieties within the range of the Chileanlowland ecotype, comparing varieties from centralChile with a variety from southern Chile. Theauthors found significant differences amongthese varieties in growth characteristics, prolineaccumulation, polyamine response, and expres-sion levels of sodium transporter genes CqSOS1and CqNHX1. These differences were generallyindicative of lower salinity tolerance in the quinoavariety from Southern Chile and were linked bythe authors to the gradient of decreasing exposureto salinity and increasing precipitation that runsnorth to south in Chile.

A recent study measured the salinity toleranceamong four quinoa varieties of Chilean lowlandorigin (Peterson 2013). All four varieties weresignificantly more tolerant to Na2SO4 than theywere to NaCl, as measured by yield decreasesat 32 dS/m relative to a nonsalt control. Yielddeclines for quinoa varieties ranged from 43.7%to 65.4% under 32 dS/m NaCl and from 10.8%to 51.9% under 32 dS/m Na2SO4. Of particularsignificance is that these differences generallyappeared to match the latitude of origin of thevarieties in Chile, in accordance to the findingsof previous studies. In terms of yield, the north-ernmost variety, UDEC-1, was generally mosttolerant and the southernmost variety, QQ065,was most susceptible to salinity (Peterson 2013).

Further investigation to confirm a geograph-ical gradient of saline tolerance among Chileanlowland accessions could prove invaluable inidentifying the most saline-tolerant Chilean low-land germplasm. In addition, given the increasingtemperatures that are also found at more north-ern and lower latitudes in Chile (Climatologia;Ruiz-Carrasco et al. 2011), greater heat tolerancemay be found in conjunction with greater salinitytolerance.

A field study performed in Southern Italyfound that the Danish quinoa variety “Titicaca”had no significant difference in yield whenirrigated with saline water of 22 dS/m, mixed toapproximate a 1 : 1 ratio of seawater to freshwater,compared to a fresh water control (Pulventoet al. 2012). In comparison, barley, considered asaline tolerant grain, has a salinity threshold of8 dS/m (Maas 1986). When quinoa was grownon a saline-sodic soil in Greece with an EC of6.5 dS/m, the seedlings had poor establishment,which the authors linked to high pH, high Na+,and poor soil physical characteristics due to soilsodicity. Varieties responded differently whengrown on a nonsaline soil, indicating varietaldifferences in tolerance. Overall, yield wassubstantially decreased, with the best performingvariety under saline-sodic conditions yielding1.27 t/ha (1,130 lbs/ac), whereas the bestperforming variety under nonsaline conditionsyielded 2.30 t/ha (2,050 lbs/ac) (Karyotis et al.2003). The added effects of sodicity to salinitylikely explain the large differences in yieldresponse in that experiment compared to thefindings by Pulvento et al. (2012). As soil crustingreduces quinoa emergence, the tendency of sodicsoils to form a crust may be an impediment to thepotential of quinoa to be grown on these soils.The larger effect of sodicity compared to salinityis supported by an early experiment by Torres(1955), which compared the response of quinoato saline, saline-sodic, and sodic soils. Sodicitywas found to have a more detrimental impacton quinoa biomass yield compared to salinity,though differences in sodicity tolerance were seenbetween the two varieties examined.

PRODUCTION ASPECTS

Variety selection

Quinoa is traditionally divided into five main eco-types: Valley, which is grown between 2,000 and4,000 m elevation from Central Peru northward;Altiplano, grown at 4,000 m elevation aroundLake Titicaca; Salar, grown at 4,000 m aroundsalt flats in southern Bolivia; Subtropical, from


the Yungas region of Bolivia; and Sea level, fromtemperate latitudes in southern Chile (Tapia et al.1980 cited in Risi and Galwey 1984). The Sealevel ecotype, also referred to as Chilean lowlandecotype, is recognized as the best adapted to tem-perate latitudes and high summer temperatures.After initial trials, Chilean varieties were chosento form the basis of breeding programs in Europeand in Colorado (Johnson 1990; Jacobsen 1999).In initial trials, Chilean lowland varieties werethe best adapted to cultivation in Washingtonstate (unpublished data), and only Chilean andsouthern Bolivian varieties set seed in Colorado(Johnson 1990). Bertero (2003) concluded thatChilean lowland and Altiplano varieties, charac-terized by low photoperiod sensitivity and a shortbasic vegetative period, were most suited for cool,temperate latitudes.

However, there are reports of non-Chileanvarieties producing good yields at high latitudelocations in Europe. A wide range of Peruvian andBolivian varieties produced seed in a field trial inFinland, at two locations above 60∘N (Carmen1984). Likewise, Valley and Altiplano varietiesproduced significant yields in England, as didBolivian and Peruvian varieties in Denmark.However, non-Chilean varieties generally neededlonger times to reach maturity (Risi and Galwey1991b; Jacobsen and Stølen 1993; Jacobsen 1997).Christiansen et al. (2010) found that an 18-h-longphotoperiod induced a “stay green” reaction in“Real,” a Bolivian variety.

Overall, non-Chilean varieties failed to set seedin field trials in Washington state (unpublisheddata). Bertero (2003) also noted failure of thesevarieties to reach maturity in Argentina.

In an experiment using “Kanckolla,” anAltiplano variety, long daylength and high tem-peratures were found to decrease the amount ofseed filling. The two factors, taken separately, hadsmall but significant effects. However, when 16-hdaylength was combined with 28∘C (82∘F), seedsize decreased by 73% (Bertero et al. 1999). Thisrelatively low threshold for high temperatures,combined with the negative influence of longdaylength, suggests that most non-Chilean vari-eties likely have negligible potential for cultivationin temperate regions of North America.

Fertilization

Fertilizer recommendations for quinoa in Col-orado were 135 kg N/ha (120 lbs N/acre), basedon results from early trials (Johnson and Crois-sant 1985). However, after more extensive fieldresearch, the recommendation was increased to170–200 kg N/ha (150–180 lbs N/acre). Higherlevels of nitrogen were found to have adverseeffects, leading to lodging and delayed maturity(Oelke et al. 1992). Under Danish conditions,yield was generally highest at 160 kg N/ha(143 lbs N/ac) compared to the lower levelsof 120 kg N/ha (107 lbs N/ac), 80 kg N/ha(71 lbs N/ac), and 40 kg N/ha (36 lbs N/ac).However, increase in yield response under higherfertilization levels was minimal. At 40 kg N/ha,yield was only 24.1% lower than at 160 kg N/ha(Jacobsen et al. 1994). Trials in Denmark andthe Netherlands showed differences in nitrogenresponse across locations and years, althoughgeneral recommendations of 100–150 kg N/ha(89–134 lbs N/ha) were given. A fertilizationlevel of 50 kg N/ha resulted in poor yields,whereas nitrogen in excess of 150 kg N/ha wasfound to have meager benefits (Darwinkel andStølen 1997).

A study performed by Schulte auf’m Erleyet al. (2005) in southern Germany found quinoaquite responsive to increased nitrogen fer-tilization. Yields at no fertilization produced1,790 kg/ha (1,597 lbs/ac), whereas 120 kg N/ha(107 lbs N/ac) caused yields to almost double to3,495 kg/ha (3,118 lbs/ac). Nitrogen utilizationefficiency (g grain/g Nplant) did not change underincreasing fertilization, though a significantdifference was seen between the two varietiestested (Schulte auf’m Erley et al. 2005).

In another experiment, conducted undergreenhouse conditions, nitrogen utilizationefficiency showed significant decreases underincreasing N, in contrast to the results observedby Schulte auf’m Erley et al. (2005). This dif-ference is notable in that one of the varietiestested, “Faro,” was common to both experiments,indicating different nitrogen dynamics due toenvironment. Again, there was a significantdifference between varieties, but this time in


nitrogen uptake efficiency (g Nplant/g Nmineral)(Thanapornpoonpong 2004).

The large variation in nitrogen dynam-ics observed at different locations, as well assignificant varietal differences, pose severalchallenges and opportunities for breeding quinoafor increased nitrogen use efficiency. Quinoahas historically thrived in marginal areas, andvarieties that are adapted to low soil nitrogenmight prove valuable for low-input agriculture.Traditional cultivation of quinoa on the PeruvianAltiplano generally involves no fertilization. Incrop rotations, quinoa is grown after potatoesand scavenges for remaining nutrients in the soil(Aguilar and Jacobsen 2003).

As organic quinoa makes up the bulk of quinoademand, with organic quinoa constituting 69%of the total US quinoa imports in 2013 (Arcode Nuñez 2014), investigating the response ofquinoa varieties to fertilization and managementunder organic conditions is crucial. Scant dataexists in this area of study; however, Bilaliset al. (2012) reported yield increases of 6% withcompost application and of 10% with cow manureapplication compared to a nonfertilized control.

Seed composition is influenced by fertilization.In the aforementioned study by Bilalis et al.(2012), saponin content increased under organicfertilization as compared to a nonfertilized con-trol. Johnson and Ward (1993) found that proteincontent was responsive to nitrogen applications,increasing by 0.1% per kg of ammonium nitrate.

Soil texture is reported to have a major impacton nitrogen uptake and nitrogen use efficiency.In a lysimeter experiment where 120 kg N/ha(107 lbs N/ac) was applied, nitrogen uptakewas 134 kg N/ha (120 lbs N/ac) under a sandyclay loam but only 77 kg N/ha (69 lbs N/ac)under a sandy soil, leading to differing yields of3,300 kg/ha (2,900 lbs N/ac) and 2,300 kg/ha(2,100 lbs N/ac), respectively (Razzaghi et al.2012).

In most studies, nitrogen was applied in asingle application, although several studies reportsplitting applications between planting and alater stage (Aguilar and Jacobsen 2003; Schulteauf’m Erley et al. 2005; Pulvento et al. 2010).Darwinkel and Stølen (1997) suggest splitting

fertilizer applications exceeding 150 kg N/ha(134 lbs N/ac) to prevent excessive salt exposure.However, there is no published research on theeffects of split fertilizer applications on nitrogenuptake in quinoa.

There are contradictory reports on theresponse of quinoa to phosphorus fertilization.In Chile, yield increased with high levels ofphosphorus fertilization (100 and 200 kg N/ha,89 and 178 lbs N/ac) when accompanied bynitrogen fertilization (Delatorre-Herrera 2003).Recommendations from South America indicatethat quinoa responds well to 80 kg N/ha (71 lbsN/ac) and 80 kg P/ha (71 lbs P/ac) (Mujica 1977cited in Aguilar and Jacobsen 2003). However,Gandarillas (1982 cited in Johnson and Ward1993) found no yield response to phosphorus orpotassium application. In Colorado, phosphorusapplications of 34 kg P2O5/ha (30 lbs P2O5/acre)did not affect yield (Oelke et al. 1992). Darwinkeland Stølen (1997) reported requirements of 70 kgP2O5/ha (62 lbs P2O5/ac) for quinoa before seedfilling and noted that existing levels of phosphorusin many agricultural soils are likely sufficient.They also note a fairly large requirement forpotassium, with uptake of 500 kg K2O/ha(446 lbs K2O/ac) and recommend applicationof 100–200 kg K/ha (89–178 lbs K/ac). Dataon the micronutrient requirements of quinoais almost nonexistent. However, Darwinkel andStølen (1997) report that manganese is a criticalmicronutrient for quinoa.

Planting/spacing

Row spacing for quinoa varies widely. In SouthAmerica, a variety of planting techniques are used.When quinoa is planted in rows, spacing rangesfrom 0.4 m (16 in) and 0.8 m (31 in). Wide rangesof optimal sowing density have also been reported(Tapia et al. 1980 cited in Risi and Galwey 1984).

Recommendations for Colorado were basedon a plant density of 320,000 plants/ha(130,000 plants/acre) and a sowing densityof 0.6–0.8 kg/ha (0.5 to 0.75 lbs/acre). Therewas no set row spacing recommended, althoughspacing greater than 36 cm (14 in) was beneficial(Johnson and Croissant 1985). In experiments in


England, highest yields were seen for the Chileanvariety ‘Baer’ under the closest row spacingtested, at 20 cm (8 in) spacing seeded at 20 kgseed/ha (18 lbs seed/ac). Increasing plant densitydecreased the amount of branching on plants andalso resulted in earlier maturity in the field (Risiand Galwey 1991a).

Jacobsen et al. (1994) investigated row spacingsof 50, 25, and 12.5 cm and found no significantdifferences in yield between them. The widestspacing of 50 cm (20 in) was combined withmechanical hoeing to control weeds, and plantsunder this spacing appeared healthiest, whereasplants at the 25 cm (10 in) and 12.5 cm (5 in)row spacings were best able to crowd out weeds.Moreover, optimal plant density was calculatedto be 327 plants/m2 (1,320,000 plants/acre) witha standard deviation of 220 plants/m2 (890,000plants/acre), leading the authors to conclude thatyield could remain stable over a wide range ofplant densities. On the basis of later experimentsin Denmark and the Netherlands, Darwinkel andStølen (1997) confirmed the stability of yieldacross a wide range of row spacings, rangingfrom 12.5 cm (5 in) to 75 cm (30 in), and plantdensities ranging from 30 to 250 plants/m2 (25 to210 plants/yd). On the basis of harvesting con-siderations and weed competition, a seeding rateof 6 kg/ha (5.4 lbs/ac) with target plant densitiesof 100 to 150 plants/m (85 to 125 plants/yd) wasrecommended for quinoa cultivation in northernEurope.

The large range of plant densities, row spacing,and seeding rates found in these studies indicatethe large influence that location and weed pres-sure, as well as variety characteristics, have onyield. Given the wide range of conditions foundacross temperate North America, further researchwill be necessary to determine the proper spacingand seeding rates for new locations.

Planting depth for quinoa is also variabledepending on soil type and conditions. Oelkeet al. (1992) recommended planting at a depthof 1.3 to 2.5 cm (0.5 to 1 in) in Colorado. Exces-sively deep sowings were noted to lead to pooremergence due to waterlogging, whereas plantingdepths that were too shallow left seeds vulnerableto soil drying. In Europe, high germination

required adequate contact of seeds with soil withthe proper moisture level (Darwinkel and Stølen1997). Aufhammer et al. (1994) found that soilcrusting had a highly damaging effect on seedlingemergence. They stressed the importance of alight-textured seedbed for successful germina-tion. Quinoa germination rates were reported todrop steeply at depths greater than 2 cm (0.8 in).At shallower depths, greater emergence wasobserved in a sandy soil than a loamy clay soil.

Reports from Europe confirm the need for afine-textured and even seedbed and likewise indi-cate that heavy clay soils can cause problems withearly establishment of the root system. Plantingdepths of 1 to 2 cm (0.4 to 0.8 in) were recom-mended (Darwinkel and Stølen 1997).

Temperature has a significant effect on thepercentage and rate of germination but there arevarying reports on the optimum temperatureneeded for successful germination. In Denmark,seed is usually planted when the soil temperatureis 7–8∘C (45–46∘F). An experiment with aDanish variety of Chilean lowland origin showedmaximum germination between 15 and 20∘C(59–68∘F). However, high rates of germinationwere seen for a wide range of temperatures,including 8∘C (46∘F), the lowest temperaturetested (Jacobsen and Bach 1998). Recommendedsoil temperatures for planting in Colorado were7–10∘C (45–50∘F) (Johnson and Croissant1985). For England, reports indicated that soiltemperatures of 5–8∘C (41–46∘F) were suitablefor planting quinoa in the spring (Galwey 1989).Darwinkel and Stølen (1997) recommended soiltemperatures exceeding 10∘C (50∘F) for plantingand note that lower temperatures inhibit propergermination and establishment.

In a germination experiment with the Danishvariety “Olav,” temperatures of 6∘C (43∘F)inhibited germination, resulting in only 25% ofthe germination found at 20∘C (68∘F) (Jacobsenet al. 1999a). The study also showed that the dateof harvest was a significant factor for germinationat low temperatures. For seed that had beenharvested early, there was 0% germination. Thegermination percentage increased to a maximumof 45% with a later time of harvest.


Christiansen et al. (1999) investigated fivePeruvian quinoa lines for their ability togerminate at low temperatures. In contrast to theresults reported by Jacobsen, high germinationwas seen at temperatures as low as 2∘C (36∘F),indicating that variation exists in quinoa forminimum germination temperature.

For some areas in North America, sufficientlyhigh soil temperatures may be the determin-ing factor for planting date. The temperaturegermination study by Jacobsen et al. (1999a)investigated only one variety of Chilean lowlandorigin. Further screening of a wide range ofChilean lowland varieties for their ability togerminate at lower temperatures could identifyvarieties suited for earlier planting. If this traitis not identified in the germplasm screened, itcould potentially be brought in from non-Chileanvarieties such as those identified by Christiansenet al. (1999). Earlier planting could mean earlierestablishment, enhanced competitiveness withweeds, and earlier harvest time. Germinationunder low temperatures would also need to becombined with seedling vigor and proper estab-lishment under such conditions. For instance,early seeding under northwestern Europeanconditions showed not only poor germinationbut also poor emergence and, subsequently, poorgrowth (Darwinkel and Stølen 1997).

Maturity and harvesting

Days-to-maturity is a critical yet highly variablefactor for the successful cultivation of quinoa. InColorado, days to maturity range from 90 to 125days (Johnson and Croissant 1985), whereas daysto maturity have ranged from 100 to 130 days fordifferent varieties grown in Eastern Washington.Maturity has been observed to vary significantlydepending on environmental variation in the field(unpublished data). In Greece, maturation timewas shown to vary from 110 to 116 days comparedto the 110 to 180 days reported for Denmark(Jacobsen 2003). Within the same location,maturity time has been shown to vary widelyfrom year to year (Gesinksi 2000; Jacobsen 1998).The wide range of maturity time by locationand environmental conditions emphasizes the

importance of testing quinoa in new locationsover multiple years.

Quinoa can be mechanically harvested throughthe use of a combine. However, adjustments areneeded for the small seed size and large stems. InColorado, quinoa harvest recommendations aresimilar to sorghum. Combining does not resultin a totally clean product and further processingis necessary after combining. Recommendationsinclude the use of a fanning mill and gravityseparator (Oelke et al. 1992). Darwinkel andStølen (1997) also confirm the necessity ofcleaning after combining, although they note thatthe percentage of chaff can be kept under 5%if done under optimum field conditions with aproperly adjusted combine.

Jacobsen et al. (1994) compared the efficacyof swathing compared to combining and foundno significant differences in yield between thetwo methods when performed at their respectiveoptimal harvest time. Swathing did allow forharvest earlier in the season than combining,when the plants were still somewhat green. Thiscould be advantageous in situations where earlyharvest is important, particularly during the stagewhen mature seed has formed but plants have notfully senesced and cannot be combined. This hasbeen an issue for quinoa grown in western Oregonand western Washington state, where early onsetof seasonal rains in late summer and early autumncan cause preharvest sprouting.

In Colorado, steady yields of 1,340 kg/ha(1,200 lbs/acre) were reported over a 3-yearperiod (Johnson and Croissant 1990). Withproper management, however, this can increaseto over 2,000 kg/ha (1,800 lbs/acre) (Oelkeet al. 1992). In Saskatchewan, yield is reportedto range from 840 to 1,400 kg/ha (750 to1,250 lbs/acre), although yields exceeding2,200 kg/ha (2,000 lbs/acre) have been reported.On the other hand, complete losses can also occur(AAFRD 2005).

Quinoa yields reported in Europe exceedthose of Colorado. Yields in Denmark typi-cally range from 2,000 to 3,000 kg/ha (1,800to 2,700 lbs/ac) (Jacobsen et al. 2010). Undertwo field experiments in England, the variety“Baer” yielded 5,140 kg/ha (4,590 lbs/ac) (Risi


and Galwey 1991b). In Southern Italy, thevariety “Regalona Baer” yielded 3,420 kg/ha(3,050 lbs/ac) and 3,000 kg/ha (2,680 lbs/ac) over2 years (Pulvento et al. 2010). In Chile, “Baer”is reported to produce yields of 3,000 kg/ha(2,680 lbs/ac) under field conditions and6,500 kg/ha (5,800 lbs/ac) under experimentalconditions (Delatorre-Herrera 2003).

This wide variation in yield indicates the largeeffect of location and variety on the performanceof quinoa. At present, yield data in temperateNorth America are available from only two loca-tions. Further variety testing will help determineyield potential for quinoa in new areas.

CHALLENGES TO QUINOA PRODUCTION

As a relatively new crop in North America, quinoafaces a diverse range of challenges as it continuesto be tested across a range of growing environ-ments across North America. The most limitingof these challenges is high summer temperatures,which greatly restricts the range of quinoa cultiva-tion across the continent to areas with mild sum-mer temperatures.

In areas where quinoa seed set is not threatenedby high temperatures, other major challenges,both abiotic and biotic in nature, exist and posepotential threats to successful quinoa cultivation.

Waterlogging and preharvest sprouting

The native range of quinoa cultivation includesareas characterized by high rainfall. For instance,a quinoa variety was collected from a locationon Chiloé Island in Chile (Wilson 1978), anisland characterized by high levels of annualprecipitation (2,500–3,000 mm or 100–120 in)(Vera 2006). However, when rainfall coincideswith seed maturity, preharvest sprouting canoccur and cause harvest loss among susceptiblevarieties. Preharvest sprouting was observed inquinoa trials held in 2010 in Olympia, Wash-ington. Here, a rare heavy rainfall event in latesummer caused substantial sprouting in many ofthe 44 varieties tested. However, a few accessionsproved more resistant to sprouting, including

PI 614880 (unpublished data 2010), which hadbeen collected from Chiloé Island. This accessionhas been shown to exhibit seed dormancy thatconfers preharvest sprouting resistance (Ceccatoet al. 2011). Variety trials in 2013 at two locationsin western Washington state were also affectedby rains in early September, causing sproutingin many varieties (Fig. 10.1) and also revealinga spectrum of preharvest sprouting resistanceamong the range of varieties tested.

Preharvest sprouting was also a challengefor quinoa breeding efforts in the Netherlands(Mastebroek and Limburg 1997). Quinoa vari-eties in the quinoa program at CPRO-DLOin Wageningen were successfully screened forpreharvest sprouting resistance by testing thedormancy of seeds relative to ripening. Variabilitywas found within the accessions and selection fortolerance to preharvest sprouting was successfullyachieved in the CPRO-DLO breeding program.

In a greenhouse experiment, González et al.(2009) noted a negative impact from waterlogging,which reduced total plant dry weight and leaf areamore severely than that of drought stress. Unnec-essary irrigation of seedlings can cause stuntingand damping off, and irrigation of quinoa duringlater growth stages is reported to increase vege-tative growth without a corresponding boost in

Fig. 10.1 Preharvest sprouting.


seed production (Oelke et al. 1992). Waterloggingin the germination phase had a deleterious impacton quinoa in a trial in the United Kingdom;varietal differences in tolerance to this stress wereobserved (Risi and Galwey 1989).

Disease

Owing to its geographical isolation, quinoa inNorth America has escaped many of the diseasepressures common to quinoa in its native range.However, at least one major pathogen of quinoa,Peronospora variabilis, which causes downymildew, has been reported in quinoa grown inCanada (Tewari and Boyetchko 1990). Downymildew has also been observed in field trialsin Washington state (unpublished data, 2012)and in Pennsylvania (Testen et al. 2012). Testenet al. (2014) identified widespread infection ofNorth American quinoa. Molecular screeningconfirmed P. variabilis infection in samples ofcommercially produced quinoa from Canada,Oregon, and Colorado. The strains of P. variabilisinfecting North American quinoa were also foundto be genetically distinct from P. variabilis strainsisolated from South America quinoa.

The downy mildew pathogen infecting quinoahas been shown to be closely related to strainsthat infect Chenopodium album, a common weedin North America (Choi et al. 2010). The authorssuggest the possibility that C. album may be apotential inoculum reservoir for downy mildewin quinoa. Using PCR-based methods, Testenet al. (2014) detected P. variabilis from a weedyC. album and an unidentified Chenopodium sp.collected in Ecuador. More investigation isneeded on the potential of C. album and otherclosely related Chenopodium spp. to host strains ofP. variabilis to which C. quinoa is susceptible. AsChoi et al. (2010) demonstrated, downy mildewexhibits a high level of host specificity. No threatis posed from strains of downy mildew that infectrelated crops such as spinach and beets, as thesestrains belong to Peronospora farinosa, a separatespecies from P. variabilis.

Variation for resistance to downy mildew existswithin the quinoa germplasm. Chilean lowlandvarieties have been reported to carry more

resistance to the pathogen than other ecotypes(Fuentes et al. 2008). However, reports fromDenmark of P. variabilis infecting Dutch andDanish varieties indicate that problematic levelsof susceptibility to P. variabilis do exist amongvarieties with a Chilean lowland background(Danielsen et al. 2002).

The close relative C. berlandieri has been notedto have high resistance to downy mildew (Jellenet al. 2011). The domesticate C. berlandieri subsp.nuttalliae has been crossed with quinoa with thegoal of introgressing downy mildew resistance(Bonifacio 2004). In a study screening downymildew resistance among quinoa varieties andChenopodium spp. under field conditions in India,accessions of C. berlandieri subsp. nuttalliae andthe North American species C. bushianum werereported to be immune to downy mildew (Kumaret al. 2006). The authors also observed diverseresponses, ranging from lack of disease to highsusceptibility, from a wide range of quinoa vari-eties, leading the authors to postulate the existenceof multiple pathotypes. Reports from breedingefforts in the CPRO-DLO program indicatedthat downy mildew resistance was dominantlyinherited (Mastebroek and van Loo 2000).

The reported diversity for downy mildew resis-tance should allow for the breeding of resistantvarieties. As C. berlandieri subsp. nuttalliae andC. bushianum have both been successfully crossedwith quinoa, these species represent anothersource for downy mildew resistance (Wilson1980).

Danielsen and Munk (2004) developed astandardized method, which they called the“three-leaf technique,” to determine the severityof downy mildew infection in terms of yieldreduction. They also noted the preference ofdowny mildew fungi for cool, moist conditions.The Salares-type variety “Utusaya” was found tobe highly susceptible to downy mildew. However,in its usual range of cultivation, “Utusaya” escapesinfection because of dry climate (Danielsen andMunk 2004). Escape from downy mildew infec-tion should be possible in western regions of theUnited States characterized by dry summers.This is supported by reports of reduced infection


in Europe under dry summer conditions as com-pared to more humid summers (Jacobsen 1999).In semi-arid conditions of eastern Washingtonstate, downy mildew has been seen on youngplants after the early spring rains, but infectionstopped with seasonal summer drought andappears to be a minor issue. Areas characterizedby wetter conditions and high humidity through-out the growing season may find downy mildew tobe a more significant problem. As downy mildewin quinoa has been shown to be transmissibleby seed due to oospores that form in the seedpericarp, care must be taken when introducingquinoa in new areas to prevent introducing thepathogen as well (Danielsen et al. 2004).

Additional Peronospora spp. may threatenquinoa. Testen et al. (2014) report infectionof Ecuadorian quinoa from an undescribedPeronospora sp., which produce unique symptomsin plants characteristic of a systemic infection.

Other fungal pathogens have also been reportedto infect quinoa in North America. Sclerotiumrolfsii causes damping-off of quinoa seedlings,as well as seed rot in a fall quinoa variety trialin Southern California (Beckman 1980). Morerecently, two new pathogens, Passalora dubia andan Ascochyta sp., have been found on quinoa inPennsylvania (Testen et al. 2013a, 2013b). Thepotential impact of these pathogens for quinoacultivation is currently unknown, and no reportsexist of these pathogens outside of researchcontexts.

Insect pests

Many insect pests have been reported forquinoa in its native range in South America,the most damaging of these being the quinoamoth (Eurysacca melanocampta and Eurysaccaquinoae) (Rasmussen et al. 2003). The potentialfor transmission of pests from South Americato North America is currently unknown. Thisdeserves further investigation, particularly assome farmers trying to grow quinoa in NorthAmerica plant quinoa seed that have been soldas food. This presents a possible route for theintroduction of seed-borne pests of quinoa, and

also the potential spread of these pests to closelyrelated Chenopodium spp.

Existing reports of insect pest pressuresin quinoa from Colorado and South Americaindicate little overlap in species (Cranshaw et al.1990; Rasmussen et al. 2003). Although two insectspecies (Macrosiphum euphorbiae and Helicoverpazea) reported in Peru and Bolivia were also foundin fields in Colorado, these species originate fromNorth America. Subsequent pest identificationsfrom Washington and Maine (I. Milosavljevic,personal communication, 2013; Conant 2002)have not revealed pests in common with thosereported by Rasmussen et al. (2003). Thus,existing evidence suggests that transmission ofinsect pests from South America to temperatelocations in North America has not occurred.

As quinoa continues to be grown in NorthAmerica, it is likely that native pest species willextend their host range to include quinoa. Thishas occurred in Europe, where two pests thatnormally feed on C. album, Scrobipalpa atriplicellaand Cassida nebulosa, have begun to attack quinoa(Sigsgaard et al. 2008).

Oelke et al. (1992) reports that insect pressurewas not determined to be a significant factor forquinoa grown in Colorado. However, a study ofpest pressures in Colorado found a wide range ofinsect pests on quinoa several years after its intro-duction. Many of the reported pests were alsopests of C. album and Beta vulgaris. The majorinsect pests attacking seedlings were Melan-otrichus coagulatus (Uhler) and the false cinchbug, Nysius raphanus Howard. Beet armyworm,Spodoptera exigua (Hübner), caused large-scaledefoliation at one location near Crestone, Col-orado. Another damaging foliar feeder is theboat gall aphid Hayhurstia atriplicis (L.). Lygusspp. were noted as injurious seed feeding pests,whereas the sugarbeet root aphid (Pemphigus pop-ulivenae Fitch) caused yield declines (Cranshawet al. 1990). Oelke et al. (1992) recorded sugarbeetroot aphid as a significant quinoa pest whosepoints of entry are cracks in the soil. In addition,flea beetles and aphids were reported on quinoagrown in Minnesota (Robinson 1986). During aquinoa trial in Maine, a plutellid moth (species


unidentified) was found to attack plants (Conant2002).

Darwinkel and Stølen (1997) noted someoverlap in the pests of beets and quinoa inEurope. Beet flea beetles (Chaetocnema concinnaand Chaetocnema tibialis) and beet carrion beetles(Aclypea opaca) were found to feed on quinoagrown in sandy soil, though no data is given onthe relative seriousness of these pests. Black beanbeetle (Aphis fabae) was also reported as a pestlikely causing decreases in yield.

In Washington state, aphids and Lygus sp. havebeen the major pests at test plots throughout thestate since trials were initiated in 2010. Harvestingaphid-infested plants results in quinoa seed mixedwith honeydew particles, which are considerablydifficult to remove from harvested quinoa seed.Lygus sp. has been observed to take shelter in morecompact inflorescences (unpublished data, 2010).In 2013, buckthorn aphid (Aphis nasturtii), yellowstriped armyworm (Spodoptera ornithogalli), andCrambus sp. were identified as pests in the field (I.Milosavljevic, personal communication 2013).

Various control methods for quinoa pestsin South America have been recommended,although much research remains to be done todevelop appropriate IPM strategies. Current pestcontrol strategies that are most transferable toNorth American conditions are crop rotation,intercropping, and the use of biocontrol agents.Varietal resistance for pests such as quinoa mothhas been observed (Rasmussen et al. 2003).

As pest pressures change and develop withexpanding quinoa production in North America,strategies for pest control will likewise change.Given the current pest pressures reported, somerecommendations can be made. In Colorado,Cranshaw et al. (1990) noted the syrphid larvae(Diaeretiella rapae) and the convergent ladybird beetle (Hippodamia convergens) as predatorsof the Chenopod aphid, Hayhurstia atriplicis.Variations in aphid pressures between sites werealso observed. The aforementioned species andother aphid parasitoids should be investigatedas potential biocontrol agents. Furthermore,the factors that determine the severity of aphidinfestation require further study.

As quinoa and other Chenopodium species sharecommon pests, studying the potential of weedyChenopodium sp. as alternate hosts is warranted.Close rotations of quinoa with related crops suchas beets should be carefully monitored to ensurethat pests common to both crops do not spread.

Weed control

The slow growth of quinoa after germinationmakes weed management particularly challeng-ing. Related Chenopodium spp. often pose a majorweed pressure, due to their similarities to quinoain early growth habit and appearance. Commonlambsquarter was also noted as a major weedpressure in southern Colorado, along with pig-weed, kochia, and sunflower (Oelke et al. 1992). InColorado, weed management recommendationsfor growers included early sowing, plantingin areas of low weed pressure, and cultivation(Johnson and Croissant 1985). Tilling the soil forplanting after irrigating was found to be effective,particularly with controlling Chenopodium spp.(Oelke et al. 1992). Late planting of quinoa inEngland led to complete losses due to heavy weedpressure (Risi and Galwey 1991a), confirming theimportance of early establishment of quinoa.

Grasses were found to cause major yieldreductions in quinoa. Johnson and Ward (1993)saw reductions in yield from 1,822 kg/ha(1,626 lbs/ac) to 640 kg/ha (571 lbs/ac) due tocompetition from grassy weeds.

Jacobsen et al. (2010) compared the efficacyof inter-row hoeing and harrowing for weedcontrol under Danish conditions. They foundthat inter-row hoeing, when combined with a rowspacing of 50 cm, was most effective at reducingweed pressure. Harrowing had a significant butless pronounced impact. Although both methodshad a significant decrease on quinoa stands dur-ing one of the 2 years the study was conducted,yield significantly increased with both methods.Chenopodium album was the predominant weedspecies, indicating that these methods wereeffective in controlling weedy Chenopodium spp.

A study by Risi and Galwey (1991b) in which10 quinoa varieties were grown in Englandshowed distinct differences in the negative impact


of weed pressure on plant height. Their observa-tions indicated that some quinoa varieties mighthave greater ability to compete with weeds.

Cross-pollination of C. quinoa with weedyC. berlandieri has been confirmed at a farm innorthern Washington state (Wilson and Manhart1993). Oelke et al. (1992) reported putativehybrids between quinoa and common lamb-squarter in Colorado (species unspecified). Suchpollination could have consequences in terms ofmaintaining purity of quinoa varieties. Controlof C. berlandieri will prove critical in preventingunwanted cross-pollination.

Saponins

Many varieties of quinoa contain saponins in theseed pericarp. Saponins give quinoa a bitter tasteand make it unpalatable. In addition, saponinshave potential negative health effects and havebeen shown to be disruptive to intestinal mem-branes in rats (Gee et al. 1993). For quinoa tobe marketable, saponins must be removed afterharvest. This is generally done through abrasionor by washing the saponin from the seed (Johnsonand Ward 1993). Alternatively, brushing has beenused as a saponin removal method (Darwinkel andStølen 1997). Removal of the saponin throughabrasion can result in loss of minerals such ascalcium (Konishi et al. 2004).

While industrial uses for quinoa saponin havebeen proposed (Jacobsen 2003), the presence ofsaponins currently poses postharvest difficultiesrather than an economic opportunity. The infras-tructure required for removal of saponins remainsa challenge for small-scale quinoa growers.Commercial production of quinoa in Coloradoonly began once machinery to remove saponinwas obtained (Johnson 1990).

Saponin-free varieties of quinoa do exist,though they are not found in the original Chileanlowland germplasm. The CPRO-DLO quinoabreeding program successfully introgressedthe saponin-free trait into improved varieties(Mastebroek and Marvin 1999). The presence ofsaponin is both qualitatively and quantitativelycontrolled. Its presence is governed by a singlegene with two alleles. Saponin production is

dominant, with homozygous recessive plantsproducing seeds lacking saponin (Ward 2001).When the dominant phenotype is expressed,saponin content is then governed quantitatively.Efforts to breed low saponin varieties quanti-tatively have not been successful, due to lackof sufficient response to selection (Ward 2000).Future efforts to develop saponin-free varietieswill likely rely on generating plants that arehomozygous recessive for the qualitative trait.However, this comes with the potential drawbackof saponin production being restored throughcross-pollination from other varieties that containsaponin. Proper separation of varieties lackingsaponin from those with saponin will be necessaryto prevent cross-pollination.

While the removal of saponin remains anobstacle for quinoa production, saponin-freevarieties have drawbacks. Reports from SouthAmerica and Europe indicate that saponin-freevarieties can suffer yield losses, some quite severe,due to feeding by birds (Risi and Galwey 1991b;Rasmussen et al. 2003; Darwinkel and Stølen1997). However, saponin-containing varietiesmay also suffer yield losses due to birds, as rainhas been reported to wash away saponins (Oelkeet al. 1992). This was observed at a trial site inChimacum, Washington, where feeding damagewas observed following rains in late summer(unpublished data, 2013)

Drought and salinity can have significanteffects on saponin content. Irrigation with salinewater resulted in a 30% increase in saponincontent compared to freshwater irrigation. At thelowest irrigation level, saponin content decreased42% in comparison to the full irrigation control(Gómez-Caravaca et al. 2012).

ALTERNATIVE USES OF QUINOA

Forage

In addition to the worldwide interest in quinoafor its seed, quinoa has also attracted attention asa forage crop. Carlsson et al. (1984) investigatedquinoa in southern Sweden and concluded thatit was a promising crop for the production of


green liquid protein concentrate. Dry matterproduction was found to increase with high levelsof fertilization, up to 470 kg N/ha (420 lbs N/ac).

Quinoa biomass had high crude protein andlow fiber when harvested near the floweringperiod and was competitive with alfalfa andgrass when compared on a cost basis. Quinoasilage was found to be an acceptable methodof storing quinoa fodder long term. Increasednitrogen applications were recommended forforage quinoa, with 100 kg N/ha (90 lbs N/ac)applied at sowing followed by an additional200 kg N/ha (180 lbs N/ha) applied 5 weeks later(Darwinkel and Stølen 1997). In contrast, tests inthe Netherlands showed that quinoa performedpoorly as a forage crop in comparison with grassand clover (van Schooten and Pinxterhuis 2003).

Feed

The balance of amino acids in quinoa seed hasgenerated interest in its utility as an animalfeed. However, the value of quinoa for humanconsumption currently exceeds its value as animalfeed. This would likely restrict any role of quinoaas a feed to low-quality quinoa and to organicfarmers looking for a high-quality, protein-richalternative to maize–soy mixes.

Carlson et al. (2012) tested quinoa hull meal,which contains the saponin-rich pericarp, as afeed additive for pigs. South American quinoahull meal was supplied at 100, 300, and 500 mg/kgand Danish-grown quinoa at 300 mg/kg; feedintake and utilization, as well as growth rate, wereall unaffected compared to those of pigs fed acontrol diet lacking quinoa hull meal, despite theeffects of South American quinoa hull meal onintestinal epithelial physiology detected ex vivo.

Several studies have been conducted on the useof quinoa as poultry feed but with mixed results.Improta and Kellems (2001) tested diets basedon raw, polished, and washed quinoa for broilerfeed. The survival and growth rates of chicks feda diet of raw quinoa were severely reduced, andthis effect was attributed to antinutritional factors(Improta and Kellems 2001). With the polishedquinoa diet, this effect was much reduced,whereas the effect of the washed quinoa diet

was comparable to that of the maize/soybeanmeal control diet. Improved performance wasalso seen in chicks fed diets with higher crudeprotein percentage, although this may also be dueto the lower percentage of quinoa provided withincreased supplementation of soybean meal.

Jacobsen et al. (1997) found that increasinglevels of both unprocessed and dehulled quinoa ina mixed broiler diet caused depression in broilergrowth. In contrast to the previous study, thechicks had poor growth when dehulled quinoawas included in the diet. The authors suggestedthat aside from the bitter saponins present inthe hulls, other antinutritional factors werealso responsible for this effect on the chicks.They recommended that quinoa comprise nomore than 150 g/kg (15% by weight) of broilerdiets. In a study investigating the combinationof two-layer diets with a supplemental foragerotation, a 34-day-long quinoa forage periodconsisting of two quinoa varieties, one of whichwas saponin-free, was included with no neg-ative effects on layers reported (Horsted andHermansen 2007).

CONCLUSION

Expanded production of quinoa in temperateareas of North America poses many challengesand opportunities. Despite the main obstacleof heat susceptibility, breeding efforts utilizingwithin-species diversity may result in varietieswith improved heat tolerance. Should that proveinsufficient, the North American Chenopodiumspp. within quinoa’s secondary gene pool mayprove to be a promising source for introgressionof heat tolerance genes. Existing genetic diversityhas been identified that should enable farmers andscientists to overcome challenges posed by downymildew, saponins, and preharvest sprouting.Many aspects of quinoa cultivation in NorthAmerica remain unknown, particularly diseaseand pest pressures, because of quinoa’s relativenovelty to North America and its geographicalisolation from pest pressures found in its nativerange of cultivation. The high level of abioticstress tolerance in quinoa may give it a distinct


advantage in areas with marginal agriculturallands, specifically those affected by soil salinity.Interest and demand for domestically producedquinoa remains high, and with further researchand plant breeding efforts, there is considerablepotential for expanded quinoa production inNorth America.

ACKNOWLEDGMENTS

Special thanks go to Ivan Milosavljevic forinsect identification and to Hannah Walters forproviding preliminary findings. We would alsolike to acknowledge the dedication of the diversegroup of individuals who have helped lay thefoundational work for quinoa as a crop in NorthAmerica. Last but not least, we would like toexpress our sincere gratitude and respect for themany indigenous peoples of South America who,living in close relationship to quinoa, have grownand shaped this dynamic crop over millennia.

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Chapter 11

Nutritional Properties of Quinoa

Geyang WuSchool of Food Science, Washington State University, Pullman, WA, USA

INTRODUCTION

Quinoa is known as a “complete food” andhas been called “mother grain” in the Andes(Abugoch 2009; Vega-Gálvez et al. 2010) due toits high nutritional value (Table 11.1) (Jancurováet al. 2009). The quinoa seed is as small as a milletseed, flat and oval shaped, with color rangingfrom dark red to pale yellow. The protein contentin quinoa is higher than that in other cereals andaccounts for about 16.5% of its dry weight. Lipidsare about 6.3% and higher than the lipid contentin other cereals. Carbohydrates are the majorcomposition in quinoa and comprise around69%. The fiber and ash content of quinoa are3.8%, comparable to those in other cereals.

In this chapter, the chemical composition andnutritional properties of quinoa is reviewed. Thecontent, composition and quality of protein, car-bohydrates, lipids, vitamins, minerals, antinutri-tional factors, and bioactive compounds are alsosummarized.

PROTEIN

Quinoa seed is considered a complete food(Abugoch 2009), primarily because its proteinis high in content and quality, with a balancedamino acid profile. The net protein utilization(NPU) of quinoa is 68, digestibility (TD) is 95,biological value (BV) is 71, and all of these are


indicators of the high quality of quinoa protein(Ruales et al. 2002).

The protein content of quinoa rangesfrom 8% to 22% among different varieties(Valencia-Chamorro 2003), higher than that ofother cereals such as wheat (9–14%) (Khanand Shewry 2009; Jancurová et al. 2009), barley(8–14%) (Cai et al. 2013), and rice (6–15%)(Juliano 1985) and lower than that of soy beans(28–36%) (Table 11.2). The reason for the highvariability in protein content among quinoa vari-eties is not clear yet, though both the genotypeand the growing environment can affect proteincontent.

About 57% protein exists in the embryo ofquinoa seed, 39% in the perisperm, and only 4%in the bran (including seed coat and pericarp)(Ando et al. 2002) (Table 11.2). Prego et al. (1998)studied the structural form of protein in quinoaseed. Fig. 11.1 shows protein bodies (PBs) (blackparticles) in spongy tissue of a quinoa cotyledon(a) and in endosperm cells (b). The diameterof the PBs in the cotyledon ranges from 0.3 to3 μm and 1 to 3 μm in the endosperm. These PBscontain one or more globoid crystals that storeminerals P, K, and Mg.

The amino acids of quinoa are well balancedand comparable to those of soy protein, casein,and wheat (Table 11.3) (Wang et al. 1999; USDA2011, 2005; Tang et al. 2006; Abugoch et al. 2008).Quinoa seed has high levels of arginine, glycine,lysine, methionine, threonine, and tryphtophan

193


Table 11.1 Chemical Composition of Quinoa and Cereals (Jancurová et al. 2009).

Quinoa Barley Maize Rice Wheat Oat Rye

Protein 16.5 10.8 10.22 7.6 14.3 11.6 13.4Lipid 6.3 1.9 4.7 2.2 2.3 5.2 1.8Fiber 3.8 4.4 2.3 6.4 2.8 10.4 2.6Ash 3.8 2.2 11.7 3.4 2.2 2.9 2.1Carbohydrates 69 80.7 81.1 80.4 78.4 69.8 80.1kcal/100 g 399 383 408 372 392 372 390

Table 11.2 Protein Content in Quinoa Seed Fraction (Ando et al. 2002).

Whole Grain Milled Grain Bran Perisperm Embryo

Protein content 12.9 13.3 6.1 7.2 23.5Proportion % 100 96 4 39 57

PB

PB

(a) (b)

Fig. 11.1 (a) Spongy tissue of quinoa cotyledon and (b) endosperm cell showing protein bodies (PBs) with globoid crystal(black arrow) (Prego et al. 1998).

compared to wheat. Glutamic acid and cysteineare lower in quinoa than they are in wheat,whereas histidine, isoleucine, phenylalanine,serine, and valine contents are comparable.Soy bean protein and casein are considered anutritionally balanced protein with high quality(Tang et al. 2006). The amino acids in quinoa arecomparable to those in casein, another indicationthat quinoa has excellent amino acid and proteinquality.

Quinoa seed is a great source of amino acidsas it contains all the essential amino acids(Table 11.4) (Friedman and Brandon 2001; Abu-goch et al. 2008). Moreover, all of the essentialamino acid content in quinoa are higher than therequirements suggested by FAO/WHO.

The protein in cereal is divided into fourgroups, namely albumin, globulin, prolamins, andglutelins. Albumin and globulins are the majorproteins in quinoa (76.6%), whereas the contentof glutelins and prolamins are much lower, at

12.7% and 7.2%, respectively (Table 11.5).Gluten is the protein complex formed by linkagesbetween proteins such as gliadins and gluteninsin wheat or glutelins and prolamins in othercereals (Koziol 1992). Gluten is critical to doughelasticity, loaf shape, and in imparting a chewytexture to the end product. However, a signif-icant proportion of the population in Westerncountries suffer from gluten intolerance andcoeliac disease. Coeliac disease is a chronic smallintestine inflammatory disease caused by geneticintolerance to gluten, such as gliadin of wheatand prolamins of rye and barley (Gallagher et al.2004). The prevalence of coeliac disease used tobe significantly underestimated from epidemi-ological studies (Hovdenak et al. 1999; Fasanoand Catassi 2001). Sabatino and Corazza (2009)discussed a more accurate method of estimatingthe true prevalence of coeliac disease usingserological tests for IgA antigliadin antibodies.With this method, studies showed that coeliac

Nutritional Properties of Quinoa 195

Table 11.3 Amino Acids of Quinoa, Soy, Casein, and Wheat(mg/g).

Amino Acid Quinoaa Soy Proteinb Caseinc Wheatd

Arginine 99.7 41.0 37.0 43Aspartic acid 80.1 118.1 63.0 51Glycine 53.8 38.6 16.0 37Glutamic acid 163.6 212.9 190.0 322Histidine 25.8 29.0 27.0 22Isoleucine 43.3 44.8 49.0 40Leucine 73.6 70.0 84.0 68Lysine 52.5 53.9 71.0 26Methionine 21.8 9.3 26.0 13Cystine 5.5 0.6 0.4 23Phenylalanine 44.9 53.0 45.0 48Tyrosine 35.4 37.1 55.0 –Serine 52.1 54.8 46.0 45Threonine 43.9 41.0 37.0 28Tryphtophan 38.5 – 14.0 18Valine 50.6 44.1 60.0 43Alanine 38.2 38.3 27.0 36

aAbugoch et al. (2008).bFAO/WHO suggested requirement (Friedman and Brandon2001).cUSDA (2011, 2005).dTang et al. (2006).

Table 11.4 Essential Amino Acid of Quinoa Protein andFAO/WHO Suggested Requirement (mg/g protein).

Essential Amino AcidQuinoaProteina

FAO/WHO SuggestedRequirementb

Histidine 25.8 18Isoleucine 43.3 25Leucine 73.6 55Lysine 52.5 51Methionine and cysteine 27.3 25Phenylalanine and tyrosine 80.3 47Threonine 43.9 27Tryptophan 38.5 7Valine 50.6 32

aAbugoch et al. (2008).bFAO/WHO suggested requirement (Friedman and Brandon2001).

disease in adult populations of United Kingdomand United States are 1:87 (West et al. 2003)and 1 : 105 (Fasano et al. 2003), respectively. Thedisease occurs in Caucasians in much higherfrequency compared to Africans and Asians(Hoffenberg et al. 2003; Di Sabatino and Corazza2009). The coeliac disease is life-long and the

Table 11.5 Subgroups of Protein from Quinoa, Maize, Rice,and Wheat (% Total Protein) (Koziol 1992).

Albumin+Globulins

Glutenins/Glutelins

Gliadins/Prolamins

Quinoa 76.6 12.7 7.2Maize 38.3 37.2 24.5Rice 19.2 71.9 8.9Wheat 17.1 54.4 28.5

only effective treatment is to consume gluten-freefoods (Gallagher et al. 2004). Gluten-free foodproducts are fast emerging in the western marketand the demand keeps increasing. Only smallamounts of prolamins in quinoa participate ingluten formation; thus, quinoa is recognized asgluten-free (Alvarez-Jubete et al. 2010a) andconsidered a potential ingredient in gluten-freeproducts and diet.

The quality and property of protein can beaffected by pH and temperature during extrac-tion or processing. Abugoch et al. (2008) isolatedquinoa protein by alkaline of pH9 and 11 andthen studied and compared the physicochemicaland functional properties of both isolations.Proteins from the two pH levels showed similarpatterns in native/sodium dodecyl sulfate poly-acrylamide gel electrophoresis (SDS-PAGE) andscanning electron microscope (SEM). Proteinfrom pH11 showed lower fluorescence intensityof tryptophan. Protein from pH11 showed noendotherm, whereas protein from pH9 showedan endotherm with denaturation temperatureof 98.1∘C and denaturation enthalpy of 12.7 J/g(Abugoch et al. 2008). Abugoch et al. (2009)also studied the stability of quinoa flour proteinduring storage. Protein solubility and waterabsorption were studied on quinoa flour stored atdifferent conditions. The results indicated thatquinoa flour can be stored at 20 to 30∘C in doublekraft paper bags for 2 months with no significantchange in functional properties.

Quinoa protein exhibits bioactive properties.Takao et al. (2005) provided evidence to indi-cate that dietary supplement of quinoa protein(5%) could control total cholesterol levels inboth plasma and liver of mice. The quinoa dietsuppressed enzymes that catalyze cholesterol


synthesis and stimulated cholesterol hydroxylase.In addition, lower molecular weight peptide inquinoa protein hydrolysate exhibited increasedradical scavenging activity and inhibited activityto angiotensin-converting enzyme, an importantfactor leading to hypertension (Kim et al. 2001;Wu and Ding 2001; Aluko and Monu 2003).

Protein plays a significant role in the functionalproperties of quinoa. The functional propertiesof food ingredients refer to the technologicalcharacteristics during processing, includingsolubility, emulsifying activity index, and foamingproperty. These are critical to food manufacturingas these affect the taste and mouth feel. Enzy-matic hydrolysis is a common method to improvefunctional properties of food. Aluko and Monu(2003) hydrolyzed quinoa protein with alcalaseand fractionated the hydrolysate by ultrafiltrationof 10,000 and 5,000 molecular weight cutoffmembranes. The functional properties of quinoaprotein concentration, protein hydrolysate, andmembrane permeates were studied. Proteinhydrolysate and membrane permeates exhibitedhigher solubility and lower emulsifying ability.Hydrolyzed peptides had low foaming property.

CARBOHYDRATES

Starch

Starch is the major component and predominantenergy reserve in cereal seed, providing 70–80%of human diet calories (Damodaran et al. 2008).The main source of starch in the human diet iscereal grain seed such as corn, rice, and wheat androots such as potato and cassava. Starch comprisesapproximately 55% of quinoa seed (Lindeboomet al. 2005).

Starch exists in nature as granules, smallparticles with diameters ranging from less than1 μm to more than 100 μm (Lindeboom et al.2004). Starch granules are categorized into threesize ranges: large (>15 μm), medium (5–15 μm),and small (<5 μm) (Wilson et al. 2006). In quinoaseed, starch granules are polygonal in shape, witha diameter of 0.08–2.0 μm (Ando et al. 2002),which is significantly smaller than the diameter

Table 11.6 Granule Size of Starch from Quinoa and OtherCereals (Lindeboom et al. 2004).

Source Diameter, μm

Quinoa 0.6–2Amaranth 1–2Rice 2–10Oat 2–14Buckwheat 2–14Wheat <10 and 10–35Rye 2–3 and 22–36Barley 2–3 and 12–32

EN

PE

R

F

P

H

SA

C

C

SC

Fig. 11.2 Quinoa seed structure. PE, pericarp; SC, seed coat;C, cotyledons; SA, shoot apex; H, hypocotyl–radicle axis; R,radicle; F, funicle; EN, endosperm; P, perisperm. (Prego et al.1998).

of starch granules in other cereals such as wheat,rice, and amaranth, a pseudo-cereal (Table 11.6)(Tang et al. 1998). Chen et al. (2003) indicatedthat starch granule size significantly affects theprocessing ability and quality of noodle. Noodlesmade from starch with smaller granule size offerbetter quality, which may be due to higher granulesurface area.

Most quinoa starch granules exist in perispermcells (Figs. 11.2 and 11.3) (Prego et al. 1998; Andoet al. 2002). The pericarp and seed coat cover theseed (Fig. 11.2). The endosperm consists of twocotyledons and one hypocotyl–radicle axis. The


REIH

P

C

RPC

K Ca

Mg P

S

0 0 0255 699 CPS 1179 CPS

0 0 02359 CPS 1398 CPS 480 CPS

Fig. 11.3 Refractive electron image (REI) and element mapping of a quinoa seed (P, perisperm; PC, pericarp; C, cotyledon; R,radicle; H, hypocotyl–radicle axis) (Konishi et al. 2004).

perisperm is in the middle part of the seed andconsists of 58.8% of grain weight (Ando et al.2002). Starch aggregates and granules are packeddensely in the cell of the perisperm (Ando et al.2002).

Starch granules consist of two types ofmolecules, namely amylose, which is linear,and amylopectin, which is highly branched.Amylose is composed of linear polysaccharidesof (1→ 4)-linked α-D-glucopyranosyl units withaverage molecule weight of 106 (Damodaranet al. 2008). Amylopectin is one the largestmolecules in nature, with molecule weight of107. It is composed of branched polysaccharideswith 4–5% α-D-(1→ 6) branch point linkage.Most grain starches contain about 25% amyloseand about 75% amylopectin. Amylose contentin quinoa ranges from 3 to 20% (Lindeboomet al. 2005), lower than that of wheat, corn, and

potato (Damodaran et al. 2008). Amylose andamylopectin percentage affects starch propertiessignificantly, including pasting, gelatinization,and retrogradation. Low amylose starch is morelikely to yield sticky food texture.

X-ray diffraction graphic divided starches tothree types: type A is present in cereal starch;type B exists in potatoes, roots, and resistantstarch; and type C is found in legume starch andmixture of corn and potato starch. The X-raydiffraction pattern of quinoa starch is type A, thetype common to most cereals (Table 11.7) (Andoet al. 2002).

Gelatinization temperature is the temperatureat which starches absorb water and start to swell.It reflects the amount of time it takes for cereals tocook. Gelatinization temperature is determinedusing differential scanning calorimetry (DSC).The onset gelatinization temperature (To) of


Table 11.7 Quinoa Starch Characteristics (Ando et al. 2002).

Analysis Range

X-ray diffraction pattern A-typeGelatinization, ∘CTo 54.0Tp 62.2Tc 71.0Enthalpy, ΔH, J/g 11.0

quinoa starches is 54.0∘C and the peak tempera-ture (Tp) is 62.2∘C, both of which are lower thanthat of barley and wheat starches (Tang 2004;Tang et al. 2005). The conclusion of gelatinizationtemperature (Tc) is 71.0∘C and enthalpy ΔH is11.0 J/g.

The swelling power of starch is an importantreflection of end-use properties such as noodlequality (Khan and Shewry 2009). It is calculatedas percentage of the sedimental paste weight tothe sample weight (Ahamed et al. 1996). Theswelling power of quinoa starch at 95∘C is 8.54 gH2O/g sample, lower than that of corn starch atthe same temperature (21.0 g H2O/g sample).This might be caused by the high level of lipidsthat form complexes with amylose and inhibitmobility of amylose. Freeze thaw stability ofquinoa starch is higher than that of wheat andbarley starch (Watanabe et al. 2007). Tolerance offreeze thaw suggests that quinoa can be used innovel food products.

On the basis of its properties, starch fromquinoa has been extracted and utilized in novelways. Araujo-Farro et al. (2010) utilized quinoastarch to make film, which exhibited excellentmechanical properties, low solubility, and goodbarrier properties. The quinoa starch film isedible and recyclable and can be utilized widelyin food packaging.

Sugar

Sugar content of quinoa flour was determinedby Ogungbenle (2003) (Table 11.8). Glucose andfructose can significantly increase serum glucosein human body. Their contents in quinoa are low,at 19 mg/100 g and 19.6 mg/100 g, respectively.Maltose content is as high as 101.00 mg/100 g,

Table 11.8 Sugar Content of Quinoa Flour (mg/100 gsample) (Ogungbenle 2003).

Sugar Content

Glucose 19.00Fructose 19.60D-Ribose 72.00D-Galactose 61.00Maltose 101.00D-Xylose 120.00

which indicates the potential of quinoa to be usedin malted beverages and breads. As maltose is asweet disaccharide with sweetness that is 46% ofthe sucrose standard, quinoa with high maltosecan also be used in weaning foods (Ogungbenle2003).

Dietary fiber

Dietary fiber refers to the family of carbohydratesin plants that cannot be digested in the humansmall intestine but can be partially metabolizedby microbiota in the large intestine. Dietaryfiber is divided into two types: (i) soluble fiberthat dissolves in water, including pectins, gums,mucilages, and some hemicellulose and (ii) insolu-ble fiber that does not dissolve in water, includingcellulose, lignin, lignin, and most hemicellulose.

Soluble fiber exhibits high water-holdingcapacity and creates viscous solutions. Fiberdelays gastric emptying, slows down digestion,creates postprandial satiety, and changes smallintestine transit time. Thus, a high fiber diet hasbeen shown to help with weight control.

Fiber can bond with lipids and cholesterols,resulting in decreased lipid absorption and serumcholesterol, thus helping prevent hypoglycemiaand hypolipidemia. High fiber intake increasesfecal volume to control constipation and othergastrointestinal disorders such as irritable bowelsyndrome and gallstone formation. Fiber can bedegraded and fermented in the large intestine.This property allows fiber to improve mucosalcell profile, maintain a balance of gastrointestinalmicrobiota, and protect against colon cancer.

Cereals, vegetables, and fruits are majorsources of fiber. Fiber content in quinoa is


8.8–10.3% (Wright et al. 2002), comparableto that of wheat (12.2%). The daily value offiber intake recommended by the USDA is 25 g.Quinoa is a high fiber food, as its fiber content is35.2–41.2% of the daily recommended value.

LIPIDS

Lipids in quinoa seed is about 6.9%, which ishigher compared to other cereals (Table 11.9)(Ogungbenle 2003). The iodine value is 54%,which indicates a proximate amount of unsatu-rated fatty acid fraction. Quinoa oil has a highproportion of unsaturated fatty acids that providemore health benefits compared to saturatedfatty acids. The acid value is 0.5% and peroxidevalue is 2.44%, which indicate that the lipidsare relatively stable and not easily oxidized whenexposed to heat and oxygen. Molecular weightor chain length of fatty acids can be representedby saponification value, which is the number ofmilligrams of KOH required to saponify 1 g offat under specific conditions. The saponificationvalue of quinoa lipids is 192%, lower than this is

Table 11.9 Properties of Quinoa Lipids (%) (Ogungbenle2003).

Component Value Content

Acid 0.50Iodine 54.0Peroxide 2.44Saponification 192.0

that of butter fat (241%) and comparable to soy-bean oil (194%) (Ogungbenle 2003).

The composition of lipids from quinoa isshown in Table 11.10. Palmitic acid is the mainsaturated fatty acid, comprising approximately10% of the total fatty acid content. Unsatu-rated fatty acids occupy about 87% of totallipids, including oleic acid (C18 : 1), linoleic acid(C18 : 2), and linolenic acid (C18 : 3). Linoleicacid (C18 : 2) is the major group, making up52.0% of the total lipids. Quinoa seed embryo ishigher in fatty acid content (10.2%) compared tothe perisperm, pericarp, and seed coat.

The total fatty acid of quinoa is 6.5%, higherthan that of corn oil (4%) and lower than that ofwheat germ oil (11%) (Table 11.11) (Ando et al.2002). Total fatty acid of other commercializedoil origins are much higher, ranging from 20%in olive oil to 60% in walnut oil. Saturated fattyacid in quinoa oil is 11% of total lipids, including10.2% palmitic acid and 0.8% stearic acid. High

Table 11.10 Fatty Acid Composition of Quinoa (100% DryBasis) (Ando et al. 2002).

Fatty AcidMilledGrain Perisperm Embryo

WholeGrain

Total fatty acid 6.7 5.0 10.2 6.5Myristic (C14:0) 0.2 0.1 0.2 0.2Palmitic (C16:0) 10.3 10.8 9.5 10.2Stearic (C18:0) 0.8 0.7 0.9 0.8Oleic (C18:1) 25.6 29.5 19.7 24.9Linoleic (C18:2) 52.0 49.0 56.4 52.5Linolenic (C18:3) 9.8 8.7 11.7 10.1Others 1.3 1.2 1.6 1.4

Table 11.11 Comparison of Percent Fatty Acid from Quinoa and Oil from Other Crops.

Fatty Acid Quinoa Corn Wheat Germ Olive Oil Canola Flax Coconut Oil Walnut

Total fatty acid 6.5 4 11 20 30 35 35 60Saturated FA 11.0 17 18 16 7 9 91 16Palmitic (C16:0) 10.2 – 0 – – 5 91 11Stearic (C18:0) 0.8 17 18 16 7 4 0 5Unsaturated FA 87.5 83 80 83 91 91 9 84MUFAOleic (C18:1) 24.9 24 25 75 54 19 6 28PUFA 62.6 59 55 8 37 72 3 56Linoleic (C18:2) 52.5 59 50 8 30 14 3 51Linolenic (C18:3) 10.1 – 5 – 7 58 0 5


intake of saturated fatty acid causes human healthissues such as obesity (van Dijk et al. 2009),cardiovascular disease (CVD) (Sacks and Katan2002), and type II diabetes (Hunnicutt et al.1994). Stearic acid was reported to decrease levelsof high-density lipoprotein (HDL), the goodlipoprotein that protects against CVD (Hu et al.2001). Saturated fatty acid proportion in quinoaoil is lower than that of other oils except for canolaand flax seed oil. Steric acid is only 0.8%, muchlower than that found in other oils.

Unsaturated fatty acid is divided into twocategories, monounsaturated fatty acid (MUFA)and polyunsaturated fatty acid (PUFA). TheMUFA has only one double carbon bond in lipidchain, for example, oleic acid (C18 : 1). On theother hand, PUFA has two or more double carbonbonds, such as linoleic (C18 : 2) and linoleic(C18 : 2). MUFA has been reported to exhibit anegative correlation to total mortality and CVDdeath (Jacobs et al. 1992). Olive oil is rich inMUFA (75%) and is the major source of fat in theMediterranean diet. The death rate due to heartdisease in Mediterranean populations is verylow, which can be explained by their MUFA-richdiet (Chait et al. 1993). MUFA in quinoa oil isapproximately 25%, lower than that of olive oiland canola but comparable to other oils.

Healthy PUFAs normally refer to n-6 polyun-saturated fatty acid linoleic (C18:2) and n-3polyunsaturated fatty acid linoleic (C18:2). Onthe basis of the metabolic studies, increasingintake of linoleic acid can improve lipid profile,lower cholesterol (Chait et al. 1993), and enhanceinsulin sensitivity (Lovejoy and DiGirolamo1992; Lovejoy 1999). Taking linoleic fatty acidnot only decreases the risk of coronary heartdisease (Chait et al. 1993) and significantlyreduces incidence of type II diabetes (Salmerónet al. 2001) but also decreases the risk of heartarrhythmia (Abeywardena et al. 1991). Linoleicacid content in quinoa oil is 52.5%, comparableto that in corn oil (59%), wheat germ oil (55%),and walnut oil (51%) and much higher than thatin olive oil, canola, flax oil, and coconut oil.

n-3 fatty acid α-linoleic (C18:2) (shortenedas ALA) is another functional food componentthat has been drawing attention from consumers

and the food industry. It is even more essentialto infants and children, because of its criticalfunction on brain and nerve development (Cun-nane and Thompson 1995). ALA can generatelong-chain n-3 fatty acid such as docosahexaenoic(DHA) and eicosapentaenoic (EPA) throughdesaturation-chain elongation pathway (Cunnaneand Thompson 1995). This effect of ALA isimportant because DHA and EPA enhances brainfunction and boosts the immune system. ALAalso inhibits the transformation of linoleic acidto arachidonic acid (C20:4, n-6) and controlsinflammation in the human body (Renaud andNordøy 1983). Excessive inflammation can leadto obesity (Wymann and Solinas 2013), type IIdiabetes (Oliver et al. 2010), CVD (Crumpacker2010), and gastrointestinal diseases (Ohmanand Simrén 2010). Epidemiologic studies haveprovided convincing evidence for the associationof ALA’s effect against CVD and arrhythmia(Hu et al. 1999). Although ALA in quinoa oil(10.1%) is lower than that in flaxseed oil (58%), itis relatively rich in ALA when compared to otheroil products, such as wheat germ oil (5%), canolaoil (7%), coconut oil (0%), and walnut oil (5%)(Table 11.11).

Linoleic acid and ALA compete for thedesaturation and chain elongation pathway (Garget al. 1989; Cunnane and Thompson 1995); thus,the balance between linoleic acid and ALA iscritical for human health (Chan et al. 1993). AnALA:linoleic ratio of between 1 : 10 to 1 : 5 hasbeen shown to help control coronary heart disease(Hu et al. 1999). The ratio of ALA and linoleicacid in quinoa oil is close to 1 : 5.

As a whole, the components of quinoa oil arewell balanced and beneficial to human health.Quinoa oil is low in saturated fatty acids and highin MUFA and PUFAs. Quinoa can be considereda potential oil seed with quality comparable toother commercialized functional oils.

VITAMINS

Cereals are one of the major sources of vitaminB complex. Cereal-based food products, such asbread and ready-to-eat cereal and rice, contribute


Table 11.12 Vitamin Content in Quinoa, Wheat, Rice, and Barley (mg/100 g).

Quinoaa– d RDI Wheate Ricef Barleyf

Thiamin (B1) 0.29–0.38 1.5 0.48 0.47 0.49Riboflavin (B2) 0.30–0.39 1.7 0.12 0.10 0.20Niacin (B3) 1.06–1.52 20 3.6 5.98 5.44Pyridoxine (B6) 0.487 2.0 0.43 NR NRFolate (B9) 0.781 0.4 0.054 NR NRAscorbic acid (C) 4.0 60 0 0 0α-Tocopherol (VE) (IU) 5.37 30 1.0 0.18 0.35β-Carotene 0.39 NR 0.02 NR 0.01

aKoziol (1992).bRuales et al. (2002).cRanhotra et al. (1993).dUSDA (2011, 2005).eKhan and Shewry (2009).f Jancurová et al. (2009).

approximately 45%, 30%, 28%, 14%, and 19% ofthe total daily intake of thiamin, riboflavin, niacin,vitamin B6, and folate, respectively (Khan andShewry 2009). Vitamin B provides an essentialfunction for the human body, whereas folate isknown to affect the health of the neural system.When folate-enriched cereal products werepromoted in the United States, the rate of neuraltube defects decreased (Yang et al. 2010). Studiesshowed that vitamin B6 and folate supplement candecrease the risk of coronary heart disease (Rimmet al. 1998), hyperhomocysteinemia in men(Ubbink et al. 1993), Alzheimer’s disease (Riederand Fricke 2001), and depression (Skarupski et al.2010).

Riboflavin (B2) and folate (B9) in quinoa is0.30–0.39 and 0.781, respectively, significantlyhigher than that in wheat, rice, and barley(Table 11.12). Pyridoxine (B6) in quinoa is0.487 mg/100 g, comparable to that in wheat,almost 25% of RDI, which shows that quinoa isa good resource of pyridoxine (B6). Folate, knownas folic acid and vitamin B9, plays an essential rolein embryo development and the production of redblood cells. As folate cannot be synthesized by thehuman body, it has to be supplied from the diet.Folate in quinoa is 0.781 mg/100 g, higher than inwheat, and even RDI. Therefore, quinoa is a greatresource of folate and should be recommended topregnant women.

Vitamin E refers to “tocols,” including α-,β-, γ-, and δ-tocopherols and α-, β-, γ-, andδ-totrienols, which are nonacyl lipids (Khan andShewry 2009). The relative activity of vitamin Eis calculated by tocol contents as α-tocopherolequivalents (Eitenmiller and Landen 1999).Vitamin E is the chain-breaking antioxidantthat protects the human body from free radicaloxidation (Maxwell and Lip, 1997), thus reducingthe risk of CVD (Pryor 2000; Trumbo 2005) andcancer (Papas and Vos 2001; Kline et al. 2007).Vitamin E in quinoa also protects the lipid fromoxidation. Quinoa seed oil is more stable duringprocessing and storage, even with high percentageof unsaturated fatty acids, due to the protectionof vitamin E (Ng et al. 2007).

MINERALS

In a typical western diet, approximately 50%of iron and manganese, 30% of copper andmagnesium, and 20% of zinc and phosphoruscome from cereals and cereal products (Cottonet al. 2004). Quinoa is a rich source of minerals(Table 11.13) (Ando et al. 2002). The potassium,magnesium, phosphorus, iron, magnesium, andcopper contents in quinoa whole grains arerelatively high, whereas zinc is deficient as deter-mined from the USDA daily intake reference.Most minerals in quinoa have higher content


Table 11.13 Mineral Content of Quinoa Grain Fraction (mg/mg%) (Ando et al. 2002).

Whole Grain RDIa Milled Grain Bran Perisperm Embryo

K 825.7 NR 639.3 2908.5(29%) 387.9(28%) 1125.4(43%)Mg 452.6 400 415.2 958.3(17%) 215.2(29%) 750.2(54%)Ca 121.3 1000 91.8 481.3(30%) 71.8(34%) 139.7(36%)P 359.5 1000 360.2 350.8(8%) 286.6(50%) 482.6(42%)Fe 9.5 18 9.2 14.3(13%) 7.2(48%) 11.3(39%)Mn 3.7 NR 3.4 10.8(19%) 2.4(38%) 5.1(43%)Cu 0.7 2 0.6 1.4(19%) 0.5(44%) 0.8(37%)Zn 0.8 15 0.8 0.7(9%) 0.6(48%) 1.1(43%)Na 1.3 NR 1.2 3.2(21%) 0.5(31%) 1.5(48%)aReference daily intake (USDA, 2011).

compared to that in wheat, which is deficient iniron, copper, manganese, and zinc (Khan andShewry 2009).

Konishi et al. (2004) studied mineral distribu-tion in quinoa seed by energy-dispersive X-raymicroanalysis (EDX) and scanning electronmicroscopy (Fig. 11.3). Phosphorus, potassium,and magnesium are located in the embryo andcontribute to formation of phytic acid and phytatein phytin globoids. Calcium is mainly in thepericarp and associated with pectin to develop thethick cell wall. Consequently, dehulling of quinoawould result in decreased calcium content.

ANTI-NUTRITIONAL FACTORS OF QUINOA

There are several anti-nutritional factors inquinoa, including saponins (0.1–5%), phytic acid(1.05–1.35%), and protease inhibitors (<50 ppm)(Jancurová et al. 2009; Vega-Gálvez et al. 2010).These factors could cause negative effects to thenutritional, sensory, and quality aspects of quinoaproducts. Phytic acid could bind minerals andaffect their metabolisms and functions. Quinoaalso contains small amounts of trypsin inhibitors,though at a much lower content than that in othergrains (Vega-Gálvez et al. 2010).

Saponins, found in the pericarp of the quinoaseed, are the most significant anti-nutritionalfactor in quinoa (Vega-Gálvez et al. 2010).

Saponins are plant glycosides that impart a bittertaste and form insoluble complexes with mineralsthat affect mineral absorption. As saponins arecontained in the pericarp of seed, they are easilyremoved through mechanical abrasion. Rinsingthe seed in cold alkaline water would also helpremove the saponins (Jancurová et al. 2009).

Saponins are glycosylated secondary metabo-lites that consist of a hydrophilic carbohydratechain and a lipophilic triterpene aglycone (Wink2004). Saponins in quinoa consist of carbohydratechains attached to a hydrophobic aglycone byglycosidic links. The carbohydrate chains ofquinoa saponins normally include arabinose,glucose, galactose, glucuronic acid, xylose, andrhamnose (Kuljanabhagavad and Wink 2009).Soponins are categorized into two groups(i) monodesmosidic saponins with single car-bohydrate chain and (ii) bidesmosidic saponinswith two carbohydrate chains (Kuljanabhagavadand Wink 2009). Monodesmosidic saponins areemulsifying agents and form stable foam in water.They also exhibit higher toxicity compared to thebidesmosidic saponins.

Although saponins are considered antinutri-tional factors, they also have beneficial properties,including analgesic, anti-inflammatory, antimi-crobial, antioxidant, antiviral, cytotoxic andhemolytic activity, and immunostimulatoryeffects, plus neuroprotective action. Saponins alsoincrease the permeability of the intestinal mucosaand reduce fat absorption (Abugoch 2009).


Table 11.14 Chemical Structure of the Aglycones in Quinoa (Kuljanabhagavad and Wink 2009).

Aglycone R1 R2 R3 Formula MW

HO

24 23

12

3 54

10 8

76

25

27

1516

17131426

9

1112

28 COOH

22

21

18

1920

3029 R3

R2

R1

Oleanolic acid (I) CH3 CH3 CH3 C30H48O3 456Hederagenin (II) CH2OH CH3 CH3 C30H48O4 472Phytolaccagenic acid (III) CH2OH CH3 COOCH3 C31H48O6 516Serjanic acid (IV) CH3 CH3 COOCH3 C31H48O5 5003β-Hydroxy-23-oxo-olean-12-en-28-oic acid (V) CHO CH3 CH3 C30H46O4 4703β-Hydroxy-27-oxo-olean-12-en-28-oic acid (VI) CH3 CHO CH3 C30H46O4 4703β,23α,30β-Trihydroxy-olean-12-en-28-oic acid (VII) CH2OH CH3 CH2OH C30H48O5 488

Recent studies show that there is a growinginterest in the bioactivity and health benefitsof saponins. The beneficial effects of saponinsare influenced by various functional groupsat different position of aglycones skeletons(Table 11.14) (Kuljanabhagavad and Wink 2009).Monodesmosidic saponins can affect the fluidityand permeability of cell membrane (Kuljanab-hagavad and Wink 2009). High concentrationsof monodesmosidic saponins are toxic becausethey can lyse, or break down, animal cells.However, moderate amounts of saponins canhave antifungal and antibacterial activity bylysing bacterial and fungal cells, such as those ofCandida albicans (Woldemichael and Wink 2001).The antifungal activity of saponins is dependenton the functional group of aglycone skeletons.Stuardo and San Martín (2008) pointed out thatcarbohydrate chain attached at C3 is critical forantifungal properties. Use of a saponin-basedmolluscicide to control Pomacea canaliculatasnails was tried in Southern Brazil and the resultsshowed that it could be effective in rice fields thatare not irrigated with heavily polluted water (SanMartin et al. 2008).

Inflammation is the nonimmune response tobody injury due to pathogens, damaged cells, or

irritants, with accompanying signs of increasedblood flow, vasodilation, and release of solublemediators (Ferrero-Miliani et al. 2007). Ordinaryinflammation is an important defense for bodilyhealth. However, inflammation can also be one ofthe basic reasons for many potentially fatal chronicdiseases such as CVD (Myasoedova et al. 2011),type II diabetes (Donath and Shoelson 2011), eyedisorders (Donoso et al. 2006), gastrointestinaldisease (Camilleri et al. 2011), obesity (Mathieuet al. 2010; Sun and Karin 2012), cancer (Kozlov2009), and neurodegenerative diseases, suchas Alzheimer’s and Parkinson’s diseases (Jones2001; Cameron and Landreth, 2010; Przedborski2010). Successive studies of Ghosh et al. (1983)and Mujica (1994) indicated that saponins hadanti-inflammatory activity and may explain whyplant saponins were used as anti-inflammatoryremedies in traditional medicine (Song and Hu2009; Keller et al. 2011; Raju and Rao 2012).Monodesmosidic saponins in quinoa such as3-O-β-D-glucopyranosyl oleanolic acid has thepotential to inhibit inflammation (Ma et al. 1989)and 3-O-β-D-glucopyranosyl hederagenin hasbeen reported to exhibit antioxidant activity(Ilhami et al. 2006).


BIOACTIVE COMPOUNDS

Phenolic compounds

Phenolic compounds containing at least onephenol ring are a major group of phytochemicalsin cereals, located primarily in the outer layer ofgrain (Gross 1980). Phenolics are divided intosimple phenols and polyphenols based on thenumber of phenol rings. Simple phenols includephenolic acids containing one aromatic ringwith one or more hydroxyl groups. Polyphenolsinclude phenolic acid dehydrodimers, flavonoids,lignans, and tannins that contain three or morephenol rings (Khan and Shewry 2009). Recentstudies showed that phenolics exhibited highantioxidant activity (Djordjevic et al. 2011; Minet al. 2012; Guo and Beta 2013), which wasdetermined by a combination of two methods(i) the DPPH (2,2-diphenyl-1-picylhydrazyl)scavenging capacity assay and (ii) ferric reducingantioxidant power (FRAP) assay (Karadag et al.2009).

Total phenolics content can be expressed asgallic acid equivalent (GAE). Total phenoliccompounds in quinoa seed have been reportedto be 71.7 mg GAE/100 g, which is higher thanthat in wheat (53.1 mg GAE/100 g) and amaranth(21.2 mg GAE/100 g) (Alvarez-Jubete et al.2010b). Red seeded quinoa was shown to contain50% more total phenolic content, 90% more totalflavonoid content, and 150% more FRAP thanyellow seeded quinoa (Brend 2012).

Phenolic acid

Phenolic acids are a group of phenolic com-pounds with single phenol ring. Phenolic acidsare mostly bound to cell structural componentssuch as cellulose, protein, lignin, or flavonoidsand sugars by the ester, ether, and acetyl linkages(Dervilly-Pinel et al. 2001; Yuan et al. 2005). Onlya small fraction of phenolic acids are free acids.Phenolic acids provide diverse functions to plant,such as nutrient uptake, enzyme activity, micro-bial habitation, and protection against pathogens(Ikegawa et al. 1996; Kroon and Williamson,1999). Gallic acid and rosmarinic acid are present

Table 11.15 Phenolic Acid Content in Quinoa and OtherCereals (μg/g wb).

QuinoaaWholeWheatb Cornb Riceb

Ferulic acid 440 890 380 240Caffeic acid 40 37 26 NDVanillic acid 43.4 15 4.6 7.8Gallic acid 320 ND ND NDCinnamic acid 10 ND ND NDp-Coumaric acid ND 37 31 76p-Hydroxybenzoic acid 76.8 7.4 5.7 15Syringic acid ND 13 7.8 ND

aPasko et al. (2008).bMattila et al. (2005).

with highest potential of antioxidant activity(Soobrattee et al. 2005). Ferulic acid, which isone of the main phenolic acids in cereal, not onlyexhibits high antioxidant activity but also crosslinks with arabinoxylans to form the cell wall andinsoluble dietary fiber (Faulds et al. 2004; Zhouet al. 2005; Yadav et al. 2007).

Phenolic acids in quinoa were analyzed qual-itatively and quantitatively by HPLC method(Mattila et al. 2005). Table 11.15 shows the typeand content of phenolic acids in quinoa and othercereals. Ferulic acid in quinoa is lower than it isin whole wheat, comparable to corn, and higherthan it is in rice. Gallic acid is the main phenolicacid in quinoa. p-Hydroxybenzoic acid, vanillicacid, p-coumaric acid, and cinnamic acid are alsofound in quinoa with significantly higher contentcompared to those in whole wheat, corn, and rice.

Flavonoids

Flavonoids are another group of phenoliccompounds with 2-phenyl-1,4-benzopyronebackbone and divided into subgroups as flavones,isoflavones, flavan, proanthocyanidins, andanthocyanidins. Flavonoids such as quercetinand epicatechin exhibit antioxidant activity(Leopoldini et al. 2006; Yin et al. 2012; Giménezet al. 2013) and has a negative correlation withthe risk of developing coronary heart disease(Kris-Etherton and Keen 2002; McCulloughet al. 2012) and type II diabetes (Wedick et al.2012). Flavonoids have the potential to benefit


cognitive performance both acutely and chron-ically (Lamport et al. 2012). Evidence indicatesthat flavonoids have potential to reduce the riskof cervical cancer (Ju et al. 2012), lung cancer(Khan et al. 2012), leukemia (Spagnuolo et al.2012), breast cancer (Zamora-Ros et al. 2013a),colorectal cancer (Zamora-Ros et al. 2013b), andprostate cancer (Adhami et al. 2012).

Flavonoids in quinoa include quercetin gly-cosides (43.4 μmol/100 g dw) and kaempferolglycosides (36.7 43.4 μmol/100 g dw) andare higher than that in buckwheat, whichhas 30.1 μmol/100 g dw quercetin glycosidesand nondetectable kaempferol glycosides(Alvarez-Jubete et al. 2010b). The tempera-ture and length of process can cause the lossof flavonoids in cereals (Sensoy et al. 2006).However, bread made from 100% quinoa flourmaintained most of the flavonoids content(Sensoy et al. 2006).

Isoflavones are a group of flavonoids that actas phytoestrogens in animals and human beings.They also stimulate osteoprogerin secretion,improve bone health, reduce arterial resistance,and exhibit antioxidant activities (Hsu et al. 2001;Teede et al. 2003; Li et al. 2013). Quinoa seed hasbeen shown to contain isoflavones, particularlydaidzein and genistein (Vega-Gálvez et al. 2010).

Anthocyanins are a group of flavonoid con-stituents that provide the bright red-orange toblue-violet colors in the plants. Epidemiologicalstudies showed that intake of anthocyaninsdecreases the development of CVD (Mink et al.2007). The role of anthocyanins in CVD relatestrongly with protection against oxidative stress(Wallace 2011). They provide protection fromDNA cleavage, estrogenic activity, enzyme inhi-bition, increased cytokine production, decreasedcapillary permeability and fagility, and membranestrengthening (Ramirez-Tortosa 2001; Acquavivaet al. 2003; Lazze et al. 2003; Rossi, et al. 2003;Lefevre et al. 2008). A low dose of anthocyaninsintake can reduce ischemia, lower blood pressureand lipid levels, and reduce inflammation inpatients with CVD. Anthocyanin content inquinoa has been reported at 102.4 mg CGE/100 gDW (Pasko et al. 2009), higher than that of

jasmine rice, amaranth, soy bean (Gorinstein et al.2007), and sorghum (Awika et al. 2005).

Carotenoids

Carotenoids are antioxidants, presenting provi-tamin A activity, colorants, and essentialcomponents of plant (Dini et al. 2010). They canquench singlet oxygen, which is an importantreactive oxygen species in light-induced oxy-gen. Carotenoids are also reported to preventage-related macular degeneration (AMD) andbenefit eye health (Alves-Rodrigues and Shao2004). They can reduce the risk of coronary heartdisease, protect from ischemic stroke, and protectskin from UV-induced damage (Alves-Rodriguesand Shao 2004). The carotenoids content in sweetquinoa is 0.4 mg/10 g, greater than the content ineinkorn (0.1 mg/10 g) (Hidalgo and Brandolini2008) and corn (0.07 mg/10 g) (Scot and Eldridge2005). The carotenoids in bitter quinoa are about0.08 mg/10 g.

SUMMARY

Quinoa is called “a complete food” for severalreasons. First, quinoa is high in protein, bothquantitatively and qualitatively. It contains all theessential amino acids, whereas many other cropsare deficient in some of them. For this reason,quinoa is a perfect protein supplement, especiallyfor vegetarians. Second, the lipids of quinoa arecomposed of a large proportion of unsaturatedfatty acids, which bring more health benefitsthan saturated fatty acids. Third, quinoa is richin vitamin B complex, vitamin E, and minerals,which are essential to human health. Last butnot least, bioactive compounds such as phenoliccompounds, flavonoids, and carotenoids in quinoaare the critical antioxidants in diet and providevital health benefits.

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http://www.nal.usda.gov/fnic/DRI/DRI_Energy/energy_

Chapter 12

Quinoa’s Calling

Sergio Núñez de ArcoQuinoa Specialist and Co-Founder, Andean Naturals, Inc., 393 Catamaran St., Foster City, CA, USA

INTRODUCTION

It is February 20, 2013, at the General Assemblyof the United Nations in New York. Quinoa, therediscovered staple of the Andean civilizations, isthrust into the limelight. It is the launching of theInternational Year of Quinoa (IYQ). The actingpresident of the UN opens the 64th Plenary Meet-ing with these words:

Too often in the past, we have heard extrava-gant claims for the benefits of different foods,but it is my opinion that, in quinoa, we trulyhave a plant that deserves the title of ‘superfood.’ In many ways, this traditional staple ofthe Andes region represents many of the ide-als and goals of the United Nations. It has animportant role to play in ensuring food secu-rity, boosting nutrition and, ultimately, erad-icating poverty. It also brings attention to theimportance that the United Nations attachesto indigenous knowledge and practice.

José Graziano da Silva, head of the FAO, fur-ther emphasizes the role that quinoa is expectedto play: “We are here to recruit a new ally in com-bating hunger and food insecurity – quinoa.”

Fast forward to December 31, 2013, the lastday of the Year of Quinoa. A storekeeper in a smallopen market in La Paz, Bolivia complains thatprices for quinoa have gone up so much that sales


are slow for this item. “People complain aboutthe price. They can get three bags of rice insteadof one of quinoa.” Bolivia is the second poorestcountry in the Western Hemisphere and theworld’s leading producer of quinoa. Even there,quinoa prices have doubled in 2013 reaching ahistorical high of $4/lb.

In the United States, the main consumer ofquinoa worldwide, quinoa prices are also set todouble. Quinoa packed for retail is going from$4/lb in September 2013 to $6–9/lb dependingon the presentation and retailer (Fig. 12.1).Quinoa is quickly gaining the reputation of anexclusive fancy food, a food for the wealthy:exactly the opposite of what the United Nationsenvisions.

As 2013 came to an end, the quinoa market wasrife with speculation. Prices were at a peak andno one can predict how this will impact demand.The 2014 quinoa crops in both Peru and Boliviawere expected to be at least 30% larger thanthose of previous years, and there will be addedcompetition on the market from nontraditionalquinoa-producing countries.

This is the quinoa conundrum: The UN desiresquinoa to be cheap, widespread, and accessible tothe poor; yet 45,000 smallholder farmers in theAndes recently lifted out of poverty are gratefulfor high prices. Could quinoa both provide fairincomes for thousands of smallholder farmers andbecome a healthy, inexpensive staple to the poor ofthe world?

211


Fig. 12.1 Shelf at a Whole Foods Store in California shows quinoa prices ranging from $5.50 to $9.00/lb. Photo credit: SergioNuñez de Arco.

A SNAPSHOT OF THE ECONOMICS OF ASMALLHOLDER FARMER IN BOLIVIA ANDTHE INTERNATIONAL MARKET

On October 10, 2013 at 6 AM, it is −5∘C (23∘F)as the sun begins to rise on Miguel Huayllas’3-ha field, located north of the Uyuni Salt flats, at13,000 feet in the southern Altiplano of Bolivia.Frost has struck again, but apparently the coldwas not strong enough to stop the rabbits fromcoming into his field and eating the leaves froma few rows. He will have to replant these rows byhand, with a “tempranera” or seed that has a shortgrowth cycle. The rest of the field is fine. “Thiswould have killed potatoes, barley, anything. Onlythe quinoa can withstand this cold.”

Bolivia has an estimated 35,000 smallholderfarmers like Miguel who produce quinoa, eachwith an average of 3 ha. Miguel’s production costsper hectare are $720, which includes the llamadung and some organic inputs he is provided oncredit (Table 12.1).

From each of his 3 ha, Miguel hopes to harvest19 “quintales” (100 lbs or 1 CWT apiece). Intotal, Miguel hopes to harvest 5,700 lbs. The year2013 has marked a historical high price for quinoa,reaching $2.70/lb farm-gate price by the end ofthe year. “I could sell all my quinoa right now, themiddlemen here are offering us high prices everyweekend.” Miguel, like most quinoa farmers inBolivia, only sells a third of his crop at harvest inApril and May. He then sells another third overthe course of the year to cover living expenses.The remaining third he keeps as insurance, onlyselling it in late January, once he is sure that his

Table 12.1 Production costs, based on actual resultsfrom production of Jacha Inti suppliers of organicquinoa grown in the southern Altiplano region ofBolivia.

Production costs USD per ha

Soil preparation 79.14Organic inputs (seed, fertilizer) 164.53Labor costs

Planting 71.94Weeding 28.78Fertilizing 14.39Pest Control 1 14.39Pest Control 2 14.39

Harvest costsHarvest with scythe 103.6Threshing 89.93Threshing labor 14.39Winnowing 14.39Poly-woven bags 10.07

Transport costs 100.72Total per hectare ϖ720.65

new quinoa crop will be successful. The gradualrelease of inventories at going market rates by thesmall farmers keeps the quinoa washing/cleaning(or “processing”) plants busy but fails to providethe security and volumes of forward contractingthat multinational food companies seek.

If prices stay at the current levels, Miguel’sfarm could bring in revenues of $15,390 for the2014 crop year. For a family of five, with threeworking adults, this is a per capita income ofalmost $13 per day for the adults, much highereven than the equivalent minimum wage theycould earn in the cities, which is $8 per day.Miguel, however, does not have the benefits of

Quinoa’s Calling 213

an employee; a pension for retirement and healthinsurance are luxuries that he aspires to.

Things are going well for quinoa farmers, andmuch has changed in 10 years. Back in 2004,quinoa farmers struggled to survive, producingquinoa for self-consumption and trading. Theironly hope for improvement was to move out of thecountryside to the cities. Gradually, the averagequinoa farm went from producing on less than1 ha to farming on 3 ha. Prices have gone from 60cents a pound to $2.70 in the past decade. Quinoafarmers today can send their children to nearbytowns for higher education.

“We don’t like all the uncertainty. I wish priceswould have stayed at the same level they havesince the 2008 increase,” Miguel tells us as we tryto purchase his remaining stocks. “Why shouldI sell now, if prices are going up almost everyweek?” Multiply Miguel’s position by thousandsand the market will be continuously short onquinoa and bidding ever higher prices to securethe stock available. Bolivian exporters have tofill sales contracts after all. Eager to cash in onthe quinoa craze, Bolivian exporters (usuallyprocessing plants) sold forward contracts to USimporters banking on the promises of hundreds ifnot thousands of small family farmers to deliverat a set price. These contracts were then forwardsold to food companies, distributors, and super-markets. In 2013, this situation came to a crisiswhen farmers started delivering at higher marketprices or not delivering at all. Prices skyrocketedfrom $3,600/metric ton (MT) in January 2013 to$8,000/MT at the end of the year (for washed,cleaned, export-grade white quinoa). Faced withcontract defaults from their vendors at origin,importers started bidding up the price of quinoato secure the product they had sold forward.

At the beginning of 2014, there were manyquestions in the minds of stakeholders in thesupply chain. With raw material in Bolivia costingalmost three times the price that had been stablesince the last increase in 2008, farmers were won-dering what is going on. They wanted to knowwho are buying quinoa at these ever-increasingprices? At the other end of the market, food com-panies wonder how they can include more quinoa

in their products when prices are so volatile andthey cannot be assured of long-term contracts.

Part of the solution may come from newquinoa-producing countries, including NorthAmerica, which will follow the more traditionalsupply chain model that includes annual contractsof large volumes. As the market feeds from thismuch requested new supply of quinoa, it mayseem that quinoa is headed down the path ofbeing a cheaper commodity. It may then fulfillits role as a tool to combat world hunger, as theUnited Nations calls it to be. But how will MiguelHuayllas and his fellow smallholder quinoafarmers fare in this new environment?

THE QUINOA MARKET: SUPPLY ANDDEMAND

Bolivia, Peru, and Ecuador increasequinoa acreage

It is important to note that there is very littlemarket data for quinoa. Most of the numbershere were compiled from data from the FAO,Bolivian National Statistics Bureau and Cus-toms, the Peruvian SUNAT, and US Customs(Figs. 12.2–12.4).

Evolution of quinoa, (Figs. 12.7–12.10and Fig. 12.3) acreage in Bolivia

There are an estimated 40,000 to 60,000 small-holder family farms in Bolivia that plant quinoa.

Suitable for cultivation

Lakes, salt flats, steepmountains

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Fig. 12.2 Land considered suitable for cultivation and pas-ture in the Altiplano.


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Fig. 12.4 US quinoa imports in MT per year, organic versus nonorganic. (See color insert for representation of this figure.)

The average family farm has gone from farmingunder 1 ha before the year 2000 to 3 ha at present.With this last increase, production of quinoa takesup one-sixth of the marginally productive lands ofthe Altiplano (Fig. 12.2).

Before the 1980s, Bolivian quinoa producersplanted an average of 20,000 ha of quinoa mainlyon protected hillsides. These microclimate pock-ets were planted manually onto rocky hillsidesthat provided protection against frost. Quinoa


was planted there in rotation with corn, potatoes,and beans.

After 1983, spurred by some initial demandfrom the Asociación Nacional de Productores deQuinua (ANAPQUI) for export to Europe andthe United States and by the Peruvian market,planting increased to an average of 35,000 ha(Fig. 12.3). The increase showed that quinoacould be cultivated in a semi-mechanized manner,utilizing tractors to turn over and clear flatlands. These lands, previously not utilized forcultivation, were discovered to be adequate forquinoa production. It is speculated that globalwarming caused the change in climates, makingfrosts less frequent in the flatlands and openingthese up for quinoa production.

Cesín Curi from the Center for the Promotionof Sustainable Technologies (CPTS) in Bolivia,the nonprofit organization behind the develop-ment of the leading quinoa washing and cleaningtechnology, estimates that there are 250,000 hathat are designated for planting quinoa in theBolivian highland plateau (“Altiplano”), out ofan estimated 1.5 million hectares of marginallyproductive land.

These marginal lands are in protected areas,such as around the shores of Lake Titicaca. Today,these are used for pasture and the productionof potatoes, wheat, barley, tubers, and beans.Although there still seems to be plenty of roomto grow quinoa, it will be at the expense of othercrops and will encroach on pastureland. As CesínCurri points out in his organization’s quest forfunding for experimental fields in arid lands, “Ifquinoa could be cultivated in the ‘non-suitableareas for cultivation,’ then the growth potentialfor quinoa is enormous.” Still, the questionremains of how cost-competitive cultivating in

these desert areas can be. The land there is sandyand low in nutrients and quinoa production inthese areas will most likely require syntheticfertilizers.

The US quinoa market and evolutionof prices

The United States is the main market for allquinoa exported, consuming an estimated 30%of all quinoa produced in 2013. The amount ofquinoa imports and the importance of the UnitedStates for quinoa have both increased in the pastfew years at a rapid pace, as shown in Table 12.2.

Quinoa in the eye of a market storm

Quinoa benefited from the megatrends of wholegrains, organic/natural foods, and gluten-freefoods.

The US market for quinoa had three stages ofgrowth:

• Mid 1980s to 2000. During this initial phase,the quinoa market grew to 1,000 MT. Thisphase included Hispanic food importers andnatural-food pioneers such as Ancient Harvestimporting quinoa from Bolivia, ArrowheadMills importing from Peru, and Inca Organicsimporting from Ecuador. These companiesexperienced some growth, but struggled withlow market awareness, limited distributioninto natural channels, and sourcing difficulties(mainly quality issues and low available volumesdue to limited processing plant capacities).

• 2000–2007. In the early to intermediate phase,the quinoa market grew from 1,000 to 3,300MT (Table 12.2). This phase was markedby a rapid development of the organic food

Table 12.2 US quinoa imports in metric tons per year and US imports as a percentage of total world production.

2004 2005 2006 2007 2008 2009 2010 2011 2012 2013

Quinoa imports in MT peryear

1,548 2,425 2,479 3,346 5,824 8,456 11,901 16,557 26,155 36,038

Growth per year, % 57 2 35 74 45 41 39 58 38Quinoa imported intoUnited States as percentageof world production, %

4 6 10 11 15 21 26 30


industry, which was experiencing annualgrowth rates of 15–20%. The low-carb trendled by the Atkins diet was fading, and in itsplace emerged a strong interest in whole grains.In Bolivia, quinoa processing plants developedbetter washing systems with the support ofnonprofit organizations. These in turn werein a better position to offer higher volumes ofwashed/cleaned quinoa to the market. By 2007,Trader Joe’s supermarkets started carryingquinoa nationwide, marking the transition ofquinoa from an organic niche product to aspecialty food market item.

• 2007–present. The quinoa market growsfrom 3,300 to 36,000 MT during this phase(Table 12.2). This growth phase is marked bythe entry of quinoa into the mainstream market.Larger facilities in Bolivia and Peru offer amore reliable and larger supply to food compa-nies. With importers and commodity traderswilling to take risk on importing large volumesof quinoa to provide long-term contracts toretailers, new quinoa-based lines and brandsare launched, particularly at Costco and WholeFoods supermarkets. By December 2013, therewere over 200 registered importers of quinoa inthe US market purchasing from 169 exportingcompanies. In 2012, multinational food com-panies (Kellogg, Pepsico, Mars) launched newquinoa product lines. In 2013, quinoa retailmarket leader Enray (TruRoots) was acquiredby Smuckers.

Today, quinoa is considered a standard bearerof the organic and health food movements. Of allthe quinoa sold in the United States, over 65% iscertified organic (Fig. 12.4). This is due to the factthat the brand holders and importers who spear-headed the initial growth of the market had a com-mitment to organics. As one starts looking at newproduct launches, it is evident that future marketgrowth of quinoa will no longer be in branded bagsfor retail but as an ingredient in ready-to-eat pack-aged goods.

Quinoa has three main destinations in storesand markets:

Quinoa in a retail pack for use as a side dish. All ofCostco, Trader Joe’s and one of seven brandsof quinoa on retail at Whole Foods are Bolivian

Organic. This is where Bolivian quinoa, witha larger seed and uniform size is preferred(Fig. 12.5). Quinoa in bags available at retailerssuch as Target, Marshalls, and Home Goodstend to come from Peru.

Quinoa in a grain blend for use as a side dish (e.g.,rice–quinoa blend). Of five blended products,only two have Bolivian quinoa. In blendedproducts, size, cooking time, and appearancein general are less important. This includesflash-frozen quinoa that is ready to eat. In thissegment, organic certification is less important.

In products made with quinoa (pastas, cookies, breadmixes, cereals, whisky, vodka, and shampoos)where the origin of quinoa is unknown. As themarket for quinoa evolves, there is an increaseddemand for quinoa to be used as an ingredient.In these markets, the quinoa seed size, organiccertification, cooking time, and flavor are notas important as the price (Fig. 12.6).

Fig. 12.5 Close-up of white quinoa seeds. Photo credit:Vitaliy Prokopets.

Fig. 12.6 Multiple quinoa varieties are planted and har-vested in the same fields. Photo credit: Vitaliy Prokopets. (Seecolor insert for representation of this figure.)


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Bolivian organic quinoa prices per MT price at port of origin

Fig. 12.7 Bolivian organic quinoa prices per MT price at port of origin.

Quinoa prices have been an issue in 2013, aftera period of relative stability between 2009 and2012 (Fig. 12.7). What has been an importantdeparture from recent years, however, is thedifference in price between Bolivian and Peruvianquinoa. In December 2013, Bolivian organicquinoa was sold at an average of $8,000/MT,whereas Peruvian organic quinoa went for$7,000/MT. Historically, Peruvian quinoa soldfor only $200/MT below Bolivian. This differ-ence may be influenced by multiple factors, oneof which is the higher demand and preference forBolivian quinoa (which, as mentioned earlier, ispreferred for its size and uniformity).

Both Bolivian and Peruvian governments areconcerned with the high prices of quinoa andare taking action. Rather than taking a hardstance with export controls or nationalization ofindustries, both countries have opted for subsidiesto continue providing quinoa at lower prices insocial programs such as school lunches, increasedinvestment in research into quinoa productionand processing, and funding made available forincreased production (loans for materials, seeds,and working capital to growers).

Bolivia, Peru, and Ecuador, as well as non-traditional quinoa-producing countries, areexpanding acreage in 2014 (Fig. 12.8). Bolivia’sNational Statistics Institute (INE) estimates a

29% increase in quinoa cultivations for 2014.Supply is certainly set to increase for 2014 andthe entire supply chain expects a price drop(Figs. 12.9 and 12.10). Farmers will certainly bethe first to feel the impact of the supply–demandequation, many fearing a return to subsistenceagriculture.

The quinoa grower rises out of poverty

In this section, I will focus on the economics of thefamily farmers in the Salt Flat Region of Bolivia.

The World Bank has set a poverty line of$1.25/day/adult, which equates to $112/monthfor an average quinoa-producing family withthree working adults. This threshold was passedin 2012 for the average quinoa farm with incomesgoing from $34/month/farm in 2007 to $240in 2012. As Bolivian quinoa farmers look for-ward to 2014 and beyond, their incomes couldreach $800/month with increased acreage andimproved yields.

Raúl Vera Copa, President of Association ofProducers of Quinoa and Camelids (APQC)(Fig. 12.11), an association of 200 producingfamily farms in Bolivia, shared his views duringan interview the Shared Interest documentary,which aired October 2013. Below is a translationof an excerpt of Raúl’s interview:


90,000

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Fig. 12.8a Production per country per year in metric tons (MT).

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Fig. 12.8b Quinoa production in MT per year.


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Quinoa production in MT per year

Total internal consumption

Total exports

Fig. 12.9 Quinoa production, consumption, and exports in MT per year from main producing countries.

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Fig. 12.10 Quinoa exports per country in MT per year.

I remember when there was almost notenough. Sometimes when we were young wedidn’t even have shoes to go to a party, andto go to Challapata (nearest town). We didn’tuse shoes before. Little by little things have

improved. (… ) Before, when there was noJacha Inti, no cleaning plant, we sold thequinoa to middlemen at 200, 300 or 400, andon top we also invested in clearing lands,in the planting and the care, scarecrows, all


Fig. 12.11 Raúl Vera Copa, President of APQC, an associationof 200 producing family farms in Bolivia. Photo credit: MatíasMusa.

of that, and we earned very little. But sincethere is this demand, now we are satisfiedthat quinoa has gone up in price. And alsothese earnings we don’t want to take themout to the cities. No, with the resources thatwe are using now we want… we want to livewell. And improve our houses, we want abathroom and also, I don’t know… to havea dining room, and good bedrooms, so ourchildren can stay in these fields.

The prices Raúl mentions are in “Bolivianosper Quintal,” about US$0.30–0.60/lb of unpro-cessed quinoa. One quintal= 100 lbs= 1 CWT,which is the main measure for trading quinoa inBolivia (Fig. 12.13).

Indeed, for Raúl and 50,000 similar familyfarmers, quinoa production has drasticallychanged their lives, lifting them out of poverty.The APQC is in the heart of the quinoa-producingregion of Bolivia in the southern Altiplano. Thisregion has an estimated 9,000 farms and is locatedaround the salt flats, a large expanse visible onsatellite pictures. At an altitude of 13,000 feet,this is a highland desert with arid, saline soilswhich receives only 8–12 inches of rain a year.The poor soils, lack of irrigation, and year-roundfrosts limit the cultivation of alternative cropsto some protected microclimates located aroundthe fringes of the mountains. Even today, theselands are distant from the main cities and werenot considered suitable for cultivation by theSpanish. The lands were left to the indigenouscommunities. It takes 10 hours of driving from

La Paz to reach the quinoa region, and half of thedrive is on unpaved roads (Fig. 12.12). As in thepast, today the land is communally owned, withfarmers having access to land based on heritageand years of residence in the area.

On average, farmers in the Bolivian SaltLake region cultivate farms around 6 ha. Mostfarmers have plots ranging from 1 to 5 ha; thesefarmers are considered small-scale growers.Medium-scale growers are those with 6–15 haand the few large-scale growers start at 16 ha.The lands belong to communities, with farmershaving the rights to a certain acreage inheritedfrom their parents.

Until 2008, Bolivian quinoa farmers practicedsubsistence agriculture, and they barely coveredtheir production costs. Emigration to cities wascommon. A farmer typically produced on 2 ha,with an estimated production cost of $500/ha.His land would yield 1,800 lbs, which he wouldsell at a market rate of $0.39/lb for a net incomeof $404 per year per farm, which is around $34 amonth.

Higher prices and demand in 2008 enticedfarmers to increase acreage and allowed them tostart hiring outside labor and services, mainlytractor services, and invest in organic inputs.

With the increase in quinoa demand worldwideand the subsequent increase in prices, there hasalso been a shift in the way the farmers lived.Eufraen Huayllas, President of APROCAY, in aninterview for the documentary “Shared Interest,”said that … “the quality of life has improved

Fig. 12.12 Unpaved roads leading to quinoa fields. Photocredit: Vitaliy Prokopets.


Table 12.3 Evolution of hectares farmed, quinoa production costs, and earnings for Bolivian farmers.

PeriodLand areafarmed, ha

Cost ofproduction,USD/ha Yield, lbs/ha

Sales price,USD/lb

Annualprofits, USD

Equivalent monthlynet incomea, USD

Before 2008 2 500 1,800 0.39 404 342008–2012 3 660 1,500 1.07 2,835 2362013 4 720 1,300 1.70 5,960 4972014 (projected) 6 800 1,900 1.00 6,600 550

aFarmer’s equivalent net income: (hectares planted× yield×market price)− (production cost per acre× acreage planted).

because, before, in this community, we only livedand produced for our own consumption. Wehad our sheep, our llamas and small plots…because when I was small quinoa was not valued.”APROCAY is an association with 63 memberfamilies in Bolivia.

Table 12.3 shows how the income from amedium-scale quinoa farm would have evolvedin the past few years, as demand and pricesincreased.

The shift in quinoa prices, as seen in Table 12.3,can be divided in four phases: (i) Until 2008,prices were relatively stable, with an initialweak demand driven mainly by the emergingPeruvian market and organic industry pioneers inEurope and the United States (Priméal, QuinoaCorporation). (ii) In 2008, there was a markedincrease with prices almost tripling, going from275 to 800 bolivianos per CWT ($0.40–1.15/lb ofunprocessed quinoa) (Fig. 12.13). This increasewas caused by strong demand in North Americamarked by the entry of Costco and Trader Joe’ssupermarkets to the quinoa market. (iii) Afterrelative stability from 2009 to 2012, prices onceagain drastically shot up in 2013, this time takingunprocessed quinoa prices from 800 to 1,850Bolivianos per 100 lbs ($1.15–2.59/lb). Thislatest price spike was linked to a high demand,a tight supply, and much speculation caused byall the attention given to quinoa during the IYQ.(iv) As Fig. 12.13 shows, the latest price increaseis expected to be corrected in 2014, so for theintent of determining the average income in 2014,a value of 700 Bs/CWT ($1/lb) for unprocessedquinoa was taken. This value is completelyspeculative, as it will depend on the market atany given moment. We estimate, however, that

it is unlikely that new sources will compete withBolivia at less than $1/lb of unprocessed rawmaterials.

On average, yields per hectare for mechanizedcultivation of organic quinoa in Bolivia are13 CWT (1,300 lbs), yielding seed that costs$0.55/lb. With additional inputs and improvedorganic management practices, this yield canbe increased to 20–25 CWT. This yield is lowcompared to the Peruvian nonorganic produc-tion, which yields 33 CWT/ha (3,300 lbs) andcosts $877/ha to produce, yielding seed that costs$0.27/lb to produce.

CURRENT PRODUCTION PRACTICES,INCREASED ACREAGE, AND THOUGHTSON SUSTAINABILITY

Efigenia Encinas, representative of Sumaj Camañaassociation of Women Farmers (Fig. 12.14), wasinterviewed about her farming practices andthoughts on sustainability. Below is a translatedexcerpt of her interview:

Interviewer: Do you have children, are youmarried?

Efigenia: No, I am single because I am theeldest daughter and I always have wanted torepresent the people and my family. I usedto sow quinoa by hand with my grandfather.My grandfather left us this place and I pre-serve it.

Interviewer: So, since when have youproduced quinoa?

Efigenia: Since I was 10 or 12. I used tosow by hand with my grandfather. Because


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Fig. 12.13 Farm-gate (unprocessed) quinoa prices in Bolivia in $/lb.

this community was very small, now it’s big-ger.

Interviewer: And now how do you plant?Efigenia: Now we plant with machinery.

And with this “Satiri” tractor as they callthem. With that. Before, we planted byhand. In those small fields where we werebefore, that’s where we used to produce.

Interviewer: Do you think the produc-tion will improve now with the tractors? Howdo you see it?

Efigenia: For me there are advantages anddisadvantages, because, imagine, there is landerosion that I see and the consequences ofwinds, the climate factor. Before, there werebushes everywhere, so this land was for graz-ing. Now sometimes there are no green bar-riers, so because of that the grooves made bythe tractor get swept by the wind. Before weplanted by hand, hole by hole, step by step.So these consequences can cause the produc-tion to fail.

Interviewer: So, your advice for improv-ing the production…

Efigenia: My advice for improving theproduction would be to keep the live barriersand also to raise animals in order to havenatural fertilizer, because before we alwayssowed with llama and sheep manure, withmanure, so I believe everything was natural.Now I know we need a lot of supplies, theseorganic fertilizers that are already produced.It’s like using a shampoo or oil for the pro-duction. That’s what I see. Because beforeour sacrifice (monetary investment) wassmall, but the plant was healthier. There wasnot this erosion of land. Now, I think that tomaintain the sustainability we shouldmaintain the raising of livestock, alsomake live barriers. Plant them wherethere are none.

Cultivation practices have evolved since the1960s when Efigenia Encinas planted quinoa


Fig. 12.14 Efigenia Encinas with her lamb. Photo credit:Diego Nuñez de Arco.

Fig. 12.15 Replanted quinoa in a field where earlier plant-ings had been eaten by rabbits. Photo credit: Stefan Jeremiah.

manually with her grandfather. At present,manual planting is relegated to steep hillsides,and when farmers need to replant because of frostor localized pest attacks (Fig. 12.15).

The quinoa crop year starts with the last rainsof January or February. During this time, fallowfields are overturned to allow rainfall to be cap-tured underground. This water is essential for theseeds to sprout come September/October, whenfarmers start to sow. This way, the quinoa benefitsnot only from the rains that come from Novemberto February but also from the previous rainy sea-son. Therefore, each field of quinoa uses two rainyseasons’ worth of rainfall (Fig. 12.16).

Farmers today rely on both natural indicatorsand modern technology, such as meteorologi-cal reports, to time the sowing. If planted tooearly, the quinoa will sprout but quickly run

Fig. 12.16 Quinoa emerging before first rains. Photo credit:Diego Nuñez de Arco.

Fig. 12.17 Quinoa field prepared with tractors. Photo credit:Diego Nuñez de Arco.

out of water and wither. The flowering of cer-tain bushes and cacti, the presence of lizards,scorpions, and where birds lay their eggs aresigns still used by farmers to predict frost orrain and serve to determine the types of seedsand the best locations in each field for plantingthem.

Today, most farmers hire tractors to assistin the overturning of lands and in sowing(Fig. 12.17). This is a major departure fromtraditional practices as Efigenia mentions in herinterview. The use of tractors has benefits andalso drawbacks, including soil erosion because ofthe strong winds in the highlands. Efigenia andagronomists in Bolivia point to the importanceof maintaining live barriers against the wind.These indigenous “tholas” (short bushes) seemto be as important as the llamas that feed on


them. For millennia, llamas have had a symbioticrelationship with quinoa. They provide whatis widely recognized by all quinoa farmers inBolivia as the very best of fertilizers. Most quinoafarmers will apply llama manure on their fields atleast once every 3 years.

LIVING WELL, REVERSED MIGRATION,AND CULTURAL IDENTITY

The following excerpts from interviews illustratehow farmers view their success and their hopes for“living well,” which, as Willy Choque explains,is synonymous to the farmers with sustainabledevelopment.

We have been working with some commu-nities on defining first of all what it meansto ‘live well.’ We are using ‘living well’ as adevelopment paradigm coming from withinthe communities. We have begun by realizingthat our communities did not understandthe meaning of sustainable development, forexample. But it’s easier (for the growers) toconceptualize or understand ‘living well.’Living well is in our ancestral languages:Aymara, Quechua, Guaraní. It’s easier fora producer to define what it is to live welland according to that define how he wants toimprove his life.

Willy Choque, Agronomist with the University of Oruro,during an interview for Shared Interest documentary, October

2013.

Now you can see (the impact) in the coun-try. I think it’s an improvement in all thefamilies, I think it is, that they start to buymotorcycles, they buy their jeeps, trucks,they have solid houses, comfortable families.I think it’s success that mother earth hasgiven us, to the region. Thanks to quinoa Ithink we in this region are not migrating.Before there was a lot of migration, andall those fellows who had migrated arecoming back. So I think that quinoa is inthe right place, and it’s important. It’s alsoimportant that this country is beginning to

consume more and more quinoa than before.Now there is no more discrimination. Nownobody says ‘I don’t eat quinoa’.

Alfredo Perez, President of Chamber of Quinoa Producersfrom Potosi (CADEQUIR) (Fig. 12.18)

The producer is very excited with the highprices of quinoa at this moment, and they arebuying a lot of things: houses, transportation;they have more comfort, their children aregoing to better schools, and they are learn-ing to use their money on other things, onliving well.

Danny Mamani, Agronomist and Representative of theQuinoa Producer Association Sumaj Juira

Living well, for me, means not only havingmachines. It means having a good house,good nutrition, good clothes, education,good health, that’s for me ‘living well’. Sothat’s the aim. And to raise a family. Havingthe opportunity for the children to study.

Efigenia Encinas, Representative of Sumaj CamañaAssociation of Women Farmers

What has been another valuable impact ofquinoa is that community ties are also strength-ening as producers return to their communities:

When people leave the communities, thechildren little by little lose their culturalidentity: their language, their dress, theirnutrition, etc. But now that people are backin their communities, all this culturalidentity is alive. If there are people in thecommunities, the culture is alive.

Willy Choque, Agronomist with the University of Oruro,during an interview for Shared Interest documentary, October

2013

Quinoa production contributes to socialcohesion as people return to their commu-nities and accept the responsibilities thatthese impose upon them. They participatein community events. The canvas of societyis woven.

Pablo Laguna, in “Is the commercialization of quinoa asnegative as it is being said to be?” April 7, 2013, La Razon

newspaper


It is evident that much good has come toBolivian quinoa growers through the develop-ment of the quinoa market. It is to be hoped thatthis impact will continue to expand as growersincrease acreage and improve their yields, marry-ing their traditional knowledge and productionpractices with modern adapted technologies.

OPPORTUNITIES FOR THE BOLIVIANFARMER

At the conference (International QuinoaResearch Symposium At Washington StateUniversity, August 12, 2014), there wastalk of creating a special brand for Andeanquinoa, a little like the special recognitiongranted to other traditional foods, like Bor-deaux wine. This brand would be top-qualityquinoa, and consumers might also be willingto pay extra for it, just because it would bequinoa from the land and the communitiesthat safeguarded it for thousands of years.

“Can Quinoa Farming Go Global Without Leaving AndeansBehind?” by Dan Charles for National Public Radio

The year 2014 will mark the entry into themarket of quinoa from nontraditional origins andmass agriculture. Already quinoa is being plantedsuccessfully in the United States (Pacific North-west and Colorado), Canada (Saskatchewan),Western Australia, France, and India, to name afew. Peru is also increasing their farming at sealevel along its coast, with outstanding yields thattriple those obtained by smallholder farmers inBolivia. Moreover, large producers have a distinctadvantage: the food supply chain relies on futurecontracts from reliable sources. For example,large food manufacturers who use quinoa as aningredient in their cereal (and this may be lessthan 5% of the total ingredients used) seek to havetheir purchase volumes and prices fixed for a year.In the current quinoa supply chain, this is verydifficult because quinoa comes from thousands ofsmallholder farmers, who do not release all theirproduct at once, so that supply trickles into theprocessing plants. Exporting quinoa-processing

plants are the source of purchase contracts andare currently the suppliers to the market. Theissue with these processing plants is that they canonly assure prices on what inventory they hold atthe moment. This inventory is limited by theirability to purchase quinoa stocks and processthese stocks. The largest of quinoa-processingplants in the world can process 25 containers(500 tons) per month and their working capital islimited to 60 containers (1,200 tons).

Commodity traders in the quinoa supply chainplay the important role of aggregating the sup-ply from multiple quinoa exporters, assuring therequested 6-month to 1-year-long contracts withfood manufacturers. To date, they have played acrucial role in the growth of the quinoa market.

As the market for quinoa grows, demand willflow toward sources that can offer the forwardcontracting that other mature commodities offer.Commodity traders who until today absorbedsome of the inefficiencies of the current supplychain will favor the sources that are more reliableand pose lower risk.

The lives of the Bolivian farmers have beendramatically improved and no one wishes them toreturn to a state of poverty. To prevent this situa-tion, many stakeholders agree that a niche shouldbe created for the smallholder farmer (Fig. 12.18).This niche would seek to decommoditize theirquinoa, giving it distinguishing marks such asFair Trade, Appellation of Origin, and CertifiedOrganic.

Fig. 12.18 Typical quinoa farmer family in the Potosí regionof Bolivia. Photo credit: Vitaliy Prokopets.


We are obtaining Fair Trade Certificationswith the organizations we work with, sowe can in the future protect our producersunder two main premises: organic quinoaand fair trade. What is coming in the futureis strong competition from other emergingcountries in quinoa production, but we thinkthat the actions Andean Naturals and Jacha

Inti are taking on behalf of our producers --because we consider them our family -- willprotect them. In those times of crisis, theywill continue to receive a fair price for thequinoa they produce, and all their work willbe acknowledged.

Yeris Peric, Jacha Inti Quinoa Processing Plant Agronomist,October 2008

Index

abiotic stress see environmentacreage increases in South America,

213–15, 217, 221–4Africa, 161–71

challenges and considerations forfuture research, 169–70

goals of breeding, 164–9introduction into, 161–3, 164

agro-food variables (germplasmcollections), 143–4

documentation, 147–8see also food security

agroecology see ecologyagroecosystems and insect pests, 63, 64,

77, 78, 79, 80agromorphology see morphological and

agromorphologicalcharacteristics

agronomicsAfrica, 170South America, 30–2

albumin, 194, 195allogamy see out-crossingallotetraploid, 6, 29, 97, 109, 111, 112,

114Altiplano (Andean highland

plateau/plain of Bolivia andPeru), 30, 34, 47–62

ecotype, 5, 19, 26, 29, 49, 87–8, 90,92, 99, 126

in temperate regions (incl. NorthAmerica), 177, 178

sowing, 35–6yields, trends, 47–62

Amachuma cultivar, 97Amaranthaceae, 5, 28American and European test of quinoa,

90, 93, 99amino acids, 193–4

essential, 4, 143, 163, 194, 195, 205


amplified fragment lengthpolymorphisms, 113, 117,119

ANAPQUI (National Association ofQuinoa Producers), 40, 215

Andes (of South America incl. Boliviaand Peru), 19–20, 34

breeding, 87–107genebanks, 128–30highland plateau/plains see Altiplanohistory, 19–20, 26valley ecotype see valley quinoa

animal forage and feed, 186–7anthesis, 37–8, 96, 100anthocyanins, 76, 204, 205antifungal activity, saponins, 203anti-inflammatory effects of saponins,

203antinutritional factors, 202–3Apelawa cultivar, 97aphids and Aphidae, 66–7

Malawi, 169North America, 184–5South America, 66–7

APQC (Association of Producers ofQuinoa and Camelids), 217,220

APROCAY, 220archeological studies, 2, 26, 101, 174Argentina, 116, 118, 119, 120

distribution, 128genetic structure in Northern

regions, 118germplasm, 91insect pests, 64, 65, 71, 77seed genebanks, 130

arid regions/conditions in SouthAmerica, 27, 32

Chile, reintroduction after localextinction, 20–1

see also droughtAscochyta, 184assassin bugs, 72association mapping, 113Association of Producers of Quinoa and

Camelids (APQC), 217, 220Atriplex, 10

A. hortensis, 102autogamy (self/auto-pollination), 6, 27,

96, 97autopollination (self-pollination;

autogamy), 6, 27, 96, 97aynokas, 16, 29, 89

backcrossing, 102Baer, 98, 130, 180, 181–2barley, chemical/nutrient composition,

194vitamins, 201

beet pests, 185behavioural strategies of insect pests,

73Bembeke (Malawi), 166bioactivity, 195–6, 203, 204–5biochemical strategies to resist stress

(incl. herbivory), 73biodiversity see diversityBiodiversity International (IPGRA;

International Plant GeneticResource Institute), 131, 133,141

biological control of insect pests, 63–85biological value, 4

industry and consumer requirements,95

biomechanical strategies to resist stress(incl. herbivory), 73

biotic stress and threats, 38–9resistance to, 94see also diseases; pests

227

228 Index

birds, 39, 94, 186see also poultry feed

Boliviaacreage increases, 213–15, 217,

221–4Andes see Altiplano; Andesbulk/mass selection, 101distribution in, 127farmers in

economic snapshot, 212–13opportunities, 225–6production practices/increased

acreage/thoughts onsustainability, 221–4

germplasm bank, 128, 130–58characterization and evaluation of

germplasm, 140–4current status, 132history and management, 130–2steps for management, 132–55utilization, 148–55

morphological variations, 91, 141–3poverty in, impact on, 217–21prices, 217PROINPA Foundation, 29, 88–9,

101, 126, 131, 132, 136, 148,151, 153

temperate regions (incl. NorthAmerica) and varieties from,176, 178

Bolivian Yungas (subtropical) ecotype, 5,19, 88, 90, 115, 127, 177–8

botany, 5–7, 26, 27–8breeding, 87–107

Africa, goals, 164–9germplasm collections and, 151–2goals, 92–7methods, 92–103

in genetic improvement, 96–103Brigham Young University (BYU), 103,

112bulk selection see mass selectionBunda (Malawi), 166

calcium, 202calcium oxalate glands, 27, 32Canada, 164, 173, 176, 193canola, fatty acids, 199Carabidae, predatory, 70, 71carbohydrate, 3

germplasm collections, 143see also sugar

carbon dioxide/H20 gas exchange andenvironmental stress, 10

carbon-13 values, 6cardiovasuclar disease (CVD), 200, 201,

203

carotenoids, 93, 95–6, 205β-caroyphyllene, 75casein, amino acids, 195centers of origin, 26, 28, 30, 34, 89, 116,

119, 126–7, 133centralized collection method

(germplasm samples), 133Centre for Plant Breeding and

Reproduction Research(CPRO-DLO) breedingprogram, 182, 183, 186

cereals, quinoa compared withbotany, 27chemical and nutrient composition,

193, 194lipid, 199phenolic acid, 204starch, 196vitamins, 200–1

cerros (steep slopes), 47, 51, 56, 57, 58chemical defences to pests, 73–6chemical fertilizer (inorganic fertilizer),

Africa, 169, 170Chenopodium (non-C. quinoa), 6, 19, 89,

116, 174, 183distinguishing characteristics, 90interspecific crosses/outcrossing

with, 102, 111–12, 186downy mildew resistance and, 183heat tolerance and, 174

as weeds, 185Chenopodium album, 111, 112, 117, 183,

184, 185Chenopodium ambrosioides, 28, 89, 117Chenopodium berlandieri, 6, 109, 111,

112crossing with, 111–12, 186downy mildew resistance, 183var. macrocalycium, 112

Chenopodium hircinum, 6, 19, 28, 89, 109,112, 113, 117

chicken feed, 187children in Africa, malnutrition, 162–3Chile

distribution, 127–8history in

expansion to southern latitudes in,20–1

reintroduction to arid regions afterlocal extinction, 20–1

lowland ecotype see lowland ecotypemorphological variations, 92temperate regions (incl. North

America) and varieties from,175–81

chlorophyll content and environmentalstress, 11

chloroplast photochemical reactions andenvironmental stress, 11

Choque, Willy, 224chromomycin A3, 110chromosomes, 109, 110, 111

polyploidy level, 97Chrysomelidae, 66Chrysopidae, 67

predator, 70, 71, 77CICA cultivar, 5, 6, 8–10, 11, 168climate change (incl. global warming), 1,

215yield in Southern Bolivian Altiplano

and projections of, 47, 48,52–4, 57, 59–60

see also environmentcoastal ecotype see lowland ecotypeCoccinellidae, 66

predatory, 70, 71, 77coconut oil, fatty acids, 199coeliac disease, 194–5Coipasa, 5, 49cold temperatures (and tolerance)

North America, 175–6South America, 33see also frost; hail

Coleoptera, 65, 66predatory, 71, 77

Colombia, 19, 30, 31, 34, 36, 115, 118,130, 161

distribution in, 127color

plant (germplasm collection), 142seed/grain, 28, 40, 87

breeding and, 87, 91, 95–6, 98,103

germplasm collection, 142industry and consumer

requirements, 95–6mutagenesis affecting, 103social use and, 152

Colorado, 102, 173, 176, 178, 179, 181,183, 184, 185, 186

San Luis Valley, 97, 173, 175combine harvesting

North America, 181South America, 39

commerce and industry, South America,40

requirements of, 95–6see also economics

commodity traders, 216, 225community training courses of varied

uses, 149–51conditioning of germplasm samples, 138conferences, 155, 156conservation strategies, 115

ex situ see ex situ collections

Index 229

in situ, 89, 120, 132, 149consumer requirements, 95–6Copa, Raúl Vera, 217Copitarsia sp., 64, 65, 77Coquimbo regions, 20–2core collections, 90, 116, 140, 152corn see maizecoronary heart disease, 200, 201CPRO-DLO breeding program, 182,

183, 186crop

cycle, 30, 35, 141insect pests and cropping systems and

crop management, 64, 79–80productivity, Southern Bolivian

Altiplano, 58water requirements, 37–8

cross-pollination see out-crossingculinary use

community training courses, 151US, 216

cultivars and varieties, 6–7, 88Bolivia, obtained through breeding,

152, 153Kenya, 167–9Malawi, 164, 165

growth performance, 165–6yield, 166, 167

nutritional content and, 4, 5see also genotypes

cultivation and productionAfrica, 161–71North America, 173–92, 173–92South America, 30–2, 34–41

Bolivian farmer’s costs, 212Bolivian farmer’s current

production practices, 221–4cultural practices, 37history, 2, 19–24, 26, 87–8

see also acreage; yieldscultural identity, 224Curi, Cesın, 215cytogenetics, 109–11

Danish varieties, 176, 177, 180, 183day length, 20

Africa, 168Kenya, 167

North America, 178days to maturity see maturitydecentralized collection method

(germplasm samples), 133, 136defences to pests, chemical, 73–6Denmark, 9, 164, 175, 178, 180, 181, 183

varieties (Danish) from, 176, 177,180, 183

density (sowing/planting) in temperateregions (incl. North America),179–81

depth of planting in temperate regions(incl. North America), 180

descriptors for collections, 116, 140, 141diet

animal, 187human, 195, 196, 198–9, 201

African, 161, 162, 169see also nutritional deficiencies;

nutritional valueDiptera, 97

as parasitoids of pests, 71as pests, 66, 70

diseaseshuman, quinoa’s beneficial effects,

200, 201, 203, 205quinoa

fungal, 39, 90, 94, 183–4Malawi, 169

dissemination of information on use,153–4

diversification, 19–24diversity (biodiversity), 115–18, 126

Bolivian germplasm collection, 144centers and subcenters, 19, 115,

126–7genetic, 29, 88, 89, 115, 116, 117–18,

119–20, 126, 127, 134germplasm, molecular markers, 92molecular markers and, 92, 117, 119phenotypic, 115–16

DNApolymorphisms see polymorphismsrepetitive see repetitive DNA

sequencesequence evidence for genomic

origins, 112–13documentation (germplasm samples),

134, 147–8domestication, 6

Andean, 26–7downy mildew (Peronospora farinosa and

P. variabilis), 38, 90, 94, 126,183–4

drought (and tolerance), 7–12in Malawi, quinoa as alternative crop

for regions prone to, 163in South America, 32–3

Southern Bolivian Altiplano, 52,54–5

in temperate regions (incl. NorthAmerica), 174–5

see also arid regionsDurable Resistance Project in the

Andean Region (PREDUZAproject), 101, 103, 131

ecdysteroids, 75ecology (agroecology)

adaptation to different ecologicalzones

Africa, 163–4South America, 7

biological pest control and, 77–80Malawi, 16, 164–6, 170South America, 5, 26, 30

economics, 211–26see also commerce and industry

ecotypes, 5, 19, 26, 28, 87–8, 90–1,126–7

temperate regions (incl. NorthAmerica)

cold tolerance and, 175–6variety selection and, 177–8

see also specific ecotypesEcuador, 26, 29, 30, 31, 34, 94, 118, 135,

184acreage increases, 213, 217distribution, 127germplasm, 89, 91

education, 155, 156electronic documentation of germplasm,

147, 148β-elemene, 75emasculation, 100Encalilla, 5Encinas, Efigenia, 221, 222, 223, 224England, 99, 176, 180, 181, 185entomopathogens, 72entomophagous insects, 65–72, 76–80environment (incl. climate)

Kenya, 166Malawi, 164–5nutritional content and, 4stressful, incl. abiotic factors (and

tolerance/resistance), 7–12, 22,27, 32–4, 94–5

North America, 173–7South America, 27, 32–4, 54–5

essential amino acids, 4, 143, 163, 194,195, 205

Europe, 164, 178, 180, 181–2, 184market, 215, 221see also American and European test

of quinoaEurysacca melanocampta and E. quinoae

(quinoa moth), 64, 65, 77, 80,184, 185

ex situ (germplasm and genebank)collections, 29, 88–92, 120,125–60

Andean Region, 128–30Bolivia see Boliviacharacterization and evaluation,

140–4

230 Index

ex situ (germplasm and genebank)collections (continued)

core collections, 90, 116, 140, 152descriptors, 116, 140, 141history and evolution, 134–6multiplication see multiplicationPeru (Illpa), 7, 29, 89, 128–30samples see samplessteps for ex situ management, 132–55utilization, 148–55

experimental sites in Kenya, 166

fairs, 153, 154faldas (gentle slopes in piedmonts), 47,

51, 52, 56farmers

African, maize vs. quinoa, 169Bolivian see Boliviabreeding requirements, 92–5participation by see participation

fatty acids, 3, 199–200unsaturated, 143, 199, 200, 201see also lipid

feed, animal, 186–7fertilizer, 36–7

Africa, inorganic/chemical, 169, 170organic see organic quinoaSouth America, 31, 36–7temperate regions (incl. North

America), 178–9ferulic acid, 204fiber, dietary, 198–9field plots (for germplasm

multiplication), 145–6flavonoids, 22, 76, 204–5flax, fatty acids, 199flower types, 96

see also inflorescenceflowering, 27–8, 31, 100

anthesis, 37–8, 96, 100fluorescence in situ hybridization

(FISH), 110, 111, 112folate, 3, 201Food and Agricultural Organization

(FAO)Africa and, 163ecotypes, 26nutritional content, 3, 4, 5, 22, 194,

195promotion by, 22, 25, 163

food security in Africa, 161–2see also agro-food variables

forage crop, quinoa, 186–7freeze–thaw stability of starch, 198frost

Africa, 163, 164North America, 175–6

South America, 26, 27, 33, 48, 49, 50,51, 55, 59, 60

fructose, 198fruit, 6, 28, 87functional properties, 196fungal diseases and pathogens, 39, 90,

94, 183–4see also antifungal activity

gallic acid, 204gas exchange and environmental stress,

10gelatinization temperature of starch,

197–8genebanks see ex situ collectionsgenera, crosses between, 102, 117generalist behavioral strategies of insect

pests, 73genetic diversity, 29, 88, 89, 115, 116,

117–18, 119–20, 126, 127, 134genetic maps, 103, 113, 114genetic markers and molecular markers,

103, 113–14, 117diversity and, 92, 117, 119germplasm collection, 144

genetic resources, collection see ex situcollections

genetics (in general), 5–7, 28–30, 96,109–23

breeding and, 96–103molecular, 109–23

genomeDNA sequence evidence for origins,

112–13structure, 109–11

genotypes, 93KASPar™ genotyping chemistry,

114Kenya, performance, 168–9Malawi, performance, 166, 167nutritional content and, 4saponins and, 4see also cultivars and varieties;

ecotypesgeographical distribution

(phytogeography), 30, 127–8,161

germplasm collections, 136outside South America, 136, 161

germinationfor germplasm collection

analysis, 139initial samples, 138monitoring of samples, 140, 145

postharvest studies, 40germplasm

Argentina, 91

collections see ex situ collectionsdiversity, molecular markers, 92ectotypes see ecotypesforeign, introduction, 99multiplication see multiplicationstorage, 138–40utilization, 148–55

gliadins, 194, 195global warming see climate changeglobulins, 194, 195glucose, 198glutelins, 194, 195gluten and glutenins, 194, 195glycosylated secondary metabolites see

saponinsgrain see seedgrassy weeds in temperate regions (incl.

North America), 185Graziano da Silva, José, 211Greece, 90, 93, 177, 181greenhouse (for germplasm

multiplication), 145–6greenhouse gases, 1

see also climate changegrowth

habit, germplasm collection, 142performance

Kenya, 167–9Malawi, 165–6

gynomonoecy, 106

hail, 34halophytes, 7, 32harrowing, 37

temperate regions (incl. NorthAmerica), 185

harvestingNorth America and other temperate

regions, 181–2sprouting before, 182–3

South America, 39–40Bolivian farmer’s costs, 212mechanized, 39, 95

heart disease, coronary, 200, 201heat tolerance, North America, 173–4,

176, 177, 187height of plant required by farmers, 93Hemiptera, 66

predator, 70, 71herbivorous insects see insectsherbivory-associated molecular patterns

(HAMPs), 76heterochromatin, 110heterosis, 102–3highlands

Andean see AltiplanoMalawi, 164–5

Index 231

historical perspectives (cultivation), 2,19–24, 26, 87–8

Bolivian germplasm collection,130–2, 134–6

see also originshoeing, inter-row, temperate regions

(incl. North America), 185Holland (Netherlands), 178, 180, 182,

187hot temperatures, tolerance in North

America, 173–4, 176, 177, 187Huayllas, Eufraen Huayllas, 220–1humidity

frost and, 176Malawi, 164storage and, 138, 139

hybrid(s)identifying, 117sterility, 102vigor, 102–3

hybridization, 99–102Hymenoptera, 67

parasitoid, 70, 71

IBTA (Bolivian Institute of AgriculturalTechnology), 131, 135, 151

identification of germplasm sample,correct, 140

Illpa (Puno in Peru), germplasm bank,7, 29, 89

in situ conservation, 89, 120, 132, 149Incas, 2, 26

Spanish conquest, 2, 25India, 92, 94, 99, 116, 183individual (pedigree) selection, 98,

101combined mass and, 102

industry see commerce and industryinflammation and saponins, 203inflorescence, selfing, 98information (germplasm), 147–8

dissemination, 153–4INIA see Institute of Agricultural

ResearchINIAF (National Institute for

Agricultural and ForestryResearch), 29, 89, 128, 131,132, 136

insects, 64–72beneficial (attacking phytophagous

insects), 65–72, 76–80as pests (herbivorous/phytophagous

insects), 63–86, 94Malawi, 169natural enemies, 63–86temperate regions (incl. North

America), 184–5

insoluble fiber, 198Institute of Agricultural Research

(INIA)Chile, 130, 135Peru, 89, 128, 130

INTA (National Institute ofAgricultural Technology), 130

inter simple sequence repeats (ISSR),144, 148

intercropping and insect pests, 79intergeneric cross, 102, 117intergenic spacer (IGS), NOR, 112International Plant Genetic Resource

Institute (IPGRI), 131, 133, 141International Quinoa Research

Symposium (2014), 225International Year of Quinoa, 22, 163,

211interspecific cross see Chenopodium

(non-C. quinoa)inverted sugars, 143, 144IPGRA (International Plant Genetic

Resource Institute), 131, 133,141

irrigationAfrica, 170South America, 37–8temperate regions (incl. North

America)heat stress and, 174saponins and, 186

isoflavones, 22, 205Italy, 90, 93, 177, 182

jasmonic acid, 75

Kabete Field Station, 166kaempferol, 73, 76, 205Kanckolla, 176, 178KASPar™ genotyping chemistry, 114Kenya, 166–9

La Pazgermplasm collection, 131, 136training courses, 151

labor costs for a Bolivian farmer, 212Laguna, Pablo, 224land use changes and yield in Southern

Bolivian Altiplano, 47, 48, 51,58, 60

see also acreagelandscape

natural pests and, 63yield in Southern Bolivian Altiplano

at landscape level, 47, 49, 51,56–7, 59, 60

latitude, 178

Bolivia, 136Chile, Southern, 20Kenya, 167

leaves, 27, 31succulence, and environmental stress,

11lectures and talks, 155, 156Lepidopteran pests, 39, 65, 67, 71, 75,

77see also moths

life cycle, farmers’ requirements, 94light saturation point and environmental

stress, 11–12limonene, 75linkage maps, 113–14linoleic acid (LA), 3, 75, 200α-linolenic acid (ALA), 3, 199, 200lipid (fat) content, 2–3, 199–200

germplasm collections, 143living well, 224–5llamas, 35, 80, 223–4

dung/manure, 31, 35, 59, 212, 222,224

local scale, time variation of yield inSouthern Bolivian Altiplano,54–6

lodging, 169resistance to, 94, 169

lowland (sea level) ecotype, Chilean, 5,19, 20, 26, 88, 90, 117, 119, 127

in temperate regions (incl. NorthAmerica), 175, 176, 177, 178,181

Lygaeidae, predatory, 70, 72Lygus, 184, 185

McKnight Foundation and projects,101, 103, 131

MAGDER (former name for MDRyT;Ministry of Rural Developmentand Land), 131

maize (corn)in African diet, 169chemical/nutrient composition,

194fatty acids, 199phenolic acid, 204protein, 195

Malawi, 163, 164–6pests and diseases, 169

male sterility, 97, 101malnutrition in Africa, 162–3maltose, 198Mamani, Danny, 224manual documentation of germplasm,

147, 148, 157

232 Index

manual labour, 77Africa, 170South America

harvesting, 39sowing/planting, 35, 223

marker-assisted selection, 103, 113see also genetic markers and

molecular markersmarketing, 211–26mass (bulk) selection, 98, 101

combined individual and, 102maturity, days to/period to

Kenya, 167, 168Malawi, 166temperate regions (incl. North

America), 175, 181–2MDRyT (Ministry of Rural

Development and Land-formerly MAGDER andMDRAyMA), 131

mechanizationNorth America (and other temperate

regions), harvesting, 181South America, 48, 72, 221

harvesting, 39, 95sowing, 34, 35

microsatellites (simple sequencerepeats), 103, 113, 117–18, 119,144, 148

migration, reverses, 224–5mildew, downy (Peronospora farinosa and

P. variabilis), 38, 90, 94, 126,183–4

minerals, 201–2Ministry of Rural Development and

Land (MDRyT; formerlyMAGDER and MDRAyMA),131

Miridae, predatory, 70, 72mixed cropping and insect pests, 79mobile DNA elements, 111moisture content of seed (in germplasm

collection)initial, 139reduction, 139

molecular genetics, 109–23see also genetic markers and

molecular markersmolluscicidal activity of saponins, 203monoculture, South America, 31, 79monophagous behavioral strategies of

insect pests, 73monounsaturated fatty acids (MUFA),

199, 200morphological and agromorphological

characteristicsdocumentation of germplasm

collections, 147

genetic diversity and, 116mechanized harvesting and, 95variations, 91

germplasm collections, 141–3moths

quinoa (Eurysacca melanocampta andE. quinoae), 64, 65, 77, 80, 184,185

ticona complex, 38, 64, 65, 77multiplication of germplasm, 144–6

preliminary, 136–8mutagenesis, 103

Nabidae, predatory, 70, 72Nairobi, 166, 167, 168National Association of Quinoa

Producers (ANAPQUI), 40,215

National Institute for Agricultural andForestry Research (INIAF), 29,89, 128, 131, 132, 136

National Institute of AgriculturalTechnology (INTA), 130

National System of Genetic Resourcesfor Food and Agriculture(SINARGEAA), 131

natural enemies and chemical responsesto insect herbivory, 63–85

Neotropical region, insect pests, 64, 65,68, 72, 77

Netherlands, 178, 180, 182, 187Neuroptera, 67

parasitoid, 70, 77nitrogen (N) fertilization, 36

temperate regions (incl. NorthAmerica), 178–9

nontranscribed spacer (NTS) regions of5S rRNA gene, 112

NOR intergenic spacer (IGS), 112North America, 173–92nutritional deficiencies in Africa, 162–3nutritional value/properties, 2–5, 163,

193–216Africa and, 163FAO on, 3, 4, 5, 22, 194, 195germplasm collections, 143–4

documentation/information,147–8, 153

see also diet

oat, chemical/nutrient composition, 194Olav, 180oligophagous behavioral strategies of

insect pests, 73olive oil, fatty acids, 199organic quinoa (using organic fertilizer),

31, 36–7, 80

Bolivian prices, 217temperate regions (incl. North

America), 179origin(s), 19–24, 161

centers of, 26, 28, 30, 34, 89, 116,119, 126–7, 133

orthodox vs. recalcitrant seed behavior,132

Oruro, Technical University (UTO), 88,128, 135

out-crossing (cross-pollination;allogamy), 27, 96–7, 117, 119,186

in germplasm collections, reducing,146

intergeneric, 102, 117interspecific/with allied taxa see

Chenopodium (non-C. quinoa)see also hybrids

packing of germplasm samples, 138,139–40

pampas (flat plains), 47, 48, 51, 52, 56,58, 59, 112

panicle shape and density (germplasmcollection), 142

parasitoids, 65, 70, 71, 76–7parents, selection of, 99–100participation (farmers and other

stakeholders)in breeding, 98–9in evaluation, 148–51

Patacamaya, 5, 7, 88, 93, 102, 131, 135,151, 153

pedigree (individual) selection, 98, 101Perez, Alfredo, 224Peric, Yeris Peric, 226Peronospora farinosa and P. variabilis

(and downy mildew), 38, 90, 94,126, 183–4

Peruacreage increases, 213, 217Andes see Altiplano; Andesgermplasm bank, 7, 29, 89, 128–30morphological variations, 91prices, 217temperate regions (incl. North

America) and varieties from,178, 181

pestsinsect see insectMalawi, 169non-insect, 39

birds, 39, 94, 186temperate regions (incl. North

America), 184–5PGRFA (Plant Genetic Resources for

Food and Agriculture), 125

Index 233

pHprotein content and, during

processing, 195soil, South America, 31

Pharastrepia sp. (thola), 80, 223phenolic compounds (incl. phenolic

acid), 76, 204phenological stages, 30, 32, 33, 34

predators of insects and, 77phenotypic diversity, 115–16phenylalanine ammonia lyase, 76phosphorus (P) fertilization

North America, 179South America, 36, 179

photoperiod (and photoperiodsensitivity), 6, 33–4, 96, 178

Africa, 168Kenya, 167, 168

photosynthesis and salinity, 9–11phytic acid, 76, 202phytoecdysteroids, 75phytogeography see geographical

distributionphytophagous insects see insectspig feed, 187Plant Genetic Resources for Food and

Agriculture (PGRFA), 125planting see sowing/plantingplateau, Andean see Altiplanoploidy level, 97plot scale, time variation of yield in

Southern Bolivian Altiplano,54–6

pollen exchange (in germplasmcollections), prevention, 146

pollinationartificial, 100, 101cross see out-crossingself-/auto- (autogamy), 6, 27, 96, 97

polyculture, 79polymorphisms (DNA), 113, 117

amplified fragment length, 113, 117,119

single-nucleotide, 103, 112, 113–14polyphagous (generalist) behavioral

strategies of insect pests, 73polyphenol, 76, 204polyploidy level, 97polysomaty, 111polyunsaturated fatty acids (PUFA),

199, 200Pomacea canaliculata, 203potassium (K), 37

applicationNorth America, 179South America, 36

poultry feed, 187

poverty, Bolivia farmers lifted out of,217–21

precipitationChilean arid areas, 21, 22Southern Bolivian Altiplano,

projections, 48, 49–50, 58see also hail; rainfall

predatorsof insect pests, insects as, 70, 71–2,

75, 76–7on quinoa see pests

PREDUZA project, 101, 103, 131prices, 215, 217, 221, 225

rising/higher, 164, 211, 212, 213,217, 220, 221, 224

production see acreage; cultivation;yields

productivity (crop/plant), SouthernBolivian Altiplano, 58

PROINPA Foundation, 29, 88–9, 101,126, 131, 132, 136, 148, 151,153

prolamins, 194, 195proline and drought resistance, 32promotion (of use), 153–5protease inhibitors, 75, 202protein (content and composition), 4, 5,

193–6germplasm collections, 143industry and consumer requirements,

95pseudograins and pseudocereals, 27, 28,

174pulse-reserve model, 58puna, 49, 118pyridoxine, 201

quality of life, 224–5quality traits and genetic diversity, 116quercetin, 73, 76, 204, 205quinoa moth (Eurysacca melanocampta

and E. quinoae), 64, 65, 77, 80,184, 185

radiationmutagenesis using, 103tolerance to, 33

rainfallAfrica, crops fed by, 170waterlogging and, 182

Real (Royal Quinoa), 5, 30, 127, 142, 152recalcitrant vs. orthodox seed behavior,

132Regalona, 20Regalona-Baer, 117, 182regeneration (rejuvenation) of

germplasm, 125, 144–5, 145,145–7

rejuvenation (regeneration) ofgermplasm, 125, 144–5, 145,145–7

repetitive DNA sequence, 110–11microsatellites (simple/single

sequence repeats), 103, 113,117–18, 119, 144, 148

reproduction, 96allogamous see out-crossingautogamous (self-/auto-pollination),

6, 27, 96, 97respiration and environmental stress, 12retail packs, 216retrotransposons, 111riboflavin, 201ribosomal RNA genes, 110, 111, 112rice, chemical/nutrient composition,

194phenolic acid, 204protein, 195vitamins, 201

RNA, ribosomal, genes, 110, 111, 112rodent pests, 39root/shoot ratio and drought resistance,

32rows

hoeing between, 185spacing, 179–80

Royal Quinoa (Real), 5, 30, 127, 142, 152rural areas

education, 156promotion and dissemination, 153,

154rutin, 73, 76rye, chemical/nutrient composition, 194

amino acids, 195

Sajama cultivar, 4, 101salar ecotype, 5, 19, 20, 26, 87–8, 90,

126–7temperate regions (incl. North

America), 183salinity and salt tolerance, 7–12

halophytes, 7, 32North America (and other temperate

regions), 176South America, 27, 32

salivary secretions of insects, 75–6salt flats

Bolivian farmers’ economics, 217–21ecotype see salar ecotype

Salt Overly Sensitive 1 (SOS1), 112–13salt tolerance see salinitysamples (germplasm)

characterization and evaluation,140–4

collection (sampling), 133–4

234 Index

samples (germplasm) (continued)sources, 134strategy, 134

conditioning, 138documentation, 134, 147–8germination of initial sample, 138handling, 134handling and documentation, 134packing, 138, 139–40seed number per, 137–8size, monitoring for, 145

San Luis Valley (Colorado), 97, 173, 175saponins, 3–4, 22, 75, 96, 186, 202–3

beneficial properties, 202–3bird predation and, 94, 186industry and consumer requirements,

95removal, 40temperate regions (incl. North

America), 186saturated fatty acids, 199–200Sclerotium rolfsii, 198sea level ecotype see lowland ecotypesecondary metabolites (SMs), 3, 72, 73,

74–6glycosylated see saponins

seed (and grain)color see colorexchanges, 20, 117, 118, 119–20fertilization affecting composition of,

179filling, 34, 167, 174, 178, 179

early, 31late, 31

genebanks see ex situ collectionsgermination see germinationharvest, South America, 39–40moisture content see moisturenumber/quantity (in germplasm

collection), 137–8monitoring, 145

nutritional content, 2–5amino acids, 194

orthodox vs. recalcitrant behavior,132

packing of samples, 138, 139–40saponin see saponinsize/diameter

germplasm collection, 142industry and consumer

requirements, 96sowing see sowingyield see yieldsee also single-seed descent

seed coat, saponins in, 3, 4, 22selection (in breeding), 98

bulk or mass see mass selection

individual/pedigree see individualselection

marker-assisted, 103of parents, 99–100

self-pollination (autopollination;autogamy), 6, 27, 96, 97

selfing of inflorescence, 98sexual reproduction see reproductionside-dishes, 216silage, 187simple (single) sequence repeats

(microsatellites), 103, 113,117–18, 119, 144, 148

SINARGEAA (National System ofGenetic Resources for Food andAgriculture), 131

single-nucleotide polymorphisms(SNPS), 103, 112, 113–14

single-seed descent, 102single-sequence (simple-sequence)

repeats (microsatellites), 103,113, 117–18, 119, 144, 148

social use, 152–5sodicity, 177soil conditions

South America, 31–2Southern Bolivian Altiplano soil

water storage, 52–4temperate regions (incl. North

America)fertilization affected by, 179planting affected by, 180

soluble fiber, 198SOS (Salt Overly Sensitive 1), 112–13South America, 25–45

acreage increases, 213–15, 217,221–4

agroecological conditions andregions, 5, 26, 30

agronomics, 30–2Andes of see Andesbreeding, 87–107cultivation see cultivationgeographical distribution see

geographical distributionhistory, 2, 19–24, 26, 87–8

Spanish conquest, 2, 20–1, 22, 25,26, 88, 112, 161

mechanization, 48, 72, 221monoculture, 31, 79pest control, 63–85see also specific countries and regions

sowing/plantingSouth America, 34–6, 223temperate regions (incl. North

America), 179–81soy, amino acids, 195spacing, row, 179–80

Spanish conquest of South America, 2,20–1, 22, 25, 26, 88, 112, 161

specialist behavioral strategies of insectpests, 73

species of Chenopodium, non-quinoa seeChenopodium

sprouting (preharvest), temperateregions (incl. North America),182–3

stalk strength, 94see also lodging

Standard for Genebanks, 137, 138, 139,140, 145, 146

Standardized PrecipitationEvapo-transpiration Index,Southern Bolivian Altiplano,49–50, 52, 53, 57

starch (and starch granules), 3, 196–8germplasm collections, 143

stearic acid, 199, 200sterility

hybrid, 102male, 97, 101

stomata and environmental stress, 8, 9,10, 11

storage of germplasm, 138–40subtropical (Bolivian Yungas) ecotype, 5,

19, 88, 90, 115, 127, 177–8sugar, 198

inverted, 143, 144see also carbohydrate

supply and demand, 213–15sustainability, woman farmer’s thoughts

on, 221–4Swaeda foliosa, 89, 102swathing, 181Sweden, 175, 186swelling power of starch, 198Syrphidae, predatory, 70, 185systemin, 75

talks and lectures, 155, 156taxonomy, 27–8Technical University of Oruro (UTO),

88, 128, 135telomeric repeat, 110–11temperate regions incl. North America,

173–92temperature

drought resistance and, SouthAmerica, 33–4

gelatinization (of starch), 197–8germination and, temperate regions

(incl. North America), 180–1processing, effects on protein, 195see also cold temperatures; heat

tolerance

Index 235

terpenoids, 74–6tetraploid taxa, crossability with other

species of see out-crossingthola (Pharastrepia sp.), 80, 223threshing, South America, 39ticona complex (moths), 38, 64, 65, 77Titicaca, Lake, 5, 27, 28, 29, 88, 90, 115,

119, 131, 215community training courses of varied

uses, 149–51Titicaca cultivar, 9, 166, 177tocopherol (vitamin E), 3, 201Toralapa Centre (INIAF), 89, 128, 132towns see urban areastractors, 223training courses of varied uses, 149–51transpiration and environmental stress,

10transposons, 111Tucuman (Argentina), insect pests, 65,

77

UMSA (Universidad Mayor de SanAndres), 27, 88, 128, 131

United Nations’ International Year ofQuinoa, 22, 163, 211

United States, 89, 96, 225market, 211, 215, 215–16, 221

unsaturated fatty acids, 143, 199, 200,201

urban (town) areaseducation, 156promotion and dissemination, 153,

154uses/utilization, 186–7

alternative (to human foodstuff),186–7

germplasm, 148–55UTO (Technical University of Oruro),

88, 128, 135Utusaya variety, 9, 183Uyuni, 5, 47, 49, 99

valley quinoa, 5, 19, 26, 30, 88, 126in temperate regions (incl. North

America), 175, 177, 178varieties see cultivars and varietiesvegetative period/cycle, 6, 8

drought and, 175germplasm collection, 142–3low temperatures and, 33

ventilation, 39–40vigor, hybrid, 102–3viruses, entomopathogenic, 72vitamins, 200–1

vitamin E (tocopherol), 3, 201volatile compounds, 76, 80

antiherbivore, 73, 75

walnut, fatty acids, 199Washington state, 173, 174, 175, 178,

181, 182, 183, 184, 185, 186Washington State University (WSU),

164, 174International Quinoa Research

Symposium (2014), 225water

South Americacrop requirements, 37–8Southern Bolivian Altiplano soil

water storage, 52–4stress, 33, 34

see also arid regions; drought; frost;hail; humidity; irrigation;moisture; precipitation; rainfall

water (H2O)/CO2 gas exchange andenvironmental stress, 10

water filling, 144waterlogging, 180, 182–3weeding

South America, 37temperate regions (incl. North

America), 185–6wheat, chemical/nutrient composition,

194fatty acids, 199phenolic acid, 204protein, 195vitamins, 201

windpollination by, 97protection from, 223

winter crop in US, 175women farmers production practices,

221–4

yields (grain)germplasm collection, 143higher, required by farmers, 92–3Kenya, 167–9Malawi, 166, 167Southern Bolivia Altiplano, trends,

47–62temperate regions (incl. North

America), 181–2Yungas (subtropical) ecotype, 5, 19, 88,

90, 115, 127, 177–8

(a) (b) (c)

Plate 3.1 (a–c) Examples of quinoa plants in farmer’s field showing the vast diversity of colors and the forms of panicles(Province of Omasuyos, bordered to the south and west by Lake Titicaca, Bolivia) (Del Castillo and Winkel, IRD – CLIFA, 2002–2008).


(a)

(c)

(f) (g)

(h)

(j)(l)

(d) (e)

(b)

Plate 5.1 Phytophagous insects associated with quinoa in the Neotropical region. (a) Lepidoptera, larvae feeding on quinoaleaf; (b) Leptoglossus sp. in quinoa leaf; (c,d) Oiketicus kirbyi, neotenic larvae coming out of bag or basket; (e) O. kirbyi bag orbasket in quinoa branch; (f ) adult Eurysacca sp.; (g) Eurysacca sp. larvae feeding on quinoa leaf; (h) Pyralidae, larvae; (i) Nezaraviridula, adult in quinoa panicle; and (j) adult Epicauta adspersa in quinoa leaf.

(a)

(d)

(g) (h) (i)

(l)(k)(j)

(e) (f)

(b)

(c)

Plate 5.2 Entomophagous insect on quinoa in Amaicha del Valle. (a) Parasitoid Copidosoma sp. adult; (b) Copidosoma sp. para-sitism in Eurysacca larvae; (c) Eurysacca damaged pupa; (d) parasitoid Ichneumonidae; (e) unidentified parasitoid; (f–l) predatorinsects; (f ) Eriopis connexa, immature stage; (g) Chrysoperla argentina, adult; (h) C. externa, immature stage; (i) C. externa, adult;(j) C. argentina, preying on Spodoptera frugiperda (Lepidoptera) eggs; (k) C. argentina, immature stage preying on aphids; and (l)C. externa, immature stage preying on aphids.

(a) (b)

Plate 7.2 Example of SNP assays using the KASPar™ genotyping chemistry on the Fluidigm access array in the quinoa RIL map-ping population. (a) The genotyping across the 96.96 IFC chip (96 DNA samples on the vertical, 96 SNP assays on the horizontal).(b) Individual SNP loci in a Cartesian graph. A no template control (NTC) and a synthetic heterozygote are identified.

Agroecological regions of quinoaproduction in South America

Sea Level Region

Inter-Andean Valleys Region

High Flatlands (Altiplano) Region

Salt Flatlands Region

W

N

E

S

Plate 8.2 Geographic distribution of quinoa in the Andean Region.

40,000

35,000

30,000

25,000

20,000

15,000

10,000

5,000

-2005 2006 2007 2008 2009 2010 2011 2012 2013

Conventional

Organic

Plate 12.4 US quinoa imports in MT per year, organic versus nonorganic.

Plate 12.6 Multiple quinoa varieties are planted and harvested in the same fields. Photo credit: Vitaliy Prokopets.

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