Ecology and Evolution of Dung Beetles

Ecology and Evolution of Dung Beetles, First Edition. Edited by Leigh W. Simmons and T. James Ridsdill-Smith.

© 2011 Blackwell Publishing Ltd. Published 2011 by Blackwell Publishing Ltd. ISBN: 978-1-444-33315-2

Ecology and Evolution of Dung Beetles

Edited by

Leigh W. Simmons & T. James Ridsdill-Smith

This edition first published 2011, � 2011 by Blackwell Publishing Ltd

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Library of Congress Cataloguing-in-Publication Data

Ecology and evolution of dung beetles / edited by Leigh W. Simmons & T. James Ridsdill-Smith.p. cm.

Includes index.ISBN 978-1-4443-3315-2 (hardback)1. Dung beetles–Ecology. 2. Dung beetles–Evolution. I. Simmons, Leigh W., 1960- II.Ridsdill-Smith, J., 1942-QL596.S3E26 2011595.76'49–dc22

2010046392

A catalogue record for this book is available from the British Library.

This book is published in the following electronic formats: eBook 9781444341973;Wiley Online Library 9781444342000; ePub 9781444341980; MobiPocket 9781444341997

Set in 10.5/12pt, Classical Garamond by Thomson Digital, Noida, India

1 2011

Contents

Preface xiiiAcknowledgements xvContributing authors xvii

1 Reproductive competition and its impact on theevolution and ecology of dung beetles 1Leigh W. Simmons and T. James Ridsdill-Smith1.1 Introduction 11.2 Competition for mates and the evolution

of morphological diversity 21.3 Competition for resources and the evolution

of breeding strategies 91.4 Ecological consequences of intraspecific

and interspecific competition 141.4.1 Niche expansion 151.4.2 Regional distribution and seasonal activity 171.4.3 Community dynamics 18

1.5 Conservation 191.6 Concluding remarks 20

2 The evolutionary history and diversificationof dung beetles 21T. Keith Philips2.1 Introduction 212.2 Scarabaeinae diversity and tribal classification issues 22

2.2.1 Dichotomiini and Coprini 242.2.2 Canthonini 252.2.3 Eucraniini 252.2.4 Phanaeini 252.2.5 Phanaeini + Eucraniini 262.2.6 Scarabaeini 262.2.7 Gymnopleurini 262.2.8 Eurysternini 262.2.9 Sisyphini 26

2.2.10 Onitini 272.2.11 Oniticellini 272.2.12 Onthophagini 27

2.3 Scarabaeine dung beetle phylogenies 272.4 The sister clade to the Scarabaeinae 312.5 The origin of the dung beetles 332.6 The oldest lineages and their geographical origin 342.7 Evolution of activity period 362.8 Evolution of feeding habits 362.9 Evolution of derived alternative lifestyles 37

2.10 Evolution of nidification: dung manipulation strategies 402.11 Evolution of nidification: nesting behaviour

and subsocial care 422.12 Conclusions 442.13 Future work/gaps in knowledge 45

3 Male contest competition and the evolutionof weapons 47Robert Knell3.1 Introduction 473.2 Dung beetle horns as weapons 493.3 Functional morphology of horns 503.4 Horns as predictors of victory 533.5 Are beetle horns simply tools? 553.6 The evolution of horns: rollers vs. tunnellers 563.7 The evolution of horns: population density 593.8 The evolution of horns: sex ratio 633.9 Future work 64

4 Sexual selection after mating: the evolutionaryconsequences of sperm competition and crypticfemale choice in onthophagines 66Leigh W. Simmons4.1 Introduction 664.2 Sperm competition theory 68

vi Contents

4.3 Evolution of ejaculate expenditure in the genusOnthophagus 71

4.4 Evolutionary consequences of variation in ejaculateexpenditure 72

4.5 Theoretical models of female choice 754.6 Quantitative genetics of ejaculate traits 764.7 Empirical evidence for adaptive cryptic female choice in

Onthophagus taurus 78Box 4.1 Indirect genetic benefits of cryptic female

choice in Onthophagus taurus 814.8 Conclusions and future directions 834.9 Dedication and acknowledgement 86

5 Olfactory ecology 87G.D. Tribe and B.V. Burger5.1 Introduction 875.2 Orientation to dung and other resources 875.3 Olfactory cues used in mate attraction and mate

recognition 915.3.1 Morphology of pheromone-producing and

-dispersing structures 935.3.2 Pheromone-dispersing behaviour 94

5.4 Chemical composition of Kheper pheromones 955.4.1 Electroantennographic detection 985.4.2 Comparison of the responses of beetle species

to attractant compounds 985.4.3 The pheromone-disseminating carrier material 102

5.5 Kairomones 1035.6 Defensive secretions 1045.7 Conclusions and future directions 105

6 Explaining phenotypic diversity: the conditionalstrategy and threshold trait expression 107Joseph Tomkins and Wade Hazel6.1 Introduction 1076.2 The environmental threshold model 109

6.2.1 Does the development of a horn dimorphismin male dung beetles occur in a manner consistentwith the assumptions of the ET model? 110

6.3 Applying the threshold model 1186.3.1 Predicting the mean switchpoint of a population 1186.3.2 Estimating the selection on thresholds using the

ET model 1196.3.3 Estimating selection under positive allometry 120

6.4 Future directions 123

Contents vii

7 Evolution and development: Onthophagus beetlesand the evolutionary development genetics ofinnovation, allometry and plasticity 126Armin Moczek7.1 Introduction 1267.2 Evo-devo and eco-devo – a brief introduction 1277.3 Onthophagus beetles as an emerging model system in

evo-devo and eco-devo 128Box 7.1 Developmental genetic tools available in

Onthophagus beetles: utility and limitations 1297.4 The origin and diversification of novel traits 132

7.4.1 Dung beetle horns as novel traits 1337.4.2 How horns develop 1347.4.3 The developmental genetics of horn growth 1357.4.4 The developmental genetics of pupal remodelling 1377.4.5 The origin of adult thoracic horns through

exaptation 1387.5 The regulation and evolution of scaling 140

7.5.1 Onthophagine scaling relationships: the roles ofnutrition and hormones 142

7.5.2 Onthophagine scaling relationships: the role oftrade-offs during development and evolution 143

7.5.3 Onthophagine scaling relationships: developmentaldecoupling versus common developmentalprogramme 144

7.5.4 Onthophagine scaling relationships: thedevelopmental genetics of size and shape 147

7.6 The development, evolution, and consequences ofphenotypic plasticity 1487.6.1 Developmental mechanisms and the evolutionary

consequences of plasticity 1497.7 Conclusion 151

8 The evolution of parental care in the onthophaginedung beetles 152John Hunt and Clarissa House8.1 Introduction 1528.2 Parental care theory 154

8.2.1 A conventional view of parental care theory 1548.2.2 More recent developments in parental care theory 156

8.3 Testing parental care theory using onthophagine dungbeetles 1578.3.1 Parental care in onthophagine dung beetles 158

viii Contents

8.3.2 The costs and benefits of parental care inonthophagine dung beetles 160

8.3.3 Behavioural dynamics of the sexes duringbiparental care 163

8.3.4 Confidence of paternity and paternal care 1668.3.5 Do parents optimize the care they provide? 1698.3.6 Evolutionary quantitative genetics of parental

care 1738.4 Conclusions and future directions 174

9 The visual ecology of dung beetles 177Marcus Byrne and Marie Dacke9.1 Introduction 1779.2 Insect eye structure 179

9.2.1 The apposition eye 1799.2.2 The superposition eye 179

9.3 Eye limitations 1819.4 Dung beetle vision 182

9.4.1 Dim light vision 1829.4.2 The tapetum and enlarged rhabdoms 1859.4.3 The canthus 186

9.5 Visual ecology of flight activity 1879.5.1 Diel flight activity 1879.5.2 Crepuscular flight activity 1889.5.3 Endothermy and vision 1889.5.4 Body size and flight activity 189

9.6 Sexual selection and eyes 1909.7 Ball-rolling 192

9.7.1 Orientation by ball-rolling beetles 1929.7.2 The polarization compass 1949.7.3 Polarization vision 1949.7.4 Polarization vision in dim light 196

9.8 Conclusions 198

10 The ecological implications of physiologicaldiversity in dung beetles 200Steven L. Chown and C. Jaco Klok10.1 Introduction 20010.2 Thermoregulation 20110.3 Thermal tolerance 20710.4 Water balance 20810.5 Gas exchange and metabolic rate 21510.6 Conclusion and prospectus 218

Contents ix

11 Dung beetle populations: structure andconsequences 220Tomas Roslin and Heidi Viljanen11.1 Introduction 22011.2 Study systems 221

11.2.1 The Finnish cow pat 22211.2.2 The Malagasy lemur pellet 223

11.3 Range size 22411.4 Habitat and resource selection 22711.5 Dung beetle movement 23011.6 The genetic structure of dung beetle populations 23511.7 Consequences: spatial population structures and

responses to habitat loss 23811.8 Perspectives 243

12 Biological control: ecosystem functions providedby dung beetles 245T. James Ridsdill-Smith and Penny B. Edwards12.1 Introduction 24512.2 Functions of dung beetles in ecosystems 246

12.2.1 Dung burial and nutrient cycling 24612.2.2 Control of dung-breeding flies 24712.2.3 Control of parasites 250

12.3 Dung beetles in pasture habitats 25012.4 Seasonal occurrence and abundance of native dung

beetles in Australia 25112.5 Distribution and seasonal occurrence of introduced

dung beetles in Australia 25412.6 Long-term studies of establishment and abundance 257

12.6.1 Summer rainfall climate area of Queensland 25812.6.2 Mediterranean climate area of south Western

Australia 26012.6.3 Long-term population trends 261

12.7 Competitive exclusion 26212.8 Optimizing the benefits of biological control 264

13 Dung beetles as a candidate study taxon inapplied biodiversity conservation research 267Elizabeth S. Nichols and Toby A. Gardner13.1 Introduction 26713.2 Satisfying data needs to inform conservation practice 26813.3 The role of dung beetles in applied biodiversity research in

human-modified landscapes 270

x Contents

13.3.1 Dung beetles as a viable candidate for biodiversityresearch 271

13.3.2 Dung beetles as reliable indicators ofenvironmental change 272

13.3.3 Interpreting disturbance response patterns:application of a trait-based framework forecological research 276

13.3.4 Dung beetles as ecological disturbance indicatortaxa: applied examples 286

13.4 Dung beetle conservation 28613.5 Some ways forward 290

References 293

Subject index 340

Taxonomic index 343

Contents xi

Preface

Scarabaeine dung beetles feed on the dung of herbivores as adults, and bury dungmasses as provisions for their offspring. The subfamily contains about 6,000 speciesand is found in all continents except Antarctica. Beetles of different species areattracted to the same pad of fresh dung, but they occupymany different niches, thusreducing competition. Activity of the beetles is clearly visible to the casual observerand it fascinated the early Egyptians andGreeks,who considered the rolling of dungballs as representing the sun being rolled across the sky.

In the 19th century, J.H. Fabre described cooperation between male and femalebeetles in the formation of brood balls, the female role in oviposition and, in somecases, brood care, while Charles Darwin used the horns of adult male beetles toillustrate his theory of sexual selection. The biology and taxonomy of many speciescontinued to be described through the 20th century, and books have been publishedsummarising dung beetle natural history by Halffter & Matthews (1966), repro-ductive biology by Halffter & Edmonds (1982), ecology by Hanski & Cambefort(1991) and, most recently, a general overview of their evolutionary biology andconservation by Scholtz, Davis & Kryger (2009).

Our thesis in this book is that the wealth of information now available on dungbeetles elevates them to the status of ‘model system’. Dung beetles have provedremarkably useful for broad-scale ecological studies that address fundamental issuesin community and population ecology and its extension to conservation biology. Atthe same time, they are providing valuable laboratory tools to explore fundamentalquestions in evolutionary biology; Darwin’s theories of sexual selection have beenvalidated through work on dung beetles and they are contributing to our under-standing of the evolution of parental care. Moreover, their utility for studiesof phenotypic plasticity is contributing to emerging research fields ofevolutionary developmental biology (‘evo-devo’) and ecological developmentalbiology (‘eco-devo’).

The development of genomic tools for dung beetles will no doubt invigoratefuture research on this important taxon. Thus, our aim with this book is to providedetailed and focused reviews of the important contributions dung beetles continueto provide in evolutionary and ecological research.

Leigh W. Simmons and T. James Ridsdill-SmithDecember 2010, Perth, Western Australia

xiv Preface

Acknowledgements

Wewould like to thank our co-authors and the following individuals for reviewingchapters of the manuscript:

JohnAlcock, AndyAustin, BrunoBuzatto, Paul Cooper, Saul Cunningham,VincentDebat, Raphael Didham, Mark Elgar, Doug Emlen, Federico Escobar, John Evans,Francisco Garc�ıa-Gonz�ales, Mark Harvey, Richard Hobbs, Peter Holter, GeoffParker, Alexander Shingleton, Per Smiseth, Steve Trumbo, Melissa Thomas, CraigWhite, PhilWhithers, and JochemZeal.We are indebted toWardCooper ofWiley-Blackwell for his enthusiasm for the project.

Contributing Authors

Barend (Ben) V BurgerLaboratory for Ecological Chemistry, Department of Chemistry, StellenboschUniversity, Stellenbosch 7600, South Africa

Marcus ByrneSchool of Animal, Plant and Environmental Sciences, University of theWitwatersrand, Johannesburg 2050, South Africa.

Steven L. ChownCentre for Invasion Biology, Department of Botany and Zoology, StellenboschUniversity, Private Bag X1, Matieland 7602, South Africa.

Marie DackeVision Group, Zoology, S€olvegatan 35, 223 62 Lund, Sweden.

Penny B. EdwardsPO Box 865, Maleny, Queensland 4552, Australia.

Toby A. GardnerDepartment of Zoology, University of Cambridge, Downing Street,Cambridge, CB2 3EJ, UK.

Wade HazelDepartment of Biology, DePauw University, Greencastle, IN 46135, USA.

Clarissa HouseCentre for Ecology and Conservation, School of Biosciences, The Universityof Exeter, Tremough Campus, Penryn, TR10 9EZ, Cornwall, UK.

John HuntCentre for Ecology and Conservation, School of Biosciences, The Universityof Exeter, Tremough Campus, Penryn, TR10 9EZ, Cornwall, UK.

C. Jaco KlokSchool of Life Sciences, Arizona State University, PO Box 874601,Tempe, AZ 85287-4601, USA.

Robert KnellSchool of Biological and Chemical Sciences, Queen Mary University of London,Mile End Road, London E1 4NS, UK.

Armin MoczekDepartment of Biology, Indiana University, 915 E. Third Street, Myers Hall150, Bloomington, IN 47405-7107, USA.

Elizabeth S. NicholsCenter for Biodiversity and Conservation, Invertebrate Conservation Program,American Museum of Natural History, Central Park West at 79th St.,New York, NY 10024-5193, USA.

T. Keith PhilipsSystematics and Evolution Laboratory, Department of Biology, WesternKentucky University, 1906 College Heights Blvd., Bowling Green,KY 42101-3576, USA.

T. James Ridsdill-SmithSchool of Animal Biology, University of Western Australia, Crawley 6009,Crawley, Western Australia.

Tomas RoslinDepartment of Agricultural Sciences, PO Box 27, FI-00014 University of Helsinki,Finland.

Leigh W. SimmonsCentre for Evolutionary Biology, School of Animal Biology, Universityof Western Australia, Crawley, 6009, Crawley, Western Australia.

Joseph L. TomkinsCentre for Evolutionary Biology, School of Animal Biology, Universityof Western Australia, Crawley, 6009, Crawley, Western Australia.

Geoffery D. TribeARC-Plant Protection Research Institute, Private Bag X5017,Stellenbosch 7599, South Africa.

Heidi ViljanenMetapopulation Research Group, Department of Biological and EnvironmentalSciences, PO Box 65, FI-00014 University of Helsinki, Finland.

xviii Contributing Authors