Advanced entomophagy and human evolution

Entomophagy and Evolution: Eating Insects Past, Present and

Future

Outline• Future first

– A movement towards a more sustainable protein source

• Past– Termite foraging by South African

australopithecines

• Present– Patterns of insects as food in modern foragers

and nonhuman primates

Future

Food and Agriculture Organization recommendations• Further documentation of nutritional values

• Investigate environmental sustainability

• Clarify socio-economic benefits

• Develop legal framework for production and trade

“Further documentation of nutritional values”

This should also include understanding their traditional nutritional role,

past and present




australopithecines



Past About 1.7 mya

SwartkransAu/P. robustus

Stone tools

Bone tools

About 1.7 mya

Tools of this sort are known from three sites in the Cradle of Humankind

Largest sample coming from the site of Swartkrans. 86 total Swartkrans bone tools.

3 cmPhoto: Backwell &

d’Errico, 2001

High amount of wear and polish on one end

Termite foraging?

Display at the Transvaal Museum

Cover story of PNAS v98(4) 2001By Backwell and d’Errico

Pattern and width of the striations on the Swartkrans tools match that of tools used to

experimentally excavate termite mounds

Photo: Backwell & d’Errico, 2001

Why termites?

• Nutritional food source eaten today by populations of each of the great apes, including humans

• Evidence for termites in Plio-Pleistocene Africa

• Compatible with stable carbon isotope analyses of hominin teeth?

• Two pathways

• Most plants utilize the C3 pathway - woody plants

• Chimpanzees and gorillas have a primarily C3 diet

Carbon Isotopes

• C4 plants photosynthesize faster than C3 plants under high light intensity and high temperatures

• Grasses and most savanna plants use a C4 pathway

Carbon Isotopes

Hominin Carbon Isotopes

C4 control

C3 control

Sponheimer, et al 2005

Hominin Carbon Isotopes

C4 control

C3 control

Chimpanzees


C4 control

C3 control

Swartkrans Chimpanzees


Earlier hominins Swartkrans Chimpanzees


Isotope conundrum• About 35% of the hominin diet was coming

from resources that were different from those utilized by modern great apes, even savanna chimpanzees

• The Swartkrans hominins were eating the same proportion of these resources as their non-tool-using older relatives, A. africanus, so the resource was likely not meat

It was proposed that termites could provide the answer

• Grass-foraging termites would provide the same signature as consuming grass-eating antelope, but would be easier to obtain.

• The evidence of termite foraging from the Swartkrans bone tools made this an appealing answer to the conundrum

Termite Diversity• Worldwide there are over 280 genera

and 2,700 species

• There are 85 genera in Sub-Saharan Africa

• Termite diets vary by clade feeding on wood, grass, soil

• The caste system brings additional intraspecies variation

Which genus of termites were hominins

consuming?

TrinervitermesThe most common termites in the Cradle of Humankind today

Central to previous bone tool studies

Grass foragers – C4 resources

Glue-spitting defense – low palatability

MacrotermesPrimarily eat wood resources – C3 signature

Most common genus of termites consumed by chimpanzees

Mandibular pinchers defense – pinch “fishing” probes

• Conducted experiments to assess if the mounds of the two genera were different

enough to leave distinct signatures

Use wear study

• Texture analysis = confocal microscopy and scale-sensitive fractal analysis

Use wear study

• Texture analysis = confocal microscopy and scale-sensitive fractal analysis

• Signatures not different between termite mounds (Lesnik 2011)

Use wear study

Modeling the past• There is no available direct evidence of

hominin termite selection

• Therefore, modeling the past based on present-day analogs is the best way to estimate preferences

• Termites are consumed by populations of the great apes, including humans

• Not all apes show the same preference for Macrotermes

Bwindi Mountain Gorilla

Termite desirability

• Gorillas highly select the workers of soil-feeding termites such as Cubitermes

Dja, CameroonDeblauwe and Janssens, 2008

Gorilla preferences

Modern human termite preferences

• Populations of humans across Africa regularly dig for termites, often of the genus Macrotermes, but also of other genera such as Hodotermes

• Eat soldiers year-round and alates (winged reproductives) when seasonally available

Species Caste Preferred By Crude Protein (%)

Crude Fat(%) Fe (mg/100g)

M. muelleri**

Soldiers Chimps 72 5 10

C. heghi** Workers Gorillas 15 13 2962

M. falciger* Alates Humans 21 22 _

* Phelps et al 1975**Deblauwe and Janssens, 2008

Termite Preferences and Nutrition

Frugivorous chimpanzees receive plenty of

micronutrients, but protein requirements are more difficult

to meet

Folivorous gorillas receive plenty of protein from leaves,

but micronutrient requirements are more

difficult to meetPhotos: Abigail Lubliner & Rob Kroenert

Termite preferences reflect their diets

Models for hominins eating termites

• Chimp model• protein-rich termites

• Gorilla model• micronutrient-rich termites

• Human model• variable, but definite inclusion of fat-rich

termites

• Calculated by Sponheimer and colleagues (2005)

• We do not know the proportions of food types within these categories

35% C4 foods 65% C3 foods

Reconstructing the diet of Au. robustus

Reconstructing the diet of Au. robustus• Although we do not know the exact

proportions of foods, we can minimally assume their dietary quality is not lower than chimpanzees

• Dietary quality is the amount of extractable nutrients per unit weight – Leaves = Low quality– Fruit = High quality

leavesfruit



• It can be expected that a majority of the C3 resources would come from fruit

C4 Isotope Conundrum• Cerling and colleagues (2010) show east

African robust australopithecines have 77% C4 diet

• There is no way hominins were insectivorous

C4 Isotope Conundrum• Underground storage organs -USO’s

– Sedges– Tubers

• Possibly grass

• The isotope conundrum may be solved, but no longer gives clues about amount of omnivory in the diet


leavesfruit


USOs/grasses

Crude Protein (% DM)

Crude Fat (% DM)

Micro-nutrients

Fruit 7.7 1.7 highLeaves 16.8 2.6 low

Grasses, USOs

10.5 1.6 high

Wrangham, et al., 1991Codron, et al. 2007 for savanna grasses and sedges

Nutritional Values of Different Resources


LeavesFruit∧energy

∧micronutrients

USOs/grasses∧energy

∧micronutrients

• With this sort of diet, it appears that protein would be the nutrient of most concern, so a chimpanzee model of termite predation would be appropriate

∧protein

• Au. robustus had an average cranial capacity of 587 cc

• Similar in size to specimens some attribute to early Homo

• Utilization of resources beyond what is seen in chimpanzees would be necessary to support the large, expensive organ

Au. robustus• Digging for termites

would allow for less discrimination against non-soldier castes.

• Hominins could have dug up larvae and alates in a manner similar to some modern human populations (Lesnik 2014)




australopithecines



Human preferences

Jongema, 2012

Present• Termites are not the only available edible

insect

• Caterpillars, beetle larvae, ants and many more are consumed regularly around the world

• All are highly variable in nutrients, but protein seems to be high in most

Examples of modern foragers• The San in Botswana

• The Ache in Paraguay

• The Arunta of central Australia

The San, Botswana

• When foraging, women may stop and eat termites all day (Nonaka, 1996)

Photo:PhotographersDirect

The Ache,Paraguay

• Women average 15 minutes a day in search of various insect larvae

• They will take them whenever encountered (Hawkes et al., 1982)

Photo:F1 Online Photos

The Arunta,Australia

• Women, accompanied by their children, carry digging sticks and go out in search of small fauna, including social insects that are available year-round (Bodenheimer, 1951)

Photo:Spencer and Gillan, 1899

Cross-culturally• In these example, as well as others

including horticulturalists of northwest Amazon (D. Dufour), women spend more time foraging for and eating insects than men

• There are numerous cultural factors, but evolutionary biologists are interested in a possible evolution to these patterns in our ancestors

Sexual division of laborHypotheses:

• Cooperative Provisioning Model – Divide and conquer for family provisioning

• Conflict Model – The two sexes have always employed different

foraging strategies due to differing needs

Testing the conflict model• If similar differences are seen in

nonhuman primates who supplement their diets with insects, then there is less support for the behavior relating to cooperative provisioning

Great apesChimpanzees Orangutans

Photos: Franz Lanting & John S. Canada

Old World MonkeysMangabeys Langurs

Photos: FactZoo.com & Thorsten Milse

New World MonkeysCapuchins Squirrel Monkeys

Photos: Steven G. Johnson & Otto Monge

Sexual division of labor

• In regards to insects as a food resource, it appears that the conflict model is a better fit

Sexual Division of Labor

• Women’s protein requirements increase by 50% when pregnant and lactating

• Insects may provide a reliable source of this nutrient they can obtain even when accompanied by small children

• This pattern of behavior could be expected for our hominin ancestors as well

Sexual Division of Labor• These preliminary patterns are from

currently available data

• There are many insect-foraging populations where the necessary data is not recorded or is not comparable

Why are bugs not common cuisine in the US and Europe?

entomoanthro.org

Human preferences

Jongema, 2012

Europe under ice until 18,000 ya

Europe• In glaciated Europe, hunting would have been

primary subsistence

• Not long after the end of the Pleistocene, cattle domestication occurs (about 10kya)

• With animal resources well-represented in the diet, and insects being less plentiful at northern latitudes, entomophagy is not likely

Peopling of the Americas• The first people here had to survive

crossing Beringia

Peopling of the Americas• The earliest people to arrive to the New

World likely did not eat insects

• As people migrated further and settled in and around tropic zones, insect eating may have been essential

Conclusions• Patterns of insects as food for great apes and

modern foragers suggest that insects could have been very important for hominid females

Photo: Backwell & d’Errico, 2001

20% increase in brain size across australopithecines

Conclusions• Using this resource beyond what is seen

in apes today could account for the additional resources needed by australopithecines to support their increased brain sizes

May 26-28, 2016

eatinginsectsdetroit.org

entomoanthro.org

Science

Advanced entomophagy and human evolution