advanced entomophagy and human evolution
TRANSCRIPT
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Entomophagy and Evolution: Eating Insects Past, Present and
Future
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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
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Future
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Food and Agriculture Organization recommendations• Further documentation of nutritional values
• Investigate environmental sustainability
• Clarify socio-economic benefits
• Develop legal framework for production and trade
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“Further documentation of nutritional values”
This should also include understanding their traditional nutritional role,
past and present
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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
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Past About 1.7 mya
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SwartkransAu/P. robustus
Stone tools
Bone tools
About 1.7 mya
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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
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Termite foraging?
Display at the Transvaal Museum
Cover story of PNAS v98(4) 2001By Backwell and d’Errico
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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
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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?
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• Two pathways
• Most plants utilize the C3 pathway - woody plants
• Chimpanzees and gorillas have a primarily C3 diet
Carbon Isotopes
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• 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
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Hominin Carbon Isotopes
C4 control
C3 control
Sponheimer, et al 2005
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Hominin Carbon Isotopes
C4 control
C3 control
Chimpanzees
Sponheimer, et al 2005
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C4 control
C3 control
Swartkrans Chimpanzees
Sponheimer, et al 2005
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Earlier hominins Swartkrans Chimpanzees
Sponheimer, et al 2005
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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
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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
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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
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Which genus of termites were hominins
consuming?
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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
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MacrotermesPrimarily eat wood resources – C3 signature
Most common genus of termites consumed by chimpanzees
Mandibular pinchers defense – pinch “fishing” probes
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• Conducted experiments to assess if the mounds of the two genera were different
enough to leave distinct signatures
Use wear study
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• Texture analysis = confocal microscopy and scale-sensitive fractal analysis
Use wear study
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• Texture analysis = confocal microscopy and scale-sensitive fractal analysis
• Signatures not different between termite mounds (Lesnik 2011)
Use wear study
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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
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• 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
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• Gorillas highly select the workers of soil-feeding termites such as Cubitermes
Dja, CameroonDeblauwe and Janssens, 2008
Gorilla preferences
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Modern human termite preferences
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• 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
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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
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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
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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
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• 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
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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
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leavesfruit
Reconstructing the diet of Au. robustus
65% C3 foods 35% C4 foods
• It can be expected that a majority of the C3 resources would come from fruit
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C4 Isotope Conundrum• Cerling and colleagues (2010) show east
African robust australopithecines have 77% C4 diet
• There is no way hominins were insectivorous
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C4 Isotope Conundrum• Underground storage organs -USO’s
– Sedges– Tubers
• Possibly grass
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• The isotope conundrum may be solved, but no longer gives clues about amount of omnivory in the diet
Reconstructing the diet of Au. robustus
leavesfruit
65% C3 foods 35% C4 foods
USOs/grasses
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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
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Reconstructing the diet of Au. robustus
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
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• 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
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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)
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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
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Human preferences
Jongema, 2012
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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
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Examples of modern foragers• The San in Botswana
• The Ache in Paraguay
• The Arunta of central Australia
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The San, Botswana
• When foraging, women may stop and eat termites all day (Nonaka, 1996)
Photo:PhotographersDirect
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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
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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
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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
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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
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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
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Great apesChimpanzees Orangutans
Photos: Franz Lanting & John S. Canada
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Old World MonkeysMangabeys Langurs
Photos: FactZoo.com & Thorsten Milse
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New World MonkeysCapuchins Squirrel Monkeys
Photos: Steven G. Johnson & Otto Monge
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Sexual division of labor
• In regards to insects as a food resource, it appears that the conflict model is a better fit
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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
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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
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Why are bugs not common cuisine in the US and Europe?
entomoanthro.org
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Human preferences
Jongema, 2012
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Europe under ice until 18,000 ya
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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
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Peopling of the Americas• The first people here had to survive
crossing Beringia
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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
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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
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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
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May 26-28, 2016
eatinginsectsdetroit.org
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entomoanthro.org