Katherine R Amato1, Óscar M Chaves2, Elizabeth K Mallott1, Timothy M Eppley3,4, Filipa Abreu5, Andrea L Baden6,7, Adrian A Barnett8, Julio Cesar Bicca-Marques9, Sarah A Boyle10, Christina J Campbell11, Colin A Chapman12,13,14, María Fernanda De la Fuente5, Pengfei Fan15, Peter J Fashing16,17, Annika Felton18, Barbara Fruth19,20,21, Vanessa B Fortes22, Cyril C Grueter23,24, Gottfried Hohmann25, Mitchell Irwin26, Jaya K Matthews24,27, Addisu Mekonnen17, Amanda D Melin28, David B Morgan29, Julia Ostner30,31, Nga Nguyen16,17, Alex K Piel32, Braulio Pinacho-Guendulain33,34, Erika Patricia Quintino-Arêdes9, Patrick Tojotanjona Razanaparany35,36, Nicola Schiel5, Crickette M Sanz37,38, Oliver Schülke30,31, Sam Shanee39, Antonio Souto40, João Pedro Souza-Alves40, Fiona Stewart20, Kathrine M Stewart21, Anita Stone41, Binghua Sun42, Stacey Tecot43, Kim Valenta44, Erin R Vogel45, Serge Wich20, Yan Zeng46. 1. Department of Anthropology, Northwestern University, Evanston, Illinois, USA. 2. Escuela de Biología, Universidad de Costa Rica, UCR, San José, Costa Rica. 3. Institute for Conservation Research, San Diego Zoo Global, San Diego, California, USA. 4. Department of Anthropology, Portland State University, Portland, Oregon, USA. 5. Department of Biology, Federal Rural University of Pernambuco, Recife, Pernambuco, Brazil. 6. Department of Anthropology, Hunter College of the City University of New York, New York, New York, USA. 7. The New York Consortium in Evolutionary Primatology (NYCEP), City University of New York, New York, New York, USA. 8. Amazon Mammals Research Group, National Amazon Research Institute (INPA), Manaus, AM, Brazil & Department of. Zoology, Federal University of Pernambuco, Recife, Prince Edward Island, Brazil. 9. Laboratório de Primatologia, Escola de Ciências da Saúde e da Vida, Pontifícia Universidade Católica do Rio Grande do Sul, PUCRS, Porto Alegre, RS, Brazil. 10. Department of Biology, Rhodes College, Memphis, Tennessee, USA. 11. Department of Anthropology, California State University Northridge, Northridge, California, USA. 12. Department of Anthropology, Center for the Advanced Study of Human Paleobiology, George Washington University, Washington, District of Columbia, USA. 13. School of Life Sciences, University of KwaZulu-Natal, Pietermaritzburg, South Africa. 14. Shaanxi Key Laboratory for Animal Conservation, Northwest University, Xi'an, China. 15. School of Life Sciences, Sun Yat-Sen University, Guangzhou, China. 16. Department of Anthropology and Environmental Studies Program, California State University Fullerton, Fullerton, California, USA. 17. Centre for Ecological and Evolutionary Synthesis (CEES), University of Oslo, Oslo, Norway. 18. Southern Swedish Forest Research Centre, Swedish University of Agricultural Sciences (SLU), Alnarp, Sweden. 19. Department of Human Behavior, Ecology and Culture, Max-Planck-Institute for Evolutionary Anthropology, Leipzig, Germany. 20. School of Biological and Environmental Sciences, Liverpool John Moores University, Liverpool, United Kingdom. 21. Centre for Research and Conservation, Royal Zoological Society of Antwerp, Antwerp, Belgium. 22. Laboratório de Primatologia, Departamento de Zootecnia e Ciências Biológicas, Universidade Federal de Santa Maria, Palmeira das Missões, RS, Brazil. 23. School of Human Sciences, The University of Western Australia, Perth, Australia. 24. Centre for Evolutionary Biology, School of Biological Sciences, The University of Western Australia, Perth, Australia. 25. Department of Human Evolution, Max Planck Institute for Evolutionary Anthropology, Leipzig, Germany. 26. Department of Anthropology, Northern Illinois University, DeKalb, Illinois, USA. 27. Africa Research & Engagement Centre, The University of Western Australia, Crawley, Western Australia, Australia. 28. Department of Anthropology and Archaeology, University of Calgary, Calgary, Canada. 29. Lester E. Fisher Center for the Study and Conservation of Apes, Lincoln Park Zoo, Chicago, Illinois, USA. 30. Department of Behavioral Ecology, University of Goettingen, Goettingen, Germany. 31. Research Group Primate Social Evolution, German Primate Center, Leibniz Institute for Primate Research, Goettingen, Germany. 32. Department of Anthropology, University College London, London, United Kingdom. 33. Departamento de Ciencias de la Salud, Universidad Autónoma Metropolitana (UAM), Lerma, Mexico. 34. Centro Interdisciplinario de Investigación para el Desarrollo Integral Regional (CIIDIR), Unidad Oaxaca, Instituto Politécnico Nacional, Mexico City, Mexico. 35. Graduate School of Asian and African Area Studies, Kyoto University, Kyoto, Japan. 36. Department of Zoology and Animal Biodiversity, University of Antananarivo, Antananarivo, Madagascar. 37. Department of Anthropology, Washington University in St. Louis, St. Louis, Missouri, USA. 38. Congo Program, Wildlife Conservation Society, Brazzaville, Congo. 39. Neotropical Primate Conservation, Cornwall, United Kingdom. 40. Departamento de Zoologia, Universidade Federal de Pernambuco, Recife, Pernambuco, Brazil. 41. Biology Department, California Lutheran University, Thousand Oaks, California, USA. 42. School of Resource and Environmental Engineering, Anhui University, Hefei, China. 43. School of Anthropology, University of Arizona, Tucson, Arizona, USA. 44. Department of Anthropology, University of Florida, Gainesville, Florida, USA. 45. Department of Anthropology, Rutgers University, New Brunswick, New Jersey, USA. 46. Animal Microecology Institute, College of Veterinary, Sichuan Agricultural University, Ya'an, China.
Abstract
OBJECTIVES: Although fermented food use is ubiquitous in humans, the ecological and evolutionary factors contributing to its emergence are unclear. Here we investigated the ecological contexts surrounding the consumption of fruits in the late stages of fermentation by wild primates to provide insight into its adaptive function. We hypothesized that climate, socioecological traits, and habitat patch size would influence the occurrence of this behavior due to effects on the environmental prevalence of late-stage fermented foods, the ability of primates to detect them, and potential nutritional benefits. MATERIALS AND METHODS: We compiled data from field studies lasting at least 9 months to describe the contexts in which primates were observed consuming fruits in the late stages of fermentation. Using generalized linear mixed-effects models, we assessed the effects of 18 predictor variables on the occurrence of fermented food use in primates. RESULTS: Late-stage fermented foods were consumed by a wide taxonomic breadth of primates. However, they generally made up 0.01%-3% of the annual diet and were limited to a subset of fruit species, many of which are reported to have mechanical and chemical defenses against herbivores when not fermented. Additionally, late-stage fermented food consumption was best predicted by climate and habitat patch size. It was more likely to occur in larger habitat patches with lower annual mean rainfall and higher annual mean maximum temperatures. DISCUSSION: We posit that primates capitalize on the natural fermentation of some fruits as part of a nutritional strategy to maximize periods of fruit exploitation and/or access a wider range of plant species. We speculate that these factors contributed to the evolutionary emergence of the human propensity for fermented foods.
OBJECTIVES: Although fermented food use is ubiquitous in humans, the ecological and evolutionary factors contributing to its emergence are unclear. Here we investigated the ecological contexts surrounding the consumption of fruits in the late stages of fermentation by wild primates to provide insight into its adaptive function. We hypothesized that climate, socioecological traits, and habitat patch size would influence the occurrence of this behavior due to effects on the environmental prevalence of late-stage fermented foods, the ability of primates to detect them, and potential nutritional benefits. MATERIALS AND METHODS: We compiled data from field studies lasting at least 9 months to describe the contexts in which primates were observed consuming fruits in the late stages of fermentation. Using generalized linear mixed-effects models, we assessed the effects of 18 predictor variables on the occurrence of fermented food use in primates. RESULTS: Late-stage fermented foods were consumed by a wide taxonomic breadth of primates. However, they generally made up 0.01%-3% of the annual diet and were limited to a subset of fruit species, many of which are reported to have mechanical and chemical defenses against herbivores when not fermented. Additionally, late-stage fermented food consumption was best predicted by climate and habitat patch size. It was more likely to occur in larger habitat patches with lower annual mean rainfall and higher annual mean maximum temperatures. DISCUSSION: We posit that primates capitalize on the natural fermentation of some fruits as part of a nutritional strategy to maximize periods of fruit exploitation and/or access a wider range of plant species. We speculate that these factors contributed to the evolutionary emergence of the human propensity for fermented foods.
Authors: Timothy M Eppley; Selwyn Hoeks; Colin A Chapman; Jörg U Ganzhorn; Katie Hall; Megan A Owen; Dara B Adams; Néstor Allgas; Katherine R Amato; McAntonin Andriamahaihavana; John F Aristizabal; Andrea L Baden; Michela Balestri; Adrian A Barnett; Júlio César Bicca-Marques; Mark Bowler; Sarah A Boyle; Meredith Brown; Damien Caillaud; Cláudia Calegaro-Marques; Christina J Campbell; Marco Campera; Fernando A Campos; Tatiane S Cardoso; Xyomara Carretero-Pinzón; Jane Champion; Óscar M Chaves; Chloe Chen-Kraus; Ian C Colquhoun; Brittany Dean; Colin Dubrueil; Kelsey M Ellis; Elizabeth M Erhart; Kayley J E Evans; Linda M Fedigan; Annika M Felton; Renata G Ferreira; Claudia Fichtel; Manuel L Fonseca; Isadora P Fontes; Vanessa B Fortes; Ivanyr Fumian; Dean Gibson; Guilherme B Guzzo; Kayla S Hartwell; Eckhard W Heymann; Renato R Hilário; Sheila M Holmes; Mitchell T Irwin; Steig E Johnson; Peter M Kappeler; Elizabeth A Kelley; Tony King; Christoph Knogge; Flávia Koch; Martin M Kowalewski; Liselot R Lange; M Elise Lauterbur; Edward E Louis; Meredith C Lutz; Jesús Martínez; Amanda D Melin; Fabiano R de Melo; Tsimisento H Mihaminekena; Monica S Mogilewsky; Leandro S Moreira; Letícia A Moura; Carina B Muhle; Mariana B Nagy-Reis; Marilyn A Norconk; Hugh Notman; M Teague O'Mara; Julia Ostner; Erik R Patel; Mary S M Pavelka; Braulio Pinacho-Guendulain; Leila M Porter; Gilberto Pozo-Montuy; Becky E Raboy; Vololonirina Rahalinarivo; Njaratiana A Raharinoro; Zafimahery Rakotomalala; Gabriel Ramos-Fernández; Delaïd C Rasamisoa; Jonah Ratsimbazafy; Maholy Ravaloharimanitra; Josia Razafindramanana; Tojotanjona P Razanaparany; Nicoletta Righini; Nicola M Robson; Jonas da Rosa Gonçalves; Justin Sanamo; Nicole Santacruz; Hiroki Sato; Michelle L Sauther; Clara J Scarry; Juan Carlos Serio-Silva; Sam Shanee; Poliana G A de Souza Lins; Andrew C Smith; Sandra E Smith Aguilar; João Pedro Souza-Alves; Vanessa Katherinne Stavis; Kim J E Steffens; Anita I Stone; Karen B Strier; Scott A Suarez; Maurício Talebi; Stacey R Tecot; M Paula Tujague; Kim Valenta; Sarie Van Belle; Natalie Vasey; Robert B Wallace; Gilroy Welch; Patricia C Wright; Giuseppe Donati; Luca Santini Journal: Proc Natl Acad Sci U S A Date: 2022-10-10 Impact factor: 12.779