R E S E A R CH A R T I C L E Fermented food consumption in wild nonhuman primates and its ecological drivers 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 Shanee PhD39 | Antonio Souto40 | Jo~ao Pedro Souza-Alves40 | Fiona Stewart20 | Kathrine M. Stewart21 | Anita Stone41 | Binghua Sun42 | Stacey Tecot43 | Kim Valenta44 | Erin R. Vogel45 | Serge Wich20 | Yan Zeng46 1Department of Anthropology, Northwestern University, Evanston, Illinois 2Escuela de Biología, Universidad de Costa Rica, UCR, San José, Costa Rica 3Institute for Conservation Research, San Diego Zoo Global, San Diego, California 4Department of Anthropology, Portland State University, Portland, Oregon 5Department of Biology, Federal Rural University of Pernambuco, Recife, Pernambuco, Brazil 6Department of Anthropology, Hunter College of the City University of New York, New York, New York 7The New York Consortium in Evolutionary Primatology (NYCEP), City University of New York, New York, New York 8Amazon Mammals Research Group, National Amazon Research Institute (INPA), Manaus, AM, Brazil & Department of. Zoology, Federal University of Pernambuco, Recife, Prince Edward Island, Brazil 9Laboratório de Primatologia, Escola de Ciências da Saúde e da Vida, Pontifícia Universidade Católica do Rio Grande do Sul, PUCRS, Porto Alegre, RS, Brazil 10Department of Biology, Rhodes College, Memphis, Tennessee 11Department of Anthropology, California State University Northridge, Northridge, California 12Department of Anthropology, Center for the Advanced Study of Human Paleobiology, George Washington University, Washington, District of Columbia 13School of Life Sciences, University of KwaZulu-Natal, Pietermaritzburg, South Africa 14Shaanxi Key Laboratory for Animal Conservation, Northwest University, Xi'an, China 15School of Life Sciences, Sun Yat-Sen University, Guangzhou, China 16Department of Anthropology and Environmental Studies Program, California State University Fullerton, Fullerton, California 17Centre for Ecological and Evolutionary Synthesis (CEES), University of Oslo, Oslo, Norway 18Southern Swedish Forest Research Centre, Swedish University of Agricultural Sciences (SLU), Alnarp, Sweden 19Department of Human Behavior, Ecology and Culture, Max-Planck-Institute for Evolutionary Anthropology, Leipzig, Germany 20School of Biological and Environmental Sciences, Liverpool John Moores University, Liverpool, United Kingdom 21Centre for Research and Conservation, Royal Zoological Society of Antwerp, Antwerp, Belgium Received: 3 June 2020 Revised: 3 February 2021 Accepted: 10 February 2021 DOI: 10.1002/ajpa.24257 Am J Phys Anthropol. 2021;1–18. wileyonlinelibrary.com/journal/ajpa © 2021 Wiley Periodicals LLC 1 https://orcid.org/0000-0003-2722-9414 https://orcid.org/0000-0001-6246-1265 https://orcid.org/0000-0001-5446-8563 https://orcid.org/0000-0003-1456-6948 https://orcid.org/0000-0002-4722-0532 https://orcid.org/0000-0002-5400-845X https://orcid.org/0000-0002-4137-2404 https://orcid.org/0000-0001-9217-3053 https://orcid.org/0000-0003-2191-6918 https://orcid.org/0000-0001-8770-8148 https://orcid.org/0000-0003-2088-0028 https://orcid.org/0000-0002-0612-2514 https://orcid.org/0000-0002-4674-537X https://orcid.org/0000-0001-5993-0956 https://orcid.org/0000-0002-2454-0912 https://orcid.org/0000-0001-5573-6208 https://orcid.org/0000-0003-1692-1958 https://orcid.org/0000-0002-8517-1276 https://orcid.org/0000-0002-4929-4711 http://wileyonlinelibrary.com/journal/ajpa http://crossmark.crossref.org/dialog/?doi=10.1002%2Fajpa.24257&domain=pdf&date_stamp=2021-03-02 22Laboratório de Primatologia, Departamento de Zootecnia e Ciências Biológicas, Universidade Federal de Santa Maria, Palmeira das Missões, RS, Brazil 23School of Human Sciences, The University of Western Australia, Perth, Australia 24Centre for Evolutionary Biology, School of Biological Sciences, The University of Western Australia, Perth, Australia 25Department of Human Evolution, Max Planck Institute for Evolutionary Anthropology, Leipzig, Germany 26Department of Anthropology, Northern Illinois University, DeKalb, Illinois 27Africa Research & Engagement Centre, The University of Western Australia, Crawley, Western Australia, Australia 28Department of Anthropology and Archaeology, University of Calgary, Calgary, Canada 29Lester E. Fisher Center for the Study and Conservation of Apes, Lincoln Park Zoo, Chicago, Illinois 30Department of Behavioral Ecology, University of Goettingen, Goettingen, Germany 31Research Group Primate Social Evolution, German Primate Center, Leibniz Institute for Primate Research, Goettingen, Germany 32Department of Anthropology, University College London, London, United Kingdom 33Departamento de Ciencias de la Salud, Universidad Autónoma Metropolitana (UAM), Lerma, Mexico 34Centro Interdisciplinario de Investigación para el Desarrollo Integral Regional (CIIDIR), Unidad Oaxaca, Instituto Politécnico Nacional, Mexico City, Mexico 35Graduate School of Asian and African Area Studies, Kyoto University, Kyoto, Japan 36Department of Zoology and Animal Biodiversity, University of Antananarivo, Antananarivo, Madagascar 37Department of Anthropology, Washington University in St. Louis, St. Louis, Missouri 38Congo Program, Wildlife Conservation Society, Brazzaville, Congo 39Neotropical Primate Conservation, Cornwall, United Kingdom 40Departamento de Zoologia, Universidade Federal de Pernambuco, Recife, Pernambuco, Brazil 41Biology Department, California Lutheran University, Thousand Oaks, California 42School of Resource and Environmental Engineering, Anhui University, Hefei, China 43School of Anthropology, University of Arizona, Tucson, Arizona 44Department of Anthropology, University of Florida, Gainesville, Florida 45Department of Anthropology, Rutgers University, New Brunswick, New Jersey 46Animal Microecology Institute, College of Veterinary, Sichuan Agricultural University, Ya'an, China Correspondence Katherine R. Amato, Department of Anthropology, Northwestern University, Evanston, Illinois. Email: katherine.amato@northwestern.edu Funding information Canadian Institute for Advanced Research 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 influ- ence 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 2 AMATO ET AL. mailto:katherine.amato@northwestern.edu size. It was more likely to occur in larger habitat patches with lower annual mean rain- fall 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. K E YWORD S climate, feeding ecology, fermentation, herbivore defense, human evolution 1 | INTRODUCTION Food fermentation—the anaerobic microbial degradation of carbon compounds into ethanol and/or lactic acid—is a central part of human diet and culture (Tamang & Kailasapathy, 2010). Humans from many cultures regularly incite or direct microbial fermentation of a wide range of foods that include meat and dairy products, grains, fruits, and vegetables (Battcock & Azam-Ali, 1998; Campbell-Platt, 1994; Deshpande, 2000; Tamang et al., 2017). Such foods make up 20 to 40% of the global food supply (Campbell-Platt, 1994). Although not all fermented foods contain ethanol, the majority of anthropological fer- mented food research to date targets ethanol as an indicator of fer- mentation (e.g., Dominy, 2015; Dudley, 2002; Garnier & Valamoti, 2016; Hayden et al., 2013; Kuijt, 2009; Liu et al., 2018; Milton, 2004; Ross et al., 2002; Smalley & Blake, 2003). Directed fermentation by humans has early origins. There is archaeological evidence that humans have engaged in directed fer- mentation of fruits and grains and stored the resulting ethanol in large quantities since �4300 B.C., although some suggest a date as early as 12,500 cal BP (Garnier & Valamoti, 2016; Hayden et al., 2013). Evolu- tionary changes in human genes for processing ethanol and for inter- acting with a major lineage of fermenting bacteria (Lactobacillales) are compatible with an even earlier association with fermented foods, dating back to the divergence of hominids from other primates at �10 Mya (Carrigan et al., 2015; Janiak et al., 2020; Peters et al., 2019). Limited technology for processing and storing food at this time makes it likely that our hominid ancestors relied more heavily on naturally occurring fermented foods. However, some simple forms of directed fermentation, such as burying food items or submerging them in water (Speth, 2017), may have been possible. Why humans have incorporated fermented products so promi- nently into their diet across their evolutionary history is unclear. Fer- mentation is an effective food preservative since it produces locally high concentrations of ethanol and lactic acid that ultimately prevent microbial growth and associated food spoilage (Boulton et al., 1999; Pretorius, 2000; Skinner et al., 1980; Thomson et al., 2005). Addition- ally, the physiological effects of consuming ethanol (i.e., intoxication) are believed to have facilitated social gatherings and rituals (Liu et al., 2018). Accordingly, the modern and ancient contexts in which fermented food use has been documented often suggest central roles of food preservation and socially motivated ethanol acquisition in driving the ubiquity of human fermented food use (Dominy, 2015; Dudley, 2002; Kuijt, 2009; Liu et al., 2018; Milton, 2004; Ross et al., 2002; Smalley & Blake, 2003). However, given genetic evidence that human adaptations for fermented food consumption emerged before the technology associated with its directed production and storage (Carrigan et al., 2015; Janiak et al., 2020; Peters et al., 2019), fermented food consumption may have provided another selective advantage earlier in our evolutionary history. Given their high sugar content, fruits often ferment naturally (Dominy, 2004; Duar et al., 2017; Dudley, 2002; Gorgus et al., 2016; Martinson et al., 2012; Nyanga et al., 2007; Ruiz Rodriguez et al., 2019; Weaver, 2016), making it likely that all frugivorous ani- mals consume some minimum amount of fermented foods. However, overripe fruits in the late stages of fermentation commonly remain in food patches after other fruits have been depleted. As described above, fermentation is distinct from rot or decay in that it involves distinct microbes and precludes the production of most toxic micro- bial byproducts (except ethanol). Therefore, it has been suggested that fruits in the late stages of fermentation could have been a fallback food for increasingly terrestrial hominids during periods of low food availability in patchy woodland environments (Carrigan et al., 2015). Foods in the late stages of fermentation could also convey nutri- tional benefits that provide a selective advantage to consumers year- round. Compared to unfermented foods, fermented foods have higher caloric, free amino acid, and vitamin content (Gobbetti et al., 1994; LeBlanc et al., 2013; Mitchell & Herlong, 1986; NRC, 1998; Tamang et al., 2016). In the wild, many fermented foods contain embedded insects, which provide an additional protein source (Barnett et al., 2017; Braham, 2015; Hodge & Arthur, 1996; Xiaoming et al., 2010). In addition, fermentation improves the digestibility of food by breaking down resistant starch, soluble fiber, toxins, and sec- ondary plant metabolites (Binita & Khetarpaul, 1997; Chaves-López et al., 2014; Gupta et al., 2015; Rollan et al., 2019). For example, some toxic foods, such as blowfish and cassava, can only be consumed after fermentation (Akinrele, 1964; Anraku et al., 2013). Together these properties not only directly affect consumer nutrient intake, but may also result in a more favorable balance among the nutrients of food, which in turn can play a critical role in food selection (Felton et al., 2009). Therefore, foods in the late stages of fermentation could AMATO ET AL. 3 have represented a critical nutritional resource to hominids, particularly as energetically expensive life-history traits such as long juvenile periods, short interbirth intervals, and large brains emerged across evo- lutionary time (Aiello & Key, 2002; Antón et al., 2014; Leonard & Robertson, 1992, 1997). The consumption of other high-quality diet items such as meat and cooked food has also been hypothesized to have provided essential nutritional resources for the development and maintenance of these traits in hominids (Aiello & Wells, 2002; DeCa- sien et al., 2017; Wrangham, 2009; Wrangham & Conklin– Brittain, 2003). Fermented foods contain live microbes, substrates for microbial metabolism, and microbial metabolites, which may affect consumer health and fitness either directly or indirectly through impacts on the microbiome (Jacobsen et al., 1999; Kim et al., 2016; Maldonado-Gómez et al., 2016; Marco et al., 2017). Given the broad effects of the micro- biome on host metabolism (Oliphant & Allen-Vercoe, 2019; Visconti et al., 2019), immune function (Al Nabhani & Eberl, 2020), and neuroen- docrine dynamics (Cryan et al., 2019; Sylvia & Demas, 2018), fermented foods have the potential to affect consumer physiology in many ways. Beyond intoxication caused by excessive consumption of fermented foods with high ethanol content, none of these documented physiologi- cal effects are negative. Therefore, fermented food consumption could have provided a selective advantage to hominids in addition to the nutri- tional advantages discussed above. Indeed, studies of human fermented food use consistently demonstrate a range of improved health out- comes (e.g., Bourrie et al., 2016; Burton et al., 2017; Yartey et al., 1995). However, the wide variety of positive health effects that fermented foods can produce via the microbiome make it difficult to predict spe- cific scenarios in which these properties would be most evolutionarily advantageous based on current knowledge. Even in the context of nutrition, modern human technology, and cultural practices complicate our ability to evaluate the potential fit- ness benefits of human fermented food consumption. As a result, comparative data from nonhuman primates (hereafter primates) are essential for exploring the adaptive function of this behavior. By determining how pervasive consumption of late-stage fermented foods by wild primates is and the ecological contexts in which it occurs, we can begin to more accurately assess the ecological and evolutionary forces that drive it and contextualize it within human evolutionary history. Nevertheless, few studies on this subject have incorporated primate data. A handful of comparative genetic analyses of physiological adap- tations for fermented food consumption integrate data from multiple primate species (Carrigan et al., 2015; Janiak et al., 2020; Peters et al., 2019). Additionally, some behavioral research has investigated primate ethanol affinity in response to the Drunken Monkey Hypoth- esis (Dudley, 2002, 2004). This hypothesis posits that humans direct the production of fermented foods and consume them as a result of our affinity for ethanol, which stems from our evolutionary past as frugivorous primates that used ethanol as an olfactory and/or gusta- tory signal for energy-rich fruit (Dudley, 2002, 2004). Therefore, data from other primates have been used to test the relationship between frugivory and ethanol affinity. The results indicate that primates across the Order prefer solutions of 2%–5% ethanol over water (Dausch Ibañez et al., 2019; Gochman et al., 2016; Hockings et al., 2015; Kornet et al., 1990; Mandillo et al., 1998). However, data from spider monkeys (Ateles geoffroyi) indicate that sweet solutions are preferred over etha- nol regardless of calorie content (Dausch Ibañez et al., 2019). Outside of this context, fermented food consumption is rarely mentioned in studies of primate feeding ecology, despite the fact that not all fer- mented foods contain ethanol but all of them likely confer a range of nutritional and health benefits to consumers. As a first step to address this knowledge gap, we compiled qualita- tive data describing overripe fruit consumption from primate field stud- ies around the world to estimate the minimum prevalence of late-stage fermented foods in wild primate diets, regardless of ethanol content, and the ecological contexts in which the consumption of these foods occurs. We hypothesized that local climate, primate socioecological traits, and habitat patch size (Table 1) would predict the prevalence of primate con- sumption of late-stage fermented foods. First, climate affects both the rate of fermentation and the rate of ethanol evaporation (Isu & Njoku, 1998), thereby influencing the local prevalence of late-stage fer- mented foods and the probability that primates will detect them via olfaction (Dominy, 2004; Melin et al., 2019; Nevo & Valenta, 2018). Therefore, we predicted that mean minimum annual temperature, mean maximum annual temperature, mean daily temperature, mean annual rainfall, elevation, and latitude and longitude would be associated with the occurrence of late-stage fermented food consumption in wild pri- mates. Given that fruit ferments easily in nature (Dominy, 2004; Duar et al., 2017; Dudley, 2002; Gorgus et al., 2016; Martinson et al., 2012; Nyanga et al., 2007; Ruiz Rodriguez et al., 2019; Weaver, 2016), we predicted that primate species and populations with high percentages of fruit in their diets and low percentages of leaves and invertebrates would be more likely to encounter and consume late-stage fermented food. Since home range, social group size, body size, and encephalization quo- tients are often correlated with diet (Clutton-Brock & Harvey, 1980; Dunbar & Shultz, 2007, 2017; Kudo & Dunbar, 2001), we also expected these variables to be associated with late-stage fermented food con- sumption. Finally, due to the relationship between habitat patch size and food availability more generally (Abbas et al., 2011; Fahrig, 2003; Laurance et al., 2000), we predicted that habitat patch size would predict the prevalence of late-stage fermented foods and their consumption. 2 | MATERIALS AND METHODS 2.1 | Behavioral data collection KRA, YZ, and TME identified a group of researchers who had com- pleted a wild primate field study of at least nine consecutive months using multiple approaches. We searched two general online databases (https://scholar.google.com, http://xueshu.baidu.com) using specific keywords such as “primate” and “diet” combined with primate family names one year at a time beginning with 2005. We also reviewed the literature cited in multiple primate ecology books (Brady & Carville, 2012; Campbell et al., 2011; Davies & Oates, 1994; 4 AMATO ET AL. https://scholar.google.com http://xueshu.baidu.com Dudley, 2014; NRC, 2003; Rowe & Myers, 2016; Strier, 2016). Finally, we flagged abstracts from the programs of primate conferences in 2018 and 2019, including the American Society of Primatologists and the American Association of Physical Anthropologists. KRA asked 151 researchers with relevant field studies and cur- rent email contact information to report whether they had observed their study subjects consuming fermented foods (i.e., plant foods overripe or fermenting based on their color, physical traits, smell, or other useful indicators). These food items could be found on the gro- und, but this was not necessary for a food to be deemed “fermented.” Many fruits consumed by primates are likely to have undergone some degree of fermentation (Dominy, 2004), but only late stages of fer- mentation with higher concentrations of ethanol and other microbial products (Biale, 1954) are likely to be identified using the conservative sensorial cues we employed here. For example, Astrocaryum standleyanum unripe and ripe fruits are reported to have 0% and 0.6% ethanol while fallen fruits have 0.9% ethanol and overripe fallen fruits have 4.5% ethanol (Dudley, 2004). Therefore, it is likely that we are excluding a substantial number of fermented foods from our analysis (e.g., floral nectar and fruits with other levels of maturity; Aleksey Maro, personal communication; Wiens et al., 2008; Weaver, 2016). However, our approach still represents an important contribution to this complex subject since foods that can be sensorially identified as being in the late stages of fermentation are more likely to have physi- ological effects on consumers as a result of higher concentrations of microbes and/or microbial by-products (Tamang et al., 2016). System- atic data describing chemical and microbial variables in wild fruits are necessary to more accurately quantify fermentation stages in wild food items and the probability of detection by foragers and observers. Because these traits likely vary across plant species, primate species, and environments, such an analysis is outside the scope of this study. Nevertheless, given that the ethanol content of the small number of ripe fruit species that have been measured in habitats occupied by wild primates is reported to range from 0.01% to 1.1% (Dominy, 2004; Dudley, 2004; Weaver, 2016), our conservative esti- mate is that late-stage fermented fruits in our study have an ethanol content >1%. No data exist to allow estimates of microbial biomass or concentrations of non-ethanol microbial by-products. We collated data for 40 species of primates inhabiting 50 research sites (Table S1). While these data encompass a small percentage of all extant primate species (7.9%, 40 of 504 recognized species; Estrada et al., 2017), 11 of the 16 extant primate families were represented across all continents inhabited by primates, and we included both tropical and temperate environments. Therefore, we believe that our database fairly represents the phylogenetic and geographic diversity of the order Primates. Study duration ranged from 9 to 312 months (median = 15 months), and we used data from multiple social groups or communities of 18 species distributed across 13 sites. We included data describing the location and length of the study, the elevation, mean annual maximum and minimum temperatures, mean daily tem- perature, and mean annual rainfall of the study site, the mean contri- bution of fruits, leaves, and invertebrates to the diet of the study species, the frequency with which any fermented foods were consumed relative to total observation time, and any other relevant details about the types of foods consumed or associated behavior, such as seasonality or specific handling behaviors (Table S1). 2.2 | Physical and chemical traits of consumed late-stage fermented foods For all late-stage fermented foods consumed, we compiled data from each study site or the literature describing the presence/absence of a tough husk or skin, relative fiber content, and presence/absence of secondary metabolites and their concentrations. We evaluated tough husks qualitatively. A relative assessment of fiber content compared to other fruits at the same site was possible for 35 fruits, and for 25 of these fruits, the nutritional data were available for that study site specifically. Secondary metabolite data were more difficult to compile. Quantitative data were available for 11 fruit species at three sites. For the rest of the fruits, we searched the literature using the fruit species name combined with terms such as “toxin” and “second- ary metabolite.” Because data describing secondary metabolite con- tent in fruits is sparse, in many cases we had to rely on literature describing medicinal use that implied increased concentrations of identified or unidentified secondary metabolites. Using this approach, we were able to find evidence of the occurrence of secondary metab- olites for 34 fruit species (Table 3). 2.3 | Data analysis We assessed the influence of 18 predictor variables (Table 1) on the occurrence of late-stage fermented food consumption via generalized lin- ear mixed-effects models (GLMM; Zuur et al., 2009) with a binomial distri- bution and logit link function using the function “lmer” of the R package lme4 (Bates et al., 2015). We specified the occurrence of late-stage fer- mented food consumption as a binary response variable, all the predictor variables as fixed factors, and study site as a random factor to account for data from repeated measures of the same species in different social groups at the same site. In addition to socioecological, climate, and habitat patch size variables, we included study length in all of our models to deter- mine if shorter studies were biased against what we assumed would be a relatively rare behavior (Souza-Alves et al., 2019). To avoid over- parameterization and problems of convergence with the global model, we did not consider variable interactions (see Grueber et al., 2011). We also did not include variables describing primate taxonomy because limited replication of species reduced the power of the analysis to assess the impact of these variables. Given differences in scale among the predictor variables, we stan- dardized them using the “standardize” function of the package MuMIn (Barton, 2020) as recommended by Grueber et al. (2011). We avoided multicollinearity problems by only including those variables with Variance Inflation Factors (VIF) <3 into the models (Zuur et al., 2009) using the “vifstep” function of the package usdm (Naimi et al., 2014). The seven var- iables with VIF >3 that we excluded from the global model were female AMATO ET AL. 5 body mass, male body mass, male relative encephalization quotient, per- centage of leaves in the diet, percentage of invertebrates in the diet, mean daily temperature, and elevation. We selected models with an ΔAICc <2 as the most parsimonious (Grueber et al., 2011). Given the occurrence of multiple equally parsimoni- ous models, we also performed full-model averaging on all models with an ΔAICc <2 to account for model uncertainty and to identify the best pre- dictors of patterns of late-stage fermented food consumption in our data set (Grueber et al., 2011). We used the “model.avg” function of the R package MuMIn to identify the averaged model and the predictor weight ( P wi) of each variable. We determined the coefficient of determination for each model with ΔAICc <2 using the MuMIn “r.squaredGLMM” func- tion. We performed all statistical analyses in R 3.6.3 (R CoreTeam, 2020). 3 | RESULTS 3.1 | Occurrence of late-stage fermented food consumption in wild primates Out of 40 species of wild primates studied at 50 sites, 15 species (37.5%) were reported to consume late-stage fermented foods at 23 sites in 12 countries across four continents (Figure 1). Overall, late- stage fermented food consumption occurred infrequently (Table 2, S1). We estimated that it constituted from 0.01% to 3% of the annual diet in most groups, although there were seasonal differences. For example, we found that late-stage fermented fruits could account for as much as 15% of the feeding records of Cebus imitator and Alouatta guariba clam- itans during some seasons. For some primates, such as A. guariba clam- itans, these seasons represented periods of low food availability (VBF personal observation), whereas, for many others, such as C. imitator, they did not (EKM personal observation). While we recorded late-stage fermented food consumption in all our Pan paniscus and C. imitator social groups (three and seven, respectively), not all populations or social groups of the other species studied exhibited this behavior. 3.2 | Main sources of late-stage fermented foods and behavioral strategies used Late-stage fermented food consumption was limited to fruits (Figure 2, Tables 2, 3, S1). The richness of late-stage fermented fruits exploited ranged from one to nine fruit species for a given primate species (Tables 2, 3, S1). Pan paniscus exhibited the highest richness of late-stage fermented fruit species in the diet (N = 9 fruit species), followed by Ateles geoffroyi (N = 8), Alouatta guariba clamitans (N = 7), and Cebus imitator (N = 5; Table 2). The remaining primate species exploited between one and three fruit species (Table 2). At least 31 of the 44 fruit species that were consumed in the late stages of fermentation have defenses in the form of difficult-to- break tough husks/skins (N = 16) or secondary metabolites, such as alkaloids, acetogens, saponins, and tannins (N = 25; Table 3). Almost TABLE 1 Potential predictors of fermented food consumption analyzed in this study Variable Description Socioecological traits 1. Percent leaves in diet Proportion of immature and mature leaves in diet 2. Percent fruit in diet Proportion of immature and mature fruits in diet 3. Percent invertebrates in diet Proportion of insects and other invertebrates in diet 4. Home range Size of the home range for each study group (ha) 5. Group size Number of members of each study group including adults, subadults, juveniles, and infants 6. Male body mass Adult male body mass (kg) in each study species 7. Female body mass Adult female body mass (kg) in each study species 8. Female relative encephalization quotient Endocranial volume (cc) of the adult individuals divided by adult female body mass (kg) 9. Male relative encephalization quotient Endocranial volume (cc) of the adult individuals divided by adult male body mass (kg) Climate 10. Latitude Latitude (decimal degrees) in which each study site is located 11. Longitude Longitude (decimal degrees) in which each study site is located 12. Mean annual rainfall Annual mean rainfall (mm) in each study site according to the local meteorological stations 13. Mean annual maximum temperature Annual mean maximum temperature (�C) recorded by the local meteorological stations 14. Mean annual minimum temperature Annual mean minimum temperature (�C) recorded by the local meteorological stations 15. Mean daily temperature Daily mean temperature (�C) recorded by the local meteorological stations 16. Elevation Representative elevation (m) of study site Habitat quality 17. Habitat size Size of the habitat occupied by each study group (ha); proxy for fragmentation Sampling Effort 18. Study length Number of months during which data were collected 6 AMATO ET AL. all fruits (95%) were consumed both ripe/unfermented and overripe/ fermented (Table 3). In some cases, late-stage fermented fruits were only consumed when the patch was depleted of ripe fruits (Table S1). We also reported cases in which very ripe or late-stage fermented fruits appeared to be preferred over semi-ripe and unripe fruits. Specifically, Cebus imitator at La Suerte, Costa Rica, was observed frequently knocking ripe Dipteryx oleifera (Fabaceae) fruits to the ground and returning up to 2 weeks later to consume them (up to 15% of feeding time seasonally, EKM personal observation). These fruits were never consumed unfermented by the capuchins. Eulemur fulvus at Ampijiroa, Madagascar (up to 5% of feeding time seasonally, PTR personal observation) and Ateles geoffroyi at Punta Laguna, Mexico (up to 1% of feeding time seasonally, BPG personal observation) were also reported to drop fruits to the ground and return to feed on them later. However, unlike the capuchins, both lemurs and spider monkeys consumed the target fruits in different stages of ripening, although the lemurs appeared to prefer fallen fruits over those on the trees since they would consume fallen fruits first when both were available. 3.3 | Main primate predictors of late-stage fermented fruit consumption Only climate and habitat patch size were strong predictors of late-stage fermented food consumption in wild primates. Other socioecological traits did not contribute substantially to any of our top-ranked models. We found six GLMMs equally parsimonious (ΔAIC < 2) for explaining the observed patterns in late-stage fer- mented food consumption (Table 4). These models included mean maximum and minimum annual temperature, mean annual rainfall, habitat patch size, mean minimum annual temperature, longitude, home range size, and female relative encephalization quotient and explained �99% of the observed variance (Table 4). However, only mean annual maximum temperature, rainfall, and habitat patch size were present in all six models. The model with the strongest empiri- cal support (ΔAICc = 0.00) included these three variables and mean minimum annual temperature (Table 4). The averaged model explained 99% of the observed variance, and late-stage fermented food consumption was only strongly negatively predicted by annual mean rainfall and and positively predicted by mean annual maximum temperature and habitat patch size (Table 4). 4 | DISCUSSION We found that wild primates from all major evolutionary lineages con- sume foods in the later stages of fermentation, although the behavior is relatively infrequent and limited to only a few species of fruits at the sites where we recorded it. Additionally, climatic and environmen- tal variables generally predict the occurrence of late-stage fermented food consumption better than socioecological variables. Specifically, late-stage fermented food consumption is more common in hotter, drier environments and larger, presumably less fragmented, habitats. F IGURE 1 Wild primates consuming fermented fruits. (a) Chlorocebus djamdjamensis consuming L. abyssinica at Kokosa, Ethiopia; credit Addisu Mekonnen (b) Cebus capucinus imitator consuming D. oleifera at La Suerte Biological Field Station, Costa Rica; credit: Liz Rasheed (c) Pan paniscus consuming A. mannii at LuiKatole, Democratic Republic of Congo; credit Gottfried Hohmann (d) Ateles geoffroyi consuming M. zapota at Punta Laguna, Mexico; credit Fabrizio Dell'Anna (e) Alouatta guariba clamitans consuming P. guajava at Parque S~ao Paulo, Brazil; credit Claudio Godoy (f) Macaca assamensis consuming N. cadamba at Phu Khieo Wildlife Sanctuary, Thailand; credit Oliver Schülke (g) Hapalemur meridionalis consuming Uapaca sp. at Mandena, Madagascar; credit Tim Eppley (h) Callithrix jacchus consuming P. pachycladus at Baracuhy Biological Field Station, Brazil; credit: Filipa Abreu AMATO ET AL. 7 As fermentation is a continuous process, future studies should analyze the chemical and microbial properties of the fermented fruits con- sumed at different stages by the primates to improve the resolution of these relationships. However, our findings provide an important foundation for understanding the ecological and evolutionary forces that drive fermented food consumption in primates and offer new insights into the emergence of this behavior in humans. 4.1 | Occurrence of late-stage fermented food consumption in wild primates First, although reports of fermented food consumption are rare in most studies of wild primate feeding ecology, this behavior is probably pervasive across the Order. We observed late-stage fermented food consumption in more than one-third of the primate species for which we received data. However, given that our data were biased toward late-stage fermentation and many fermented foods consumed by pri- mates cannot be identified by researchers without chemical analyses, it is likely that the prevalence of fermented food consumption among wild primates is even higher. Fruits consumed by primates commonly ferment naturally despite no clear signs to observers that fermenta- tion has occurred (Dominy, 2004; Dudley, 2002; Aleksey Maro, per- sonal communication; Weaver, 2016). Given that most primates, even those considered leaf-eaters, rely heavily on fruit during at least part of the year (Campbell et al., 2011; Rowe, 2018; Sussman, 1991), it is likely that most primates regularly consume fermented foods. This scenario becomes more probable when we consider the fact that other foods such as nectar or gums may also often ferment despite being difficult to observe (e.g., Wiens et al., 2008). Because the rela- tive concentrations of ethanol and other microbial products at differ- ent stages of fermentation—and the likelihood of perception by foraging primates—are likely to vary by plant species, primate species, and habitat, quantitative data describing these variables for a range of food items are necessary to better define fermentation stages in wild foods, and to test the extent to which primate ecology varies with food fermentation stage. This area presents exciting opportunities for future research. Nevertheless, we do not expect that all primates consume fer- mented fruits. For instance, primates of the subfamily Colobinae, TABLE 2 Wild primate species reported to consume fermented fruits Primate species Family Country Study sitea # groups Fruitsb %TFTc Locationd Alouatta caraya Atelidae Brazil ECB 1 1 T Alouatta guariba clamitans Atelidae Brazil CISM, RE, PSP, PEI 7 1–7 <0.5–2 T, G Ateles geoffroyi Atelidae Mexico, Panama PL, RBMA, EPO, BCI 5 8–15 <0.5–1 T, G Callithrix jacchus Callitrichidae Brazil BBFS 1 16,17 0.5 G Cebus imitator Cebidae Costa Rica LSBFS, SSR 6 12, 18–21 <1 G Macaca thibetana Cercopithecidae China Huangshan 1 2 G Chlorocebus djamdjamensis Cercopithecidae Ethiopia Kokosa 1 22 <1 G Macaca assamensis Cercopithecidae Thailand PKWS 1 23,24 0.01 G Papio anubis Cercopithecidae Uganda KNP 1 25 <3 G Pan troglodytes troglodytes Hominidae Republic of Congo Goualougo 1 26–28 G Pan paniscus Hominidae DRC LuiKotale, Lomako 3 29–37 T Gorilla gorilla Hominidae Republic of Congo Goualougo, Mondika 3 26,36,38 G Pongo pygmaeus wurmbii Hominidae Indonesia Tuanan 1 39–41 <<0.01 T Eulemur fulvus Lemuridae Madagascar Ampijoroa 1 42,43 5 G Hapalemur meridionalis Lemuridae Madagascar Mandena 1 43,44 <0.01 T Total = 15 6 12 23 34 44 aStudy sites: ECB = Estancia Casa Branca, CISM = Campo de Instruiç~ao de Santa Maria, RE = Reserva Econsciência, PSP = Parque S~ao Paulo, PEI = Parque Estadual de Itapu~a, PL = Punta Laguna, RBMA = Reserva de la Biósfera Montes Azules, EPO = Ejido Zamora Pico de Oro, BCI = Barro Colorado Island, BBFS = Baracuhy Biological Field Station, LSBFS = La Suerte Biological Field Station, SSR = Sector Santa Rosa, Area de Conservacion Guanacaste, PKWS = Phu Khieo Wildlife Sanctuary, KNP = Kibale National Park. bFruit species: 1 = Phytolacca dioica, 2 = Diospyros kaki, 3 = Citrus reticulata, 4 = Campomanesia xanthocarpa, 5 = Eugenia rostrifolia, 6 = Enterolobium contortisiliquum, 7 = Psidium guajava, 8 = Manilkara zapota, 9 = Enterolobium cyclocarpum, 10 = Spondias pupurea, 11 = S. radlkoferi, 12 = S. mombin, 13 = Astrocaryum standleyanum, 14 = Quararibea asterolepis, 15 = Ampelocera hottlei, 16 = Annona muricata, 17 = Pilosocereus pachycladus,18 = Dipteryx oleifera, 19 = Manilkara chicle, 20 = Stemmadenia obovata, 21 = Byrsonima crassifolia, 22 = Lagenaria abyssinica, 23 = Neolamarkia cadamba, 24 = Gmelina arborea, 25 = Mimusops sp., 26 = Treculia Africana, 27 = Gambeya lacourtiana, 28 = Detarium macrocarpum, 29 = Parinari congensis, 30 = Gilbertiodendron dewevrei, 31 = Mammea africana, 32 = Guibourtia demeusei, 33 = Dialium angolense, 34 = D. pachyphyllum, 35 = D. corbisieri, 36 = Anonidium mannii, 37 = Pouteria cf. malaccensis, 38 = Klainedoxa gabonensis, 39 = Diospyros pseudomalabarica, 40 = Ficus sundaica, 41 = Landolphia myrtifolia, 42 = Vangueria madagascariensis, 43 = Uapaca sp., 44 = Syzygium emirnense. cPercentage of total feeding time. No available information is indicated with . dLocation where food consumed: T = tree, G = ground. 8 AMATO ET AL. which are physically unable to consume large amounts of ripe fruits as a result of their sacculated foregut (Davies & Oates, 1994), as well as immature fruit specialists, such as the Neotropical Pitheciinae, were not observed consuming fermented fruit (at least not clearly overripe fruits) in any context in this study. Additionally, the physical nature of some habitats can reduce access to fermented fruits. For example, while not represented in our data set, swamps and riverbank forests reduce opportunities for fruit fermentation on the ground, and fruits in these habitats are often water-dispersed and rarely fleshy and eas- ily fermentable (López, 2001). 4.2 | Ecological contexts associated with late-stage fermented food consumption by wild primates Despite how relatively common late-stage fermented fruit con- sumption appears to be throughout the Order Primates, we found that it is selectively employed in specific ecological contexts. Although most primates include many fruit species in their diets, in most cases only one or two fruit species were consumed in the late stages of fermentation by a given primate population or social group. In some cases, this pattern appeared to be a result of pri- mates extending the utility of a fruit patch. For example, in the rare instances when Pongo pygmaeus was observed consuming late-stage fermented fruits, it was after the patch had been depleted by other frugivores (ERV personal observation). Alternatively, some primates, such as groups of Alouatta guariba clamitans in Santa Maria munici- pality, Southern Brazil, appeared to rely on late-stage fermented fruits during periods of low or altered food availability (VBF per- sonal observation). Similarly, Ateles geoffroyi on Barro Colorado Island, Panama utilized late-stage fermented Quararibea asterolepis during a period of unusual fruiting patterns associated with the pre- vious year's El Niño event, as did other frugivorous mammals and birds (Campbell, 2000). These potential uses of late-stage fermented foods as fallback foods are in line with previous hypotheses in other contexts (Carrigan et al., 2015). Other primates appeared to use fermentation to increase fruit edibility. Many fruits contain secondary metabolites, and in some cases they may reach sufficient levels to have meaningful physiologi- cal effects if consumed in large quantities (Cipollini & Levey, 1997; Janzen, 1983). At least two-thirds of the fruit species consumed in the late stages of fermentation by wild primates in this study had mechan- ical or chemical herbivore defenses when unfermented. For seven of these species, primates were reported to reject fruits unless they were very ripe or fermented. Pan troglodytes has been previously shown to preferentially consume ripe fruits of plant species whose unripe fruits have high levels of tannins since ripening reduces tannin content (Wrangham & Waterman, 1983). Therefore, it is possible that fermen- tation was used by some of our study subjects in a similar way to break down plant herbivore defenses. For example, Dipteryx oleifera, has a hard husk that can only be breached by Cebus imitator when fer- mented (EKM personal observation). F IGURE 2 Fruits consumed fermented by wild primates. (a) Lagenaria abyssinica, credit: Addisu Mekonnen (b) Stemmadenia obovata, credit: Amanda Melin (c) Vangueria madagascariensis, credit: Tojotanjona Razanaparany (d) Spondias mombin, credit: Amanda Melin (e) Landolphia myrtifolia, credit Tojotanjona Razanaparany (f) Diospoyros kaki, credit Bingua Sun AMATO ET AL. 9 T A B L E 3 C ha ra ct er is ti cs o f fr ui t sp ec ie s co ns um ed fe rm en te d P la nt sp ec ie s Fa m ily G F a Fr ui t tr ai ts R ef er en ce sb T yp e Si ze (c m ) T o ug h hu sk Se co nd ar y m et ab o lit es R el at iv e fi b er co n te n t A m pe lo ce ra ho tt le i U lm ac ea e T F le sh y 2 .5 N o A nn on a m ur ic at a A nn o na ce ae T F le sh y 1 5 –3 5 N o Y es (a lk al o id s, ac et o ge ni ns ) B ad ri e an d Sc h au ss 2 0 1 0 ,G aj al ak sh m ie t al . 2 0 1 2 ,B o ak ye et al .2 0 1 5 A no ni di um m an ni ic A nn o na ce ae T F le sh y 2 5 –4 0 Y es N o d M o de ra te d M as ie t al .2 0 1 2 ,D je u ss ie t al .2 0 1 3 A st ro ca ry um st an dl ey an um A re ca ce ae T D ry 2 –4 Y es M o de ra te B yr so ni m a cr as si fo lia M al pi gh ia ce ae T F le sh y 2 –3 N o M o de ra te d C am po m an es ia xa nt ho ca rp a M yr ta ce ae T F le sh y 1 –2 .5 N o Y es (p he no ls ) P er ei ra et al .2 0 1 2 ,d a Si lv a et al .2 0 1 6 C it ru s re ti cu la ta R ub ia ce ae T F le sh y 4 –8 N o Y es M o ra vv ej et al .2 0 1 0 ,E ze ab ar a et al .2 0 1 4 D et ar iu m m ac ro ca rp um F ab ac ea e T D ry 7 –1 0 Y es Y es (s ap o ni ns ) M o de ra te U m ar u et al .2 0 0 7 D ia liu m an go le ns ee F ab ac ea e T D ry N o Y es d Lo w d D ia liu m co rb is ie ri e F ab ac ea e T D ry N o Y es d Lo w d M al o u ek ie t al .2 0 1 5 D ia liu m pa ch yp hy llu m e F ab ac ea e T D ry N o Y es d Lo w d D io sp yr os ka ki d E be na ce ae T F le sh y 4 –7 N o Y es (p ro an th o cy an o ge n) Lo w U ts u n o m iy a et al .1 9 9 8 ,S in gh et al .2 0 1 1 D io sp yr os ps eu do -m al ab ar ic a E be na ce ae T F le sh y Y es Y es (t an ni ns ) M o de ra te d M ar id as s et al .2 0 0 8 ,P ra sa d an d R av ee n d ra n 2 0 1 1 ,I sl am et al .2 0 1 9 D ip te ry x ol ei fe ra f F ab ac ea e T D ry 4 –6 Y es En te ro lo bi um co nt or ti si liq uu m c F ab ac ea e T D ry 4 –1 0 Y es Y es (s ap o ni ns ) H ig h B o n el -R ap o so et al .2 0 0 8 ,M at lo u b et al .2 0 1 5 , G am al E l- D in et al .2 0 1 7 ,M ac h ad o et al .2 0 1 9 , A b d el -M ag ee d et al .2 0 1 9 En te ro lo bi um cy cl oc ar pu m F ab ac ea e T D ry 7 –1 5 Y es Y es M o de ra te d H es s et al .2 0 0 3 ,B ab ay em i2 0 0 6 ,L o p ez -E sc o b ar 2 0 1 4 ,G am al E l- D in et al .2 0 1 7 Eu ge ni a ro st ri fo lia M yr ta ce ae T F le sh y 1 –2 N o Fi cu s su nd ai ca M o ra ce ae T F le sh y N o N o M o de ra te d G am be ya la co ur ti an a Sa po ta ce ae T F le sh y 9 N o Y es (t an ni ns ,p he no ls ) Lo w M as ie t al .2 0 1 2 G ilb er ti od en dr on de w ev re ie F ab ac ea e T D ry Y es Y es d Lo w d G m el in a ar bo re a La m ia ce ae T F le sh y 2 –3 N o Y es bu t lo w (t an ni ns ,p he no ls ) Lo w d A m at a 2 0 1 2 ,N ay ak et al .2 0 1 2 ,N ay ak et al ., 2 0 1 3 G ui bo ur ti a de m eu se ie F ab ac ea e T D ry N o N o d Lo w d K la in ed ox a ga bo ne ns is Ir vi ng ia ce ae T F le sh y 6 Y es Y es (t an ni ns ,p he no ls ) H ig h M as ie t al .2 0 1 2 La ge na ri a ab ys si ni ca f C uc ur bi ta ce ae V F le sh y 5 –1 8 Y es Y es Lo w /m o de ra te P ar ke r et al .2 0 0 7 ,R ag u n at h an an d So lo m o n 2 0 0 9 ,A m as al u et al .2 0 1 8 La nd ol ph ia m yr ti fo lia c A po cy na ce ae V F le sh y Y es N o M o de ra te d M am m ea af ri ca na C lu si ac ea e T F le sh y 5 –1 0 N o N o d Lo w d 10 AMATO ET AL. T A B L E 3 (C o nt in ue d) P la nt sp ec ie s Fa m ily G F a Fr ui t tr ai ts R ef er en ce sb T yp e Si ze (c m ) T o ug h hu sk Se co nd ar y m et ab o lit es R el at iv e fi b er co n te n t M an ilk ar a za po ta Sa po ta ce ae T F le sh y 5 –1 5 N o Y es (t an ni ns ,s ap o ni ns ) H ig h d Sh u ie t al .2 0 4 4 ,J am u n a et al .2 0 1 1 ,L o p ez - E sc o b ar 2 0 1 4 M an ilk ar a ch ic le Sa po ta ce ae T F le sh y Y es Y es (t an ni ns ) Lo w d Le o n ti et al .2 0 0 2 M im us op s sp . Sa po ta ce ae T F le sh y N o N o Lo w d B al ig a et al .2 0 1 1 N eo la m ar ki a ca da m ba R ub ia ce ae T F le sh y 5 –7 N o Y es (t an ni ns ,p he no ls ) M o de ra te d M as ie t al .2 0 1 2 ,D je u ss ie t al .2 0 1 3 ,I sl am et al . 2 0 1 5 Pa ri na ri ex ce ls a C hr ys o ba la na ce ae T F le sh y N o N o d Lo w d Ph yt ol ac ca di oi ca c P hy to la cc ac ea e T F le sh y 1 –1 .5 N o Y es (s ap o ni ns ) Lo w A sh af a et al .2 0 1 0 ,L ib er to et al .2 0 1 0 Pi lo so ce re us pa ch yc la du s C ac ta ce ae C F le sh y 4 –6 N o (s pi ke s) Po ut er ia cf m al ac ce ns is Sa po ta ce ae T F le sh y Y es N o M o de ra te d Ps id iu m gu aj av a M yr ta ce ae T F le sh y 4 –8 N o Q ua ra ri be a as te ro le pi sc M al va ce ae T D ry 1 –2 N o H ig h Sp on di as m om bi n A na ca rd ia ce ae T F le sh y 2 –4 N o Y es Lo w d A yo ka et al .2 0 0 5 ,A d ed iw u ra an d K io 2 0 0 9 , U ga d u et al .2 0 1 4 Sp on di as ra dl ko fe ri A na ca rd ia ce ae T F le sh y 3 –5 N o Lo w Sp on di as pu rp ur ea A na ca rd ia ce ae T F le sh y 2 –3 N o Y es (p he no ls ) E n ge ls et al .2 0 1 2 St em m ad en ia ob ov at a A po cy na ce ae T D ry 3 0 –3 -5 Y es M o de ra te d Sy zy gi um em ir ne ns e M yr ta ce ae T F le sh y 1 –2 N o Y es d M o de ra te d R az af in d ra ib e et al .2 0 1 3 Tr ec ul ia af ri ca na e M o ra ce ae T F le sh y 3 0 –5 0 Y es Y es d H ig h d U gw u an d O ra n ye 2 0 0 6 ,I je h et al .2 0 1 0 U ap ac a sp p. P hy lla nt ha ce ae T F le sh y 2 –4 N o N o d M o de ra te d M u ch u w et ie t al .2 0 0 6 V an gu er ia m ad ag as ca ri en si sc R ub ac ea e T F le sh y 3 –5 Y es Y es Lo w d M ah o m o o d al ly 2 0 1 4 ,M ar o yi 2 0 1 8 N ot e: In di ca te no av ai la bl e in fo rm at io n. a G ro w th fo rm :T ,t re e; V ,v in e; C ,c ac tu s. b T he en ti re lis t o f re fe re nc es is av ai la bl e in th e Su pp o rt in g In fo rm at io n. c N ev er co ns um ed un ri pe . d D at a av ai la bl e fo r sp ec if ic si te w he re be ha vi o r w as o bs er ve d. e Se ed o r se ed an d m es o ca rp co ns um ed . f N ev er co ns um ed un fe rm en te d. AMATO ET AL. 11 Together, these patterns are compatible with the use of targeted consumption of late-stage fermented fruits in multiple ways by pri- mates as part of a broader nutritional strategy to increase food avail- ability and expand their dietary niches. We found preliminary support for this interpretation. As predicted, our models indicated that late- stage fermented food consumption was associated with climate and habitat patch size. In particular, late-stage fermented food consump- tion was more common in drier environments with more extreme mean annual maximum temperatures, as well as in larger habitat pat- ches. Habitats with higher mean annual maximum temperatures and lower annual rainfall are potentially more nutritionally stressful for pri- mates due to both chronic and seasonal reductions in food availability, as well as distinct plant growth strategies that result in increased mechanical and/or chemical defenses against herbivory (Coley & Barone, 1996; Onoda et al., 2011; Poorter & Kitajima, 2007; Zhao et al., 2013). In such environments, a primate foraging strategy that relied more heavily on late-stage fermented foods could well enhance survival during lean periods by both extending the utility of depleted food patches and increasing the digestibility of heavily defended plant foods. We do not have quantitative data relating food availability or plant-herbivore defenses to late-stage fermented food consumption across sites, precluding our ability to rigorously test this hypothesis here. However, future explorations of this relationship are warranted by our findings. Our results also indicate other potentially important mechanisms driving patterns of primate late-stage fermented food consumption. To some extent, it appears that late-stage fermented food consump- tion occurs with more prevalence in habitats where primates are more likely to come into contact with fruit in the late stages of fer- mentation. Higher mean annual maximum temperatures are likely to result in more rapid rates of fermentation and ethanol evaporation (Isu & Njoku, 1998), increasing the local prevalence of late-stage fer- mented foods and the probability that primates will detect them via olfaction (Dominy, 2004; Melin et al., 2019; Nevo & Valenta, 2018). Furthermore, larger, potentially less fragmented, habitats are often associated with an increased abundance and diversity of fruiting trees (Abbas et al., 2011; Fahrig, 2003; Laurance et al., 2000). There- fore, there may be a higher probability that primates in these habitats will encounter fermenting fruits. However, in our dataset, the effect of habitat patch size appears to be driven by two particularly large sites, Goualougo and Mondika in the Republic of Congo. As a result, it remains unclear whether factors influencing the availability of late- stage fermented foods to primates truly shape patterns of consump- tion more globally. TABLE 4 Best linear mixed models (ΔAICc < 2) and averaged-model that predict the consumption of fermented fruits in 40 wild primate species Predictor variablesa Parametersb Best supported models AICc ΔAICc wi R2c 1. habitat size+rainfall+tmax+tmin 84.5 0 0.11 1.00 2. habitat size+rainfall+tmax 84.5 0.02 0.10 0.99 3. habitat size+longitude+rainfall+tmax 85.5 0.96 0.07 0.99 4. habitat size+home range + rainfall+tmax 85.5 1.02 0.06 0.99 5. habitat size+home range + rainfall+tmax+tmin 86.5 1.96 0.04 0.99 6. female encephalization+habitat size+ rainfall+tmax 86.5 1.99 0.04 0.99 Averaged model (R2 c = 0.99) βi SE 95% CI P wi Intercept −5.2 2.3 (−9.8, −0.6) tmax 7.7 2.7 (2.3, 13.0) 1.00 rainfall −5.7 2.4 (−10.5, −0.9) 1.00 habitat size 4.9 2.0 (1.0, 8.8) 1.00 tmin −4.1 2.0 (−8.2, −0.1) 0.35 longitude 2.6 2.3 (−2.0, 7.2) 0.16 home range 1.4 1.1 (−0.8, 3.6) 0.25 female encephalization −1.1 2.4 (−5.9, 3.8) 0.09 aAbbreviations of predictor variables: tmax = mean maximum ambient temperature, tmin = mean minimum ambient temperature, rainfall = mean annual rainfall. bParameters shown are Akaike's Information Criterion (AICc) for small samples, difference in AICc (ΔAICc), model probability Akaike weights (wi), Pseudo-R 2 (R2c) indicating the percentage of the variance explained by the fixed and random factors, partial regression coefficients of the averaged-model (βi), standard errors that incorporate model uncertainty (SE), 95% confidence intervals for the parameter estimates, relative importance of each predictor variable ( P wi). The degrees of freedom of each model are equal to the number of variables in each model plus two. 12 AMATO ET AL. 4.3 | Potential evolutionary benefits of late-stage fermented food consumption The aforementioned relationships open up new perspectives on the emergence of food fermentation as an important component of the human diet. If late-stage fermented food consumption is part of an extant primate strategy for extending the time over which a particular type of fruit can be fed on and/or increasing the nutritional accessibil- ity of foods, particularly in nutritionally harsh environments or envi- ronments with high levels of inter-specific feeding competition, it may have served a similar role for our hominin ancestors. As hominins diverged from other primates, they began to more consistently occupy a more terrestrial niche (Sponheimer et al., 2013). It has been suggested that fermented fruits may have emerged as a fallback food in this context (Carrigan et al., 2015), and the patterns we observed in extant nonhuman primates provide some support for this hypothesis. Additionally, hominins including Paranthropus and Australopithecus are believed to have incorporated substantial amounts of hard and abra- sive food items, as well as underground plant storage organs, in their diets (Dominy, 2012; Kay, 1985; Plummer, 2004; Teaford & Ungar, 2000). Underground plant storage organs are mechanically challenging, contain more starch and fiber compared to most ripe fruits, and expose foragers to potentially high amounts of diverse sec- ondary plant metabolites that are toxic or can interfere with digestion (Buonocore & Silano, 1986; Dominy et al., 2008; Stahl et al., 1984; Waterman, 1984). Fermentation could have reduced both the fiber and toxin levels in these food items. In fact, fermentation is commonly used to process tubers in modern human contexts (Akinrele, 1964; Ray & Sivakumar, 2009). While the transition to more settled, agrarian communities is often associated with the advent of human fermented food production for food preservation and ritual (Kuijt, 2009; Liu et al., 2018; Ross et al., 2002), the potential nutritional benefits of fer- mentation should not be underestimated. We found evidence that these benefits may be important drivers of late-stage fermented food consumption across the Order Primates. Other nutritional and non-nutritional factors that we could not quantify should also be considered as proximate drivers of late-stage fermented food consumption in primates. First, the nutritional bene- fits of late-stage fermented fruits could be further improved by the presence of insects. While generally composed of small individuals, insect assemblages in fermenting fruit can be diverse and abundant (Braham, 2015; Feinstein et al., 2007; Hodge & Arthur, 1996). Insects can provide fat, protein, vitamins, and amino acids (Xiaoming et al., 2010), and fruit infested with them are known to be selected by some primate species in other contexts (Barnett et al., 2017). Addi- tionally, fermentation is likely to alter food taste. Anecdotal researcher taste tests in our study indicated positive changes in taste with fruit fermentation. Fermentation is generally associated with sour or acid tastes, and humans tend to prefer sweet–sour tastes (Breslin, 2013; Katz, 2012). Little is known about sour taste receptors in primates and other animals—or even sour taste preference (Montell, 2018; Roper, 2007). However, it is likely that primates share an affinity for sour taste with humans. Taste has not been systematically examined in wild primate foods, but it will likely provide additional insight into primate food choices, both fermented and unfermented. Finally, fermented foods are likely to provide health benefits to consumers as a result of probiotic and prebiotic properties (Bourrie et al., 2016; Burton et al., 2017; Löwenadler & Linberg, 1994; Marco et al., 2017; Summer et al., 2017; Tamang et al., 2016; Veiga et al., 2014; Yartey et al., 1995). These properties are likely to be stronger in late-stage fermented foods as a result of increased micro- bial activity, which may explain why these foods are targeted by some primates. Currently, without chemical and microbial data from primate foods as well as physiological and microbial data from primates, it is impossible to assess these potential relationships. However, rapidly emerging evidence of the importance of microbes for primate ecology and evolution (Amato, 2016; Amato et al., 2019; Davenport et al., 2017; Dunn et al., 2020; Gaulke et al., 2018) suggests that these interactions should not be overlooked. 5 | CONCLUSION We find that late-stage fermented fruits are consumed by a variety of nonhuman primates globally. This behavior generally targets a spe- cific subset of fruit species, some of which contain herbivore defenses that are likely degraded by bacterial fermentation. It also occurs more often in hotter, drier environments, and in larger habitat patches. As a result, we suggest that primate late-stage fermented food consumption may be part of a nutritional strategy that increases food availability by increasing the duration across which a particular fruit patch can be used, and expands dietary niche space by degrading some toxins in ripe fruit and providing easily accessible nutrients. It is possible that the human propensity for fermented food consumption is rooted in this ancestral primate strategy, which was favored during the course of human evolution by periods of nutritional stress caused by climate change events and migration to unknown or unfavorable landscapes. Future studies should pair sys- tematic assessments of spatial and temporal patterns of wild primate fermented food consumption with nutritional and microbial analyses of fermented and unfermented food items to further investigate these relationships. ACKNOWLEDGMENTS We thank Jessica Rothman for contributing data from C. ascanius, C. guereza, L. albigena, P. anubis, and P. rufomitratus at Kibale National Park and G. beringei at Bwindi Impenetrable National Park, as well as for her input on earlier versions of the manuscript. The authors would also like to acknowledge a long list of funders, permitting agencies, and people for supporting the fieldwork associated with each field site listed. This list can be accessed in the Supplementary Material. KRA is supported as a fellow in the CIFAR “Humans and the Microbiome” program. She would also like to thank the organizers of the Wenner- Gren Symposium #160 “Cultures of Fermentation,” held on October 11-17, 2019 (C. Warinner, J. Hendy, M. Aldenderfer, M. Rest) for sparking the idea for this paper. AMATO ET AL. 13 AUTHOR CONTRIBUTIONS Oscar Chaves: Methodology; writing-review & editing. Elizabeth Mal- lott: Conceptualization; methodology; writing-review & editing. Timothy Eppley: Data curation; methodology; writing-review & editing. Filipa Abreu: Data curation; writing-review & editing. Andrea Baden: Data curation; writing-review & editing. Adrian Barnett: Data curation; writing-review & editing. Julio Cesar Bicca-Marques: Data curation; writing-review & editing. Sarah Boyle: Data curation; writing-review & editing. Christina Campbell: Data curation; writing-review & editing. Colin Chapman: Data curation; writing-review & editing. María De la Fuente: Data curation; writing-review & editing. Pengfei Fan: Data curation; writing-review & editing. Peter Fashing: Data curation; writing-review & editing. Annika Felton:Data curation; writing-review & editing. Barbara Fruth: Data curation; writing-review & editing. Vanessa Fortes: Data curation; writing-review & editing. Cyril Grueter: Data curation; writing-review & editing. Gottfried Hohmann: Data curation; writing-review & editing.Mitchell Irwin: Data curation; writing-review & editing. Jaya Matthews: Data curation; writing-review & editing. Addisu Mekonnen: Data curation; writing-review & editing. Amanda Melin: Data curation; writing-review & editing. David Morgan: Data curation; writing-review & editing. Nga Nguyen: Data curation; writing-review & editing. Julia Ostner: Data curation; writing-review & editing. Alex Piel: Data curation; writing-review & editing. Braulio Pinacho-Guendulain: Data curation; writing-review & editing. Erika Patricia Quintino Aredes: Data curation. Patrick Razanaparany: Data curation; writing-review & editing. Crickette Sanz: Data curation; writing-review & editing. Nicola Schiel: Data curation; writing-review & editing. Oliver Schülke: Data curation; writing-review & editing. Sam Shanee: Data curation; writing- review & editing. Antonio Souto: Data curation; writing-review & editing. Jo~ao Pedro Souza-Alves: Data curation; writing-review & editing. Fiona Stewart:Data curation; writing-review & editing. Kathrine Stewart: Data curation. Anita Stone: Data curation; writing-review & editing. Binghua Sun: Data curation; writing-review & editing. Stacey Tecot: Data curation; writing-review & editing. Kim Valenta: Data curation; writing-review & editing. Erin R. Vogel: Data curation; writing- review & editing. Serge Wich: Data curation; writing-review & editing. Yan Zeng: Data curation; methodology. CONFLICT OF INTEREST The authors declare no conflicts of interest. OPEN RESEARCH BAGES This article has been awarded badges. All materials and data are publicty accessible via the Open Science Framework at [provided URL]. Learn more about the Open Practices badges from the Center for Open Science: https://osf.io/tvyxz/wiki. DATA AVAILABILITY STATEMENT All data are available in the supplemental material (Table S1). The R code is also available in the supplemental material. ORCID Katherine R. Amato https://orcid.org/0000-0003-2722-9414 Óscar M. Chaves https://orcid.org/0000-0001-6246-1265 Elizabeth K. Mallott https://orcid.org/0000-0001-5446-8563 Timothy M. Eppley https://orcid.org/0000-0003-1456-6948 Andrea L. Baden https://orcid.org/0000-0002-4722-0532 Julio Cesar Bicca-Marques https://orcid.org/0000-0002-5400-845X María Fernanda De la Fuente https://orcid.org/0000-0002-4137- 2404 Barbara Fruth https://orcid.org/0000-0001-9217-3053 Vanessa B. 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Am J Phys Anthropol. 2021; 1–18. https://doi.org/10.1002/ajpa.24257 18 AMATO ET AL. https://doi.org/10.1002/ajpa.24257 Fermented food consumption in wild nonhuman primates and its ecological drivers 1 INTRODUCTION 2 MATERIALS AND METHODS 2.1 Behavioral data collection 2.2 Physical and chemical traits of consumed late-stage fermented foods 2.3 Data analysis 3 RESULTS 3.1 Occurrence of late-stage fermented food consumption in wild primates 3.2 Main sources of late-stage fermented foods and behavioral strategies used 3.3 Main primate predictors of late-stage fermented fruit consumption 4 DISCUSSION 4.1 Occurrence of late-stage fermented food consumption in wild primates 4.2 Ecological contexts associated with late-stage fermented food consumption by wild primates 4.3 Potential evolutionary benefits of late-stage fermented food consumption 5 CONCLUSION ACKNOWLEDGMENTS AUTHOR CONTRIBUTIONS CONFLICT OF INTEREST OPEN RESEARCH BAGES DATA AVAILABILITY STATEMENT REFERENCES