Behavioural Processes 142 (2017) 131–137 Contents lists available at ScienceDirect Behavioural Processes journal homepage: www.elsevier.com/locate/behavproc How bonobo communities deal with tannin rich fruits: Re-ingestion and MARK other feeding processes ⁎ David Beaunea,b, , Gottfried Hohmanna, Adeline Serckxc,d,e, Tetsuya Sakamakif, Victor Naratg,h, Barbara Fruthi,j,k a Max Planck Institute for Evolutionary Anthropology, Department of Primatology, Deutscher Platz 6, Germany b Laboratoire Biogéosciences, UMR CNRS 6282, Université de Bourgogne, 6 bd Gabriel, 21000 Dijon, France c Primatology Research Group, Behavioural Biology Unit, University of Liege, Liege, Belgium d Conservation Biology Unit, Royal Belgian Institute of Natural Sciences, Brussels, Belgium e Ecole Régionale post-universitaire d’Aménagement et de gestion Intégrés des Forêts et Territoires tropicaux, Kinshasa, Democratic Republic of the Congo f Primate Research Institute, Kyoto University, Kanrin 41, Inuyama, Aichi 484-8506, Japan g Department of Infection and Epidemiology, Epidemiology of Emerging Diseases Unit, Pasteur Institute, Paris, France h Eco-Anthropology and Ethnobiology, National Museum of Natural History, Paris, France i Liverpool John Moores University, Faculty of Science/School of Natural Sciences and Psychology; Liverpool, UK j Centre for Research and Conservation, Royal Zoological Society of Antwerp, Antwerp, Belgium k Department of Developmental and Comparative Psychology, Max-Planck Institute for Evolutionary Anthropology, Leipzig, Germany ARTICLE INFO ABSTRACT Keywords: This report describes bonobo (Pan paniscus, Hominidae) behavioral flexibility and inter-community differences Coprophagy with high tannin level fruit processing. In fruiting plants, tannin should discourage certain seed dispersers (direct Canarium schweinfurthii deterrence hypothesis) such as primates. Based on data deriving from five study sites; LuiKotale, Lomako, Culture Wamba, Malebo and Manzano, we compare consumption and dispersal of fruit species rich in tannins: Parinari Feeding behavior and Musanga pulp was chewed across all communities probably for saliva tannin neutralisation. However, Seed dispersal consumption of the fruits of Canarium schweinfurthii was observed in few communities only with differences in Pan paniscus Zoochory the food process: While bonobos of Wamba, Lomako and Manzano crunched and swallowed the pulp, bonobos of LuiKotale ingested entire fruits, extracted intact fruits from feces, and re-ingested their pulp, spitting the seed after a retention time of 24 h in the digestive tract (i.e. endozoochory). We discuss potential functions of this peculiar feeding technique, likely to be a cultural behavior. 1. Introduction (Johns, 1999), as well as substances such as lectins that inhibit enzy- matic activity. Tannins are both toxics and digestive inhibitors. The One common form of the multiple and sometimes complex inter- major effects of most of them are dilution of nutritional content, re- actions between plants and animals is the consumption of seeds. In the duced digestibility, and limitation of food intake (Cooper and Owen- seed dispersal effectiveness framework, a plant can have several con- Smith, 1985; Robbins et al., 1991). The effect of tannins has been ex- sumers that differ in terms of their impact on dispersal distance and plored in insects, fish, birds and mammalian species (Clauss, 2003; germination (Schupp et al., 2010). Plants might be able to ‘choose’ Barboza et al., 2010; Omnes et al., 2017). One mammalian taxon that is higher-quality seed dispersal vectors and avoid those of lower quality. particularly interesting in this context is primates. The majority of The directed deterrence hypothesis (Cipollini and Levey, 1997; Levey contemporary primate species is frugivorous or consumes at least et al., 2006) proposes that fruits’ secondary compounds or chemical temporarily large amounts of fruit (Hohmann et al., 2010; Hawe and defense mediated by plant secondary metabolites (PSMs) have evolved Peres, 2014 Hawe and Peres, 2014). Not surprisingly, primates have to escape the action of damaging consumers such as seed predators evolved specific adaptation to frugivory such as color vision (Osorio while not inhibiting those that dispersers intact seeds. The secondary and Vorobyev, 1996), dentition (Scott, 2011), and digestive mor- compounds protecting from seed consumption include alkaloids, var- phology (Milton, 2003). Accordingly, it is reasonable to ask if primates ious glycosides, and saponins, that are potentially toxic to consumers have evolved mechanisms to cope with high tannin concentrations in ⁎ Corresponding author at: Ornithological Society of Polynesia SOP - Manu BP 7023 - 98719 Taravao - Tahiti - French Polynesia. E-mail address: [email protected] (D. Beaune). http://dx.doi.org/10.1016/j.beproc.2017.06.007 Received 25 January 2017; Received in revised form 26 June 2017; Accepted 26 June 2017 Available online 27 June 2017 0376-6357/ © 2017 Elsevier B.V. All rights reserved. D. Beaune et al. Behavioural Processes 142 (2017) 131–137 Fig. 1. Map of the field sites with five bonobo communities: LuiKotale (S2°47′- E20°21′), Lomako (N0°51′, E21°5′), Wamba (N0°11′, E22°37′), Malebo (S2°33′, E16°29′) and Manzano (S2°38, E16°23′), Democratic Republic of the Congo. their diet. There is some evidence that wild primates are sensitive to the et al., 2006). From this, one would assume that bonobos ingest low astringency caused by tannins (Dominy et al., 2001). In a recent ex- levels of tannin when compared with other species and that fruit with perimental study with three hominoid species, species-differences were high concentrations of tannin are avoided. Yet, evidence from the same found in terms of facial expression of subjects consuming a cereal with and other sites indicate that bonobos do consume tannin rich fruit, relatively high concentrations of tannin. Other studies reported that suggesting that they are able to cope with the deleterious effects of consumers avoid food with polyphenolic compounds, in both con- dietary tannins. This raises the following questions: (a) how are bo- densed and hydrolysable forms (Wrangham and Waterman, 1981; nobos adapted to process fruit with high concentrations of tannin, and Oates et al., 1977; Glander, 1982; McKey et al., 1981). While this in- (b) is there geographic variation in the way bonobos process fruit with formation makes evident that primates are sensitive to tannins and their high tannin concentrations? The latter question is particularly relevant deleterious effects, major components such as ecological variation of as other studies on African and Asian apes have shown considerable tannin distribution and specific adaptability to cope with fruit that variation in dietary patterns, social behavior, and material culture. provide important food but contain high concentrations of tannin are virtually lacking. This study explores patterns of consumption of tannin 1.1. Possible counter strategies to high tannin values rich fruit by bonobos (Pan paniscus) across different sites and popula- tions differing in terms of forest composition, habitat heterogeneity, Salivary proline-rich proteins (PRPs) have the capacity to bind and seasonal changes in food availability. Moreover, having observa- tannins forming stable complexes that prevent dilution of dietary pro- tional data from multiple sites, we ask to what extent bonobos differ in tein and facilitate excretion of detrimental tannins. To facilitate this the techniques of food processing to cope with high tannin concentra- technique, food matter has to be exposed to saliva prior to ingestion. In tions. Finally, we explore if bonobos disperse seeds of tannin rich fruit fact, bonobos and other hominid primates sometimes chew on fruits as predicted by the directed deterrence hypothesis (Levey et al., 2006), without swallowing food pulp and by doing so plant material is ex- by describing the fruit handling and its effect on the dispersal of intact tensively exposed to saliva. Yet, the technique of wadging could also be seeds. used to separate those parts of the fruit containing high concentrations Bonobos are restricted to the tropical lowland forests south of the of tannin from those that are easily digested. Another form of oral food Congo River. The species has an omnivorous diet and, besides forest processing that may serve a similar purpose is separating seeds from elephants, is one of the largest seed dispersers in this habitat providing mesocarp and discarding the former while ingesting the latter (Lambert, critical seed dispersal service to the majority of the tree species (Idani, 1998). As tannins tend to occur in higher concentrations in seeds rather 1986; Tsuji et al., 2010; Beaune et al., 2013a; Beaune et al., 2013b; than mesocarp, a simple way to reduce tannin intake is removal of Beaune et al., 2015; Beaune, 2015). Previous studies at one site re- seeds. If all consumers share the capacity of secreting salivary proline to vealed concentrations of tannins being relatively low, and that varia- an extent that even high concentrations of tannin are neutralized one tion of macronutrients was independent of tannin content (Hohmann would expect them to do so because the two other techniques, wadging 132 D. Beaune et al. Behavioural Processes 142 (2017) 131–137 and seed removal increase handling time and slow down food intake. antifeedants. Phenols and tannins were measured in the lab of the On the other hand, foraging techniques may be acquired by social