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Nutritional Composition of the Diet of the Western Gorilla (Gorilla Gorilla): Interspecific Variation in Diet Quality

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Nutritional Composition of the Diet of the Western Gorilla (Gorilla Gorilla): Interspecific Variation in Diet Quality Received: 4 January 2019 | Revised: 2 August 2019 | Accepted: 13 August 2019 DOI: 10.1002/ajp.23044 RESEARCH ARTICLE Nutritional composition of the diet of the western gorilla (Gorilla gorilla): Interspecific variation in diet quality Jessica L. Lodwick1,2 | Roberta Salmi1,3 1Interdepartmental Doctoral Program in Anthropological Sciences, Stony Brook Abstract University, Stony Brook, New York To meet nutritional needs, primates adjust their diets in response to local habitat 2Department of Ecology and Evolutionary differences, though whether these dietary modifications translate to changes in Biology, University of Connecticut, Storrs, Connecticut dietary nutrient intake is unknown. A previous study of two populations of the 3Department of Anthropology, University of mountain gorilla (MG: Gorilla beringei) found no evidence for intraspecific variation in Georgia, Athens, Georgia the nutrient composition of their diets, despite ecological and dietary differences Correspondence between sites. One potential explanation is that nutritional variability in primate diets Jessica L. Lodwick, Department of Ecology and Evolutionary Biology, University of requires greater ecological divergence than what was captured between MG sites, Connecticut, Storrs, Connecticut 06269. underpinning environmental differences in the nutrient quality of plant foods. To test Email: [email protected] whether Gorilla exhibits interspecific variation in dietary composition and nutrient Funding information intake, we studied the composition and macronutrients of the western gorilla (WG: National Science Foundation Directorate for Social, Behavioral and Economic Sciences; The Gorilla gorilla) staple diets and compared them with published data from the two MG Leakey Foundation, Grant/Award Numbers: populations. We recorded feeding time and food intake of four adult female WGs General Research Grant, Great Ape – Fellowship; Conservation International, Grant/ from one habituated group over a period of 11 months (December 2004 October Award Number: Margot Marsh Biodiversity 2005) at the Mondika Research Center, Republic of Congo, allowing for assessment Fund; U.S. Fish and Wildlife Service, Grant/ Award Number: Great Ape Conservation Fund of seasonal patterns of nutrient intake. Staple diets of WGs and MGs diverged in their dietary and macronutrient composition. Compared to MGs, the staple diet of WGs (by intake) contained higher proportions of fruit (43%) and leaf (12%) and a lower proportion of herb (39%), resulting in a higher intake of total nonstructural carbohydrate and fiber and a lower intake of crude protein. Staple gorilla fruits and herbs differed in nutrient quality between sites. Gorillas exhibit nutritional flexibility that reflects ecological variation in the nutrient quality of plant foods. Since dietary quality typically affects rates of growth and reproduction in primates, our results suggest that interspecific differences in nutrient intake and food quality may shape differences in gorilla nutrient balancing and female life history strategies. KEYWORDS ape, ecology, feeding, nutrition, primate 1 | INTRODUCTION Davies, Oates, & Dasilva, 1999; Potts, Watts, & Wrangham, 2011), socioecology (Boinski, 1999; Borries, 1993; Sterck, Watts, & van For primates with broad geographical distributions, habitats typically Schaik, 1997), and life history traits (Borries, Koenig, & Winkler, vary widely in their climates, plant communities, and resource 2001; Stoinski, Perdue, Breuer, & Hoff, 2013). To meet nutritional characteristics, leading to intraspecific and interspecific differences needs, primates may respond to environmental variability by in primate diets (Chapman & Chapman, 1999; Chapman et al., 2004; adjusting activity budgets, feeding behavior, and dietary composition Am J Primatol. 2019;e23044. wileyonlinelibrary.com/journal/ajp © 2019 Wiley Periodicals, Inc. | 1of16 https://doi.org/10.1002/ajp.23044 2of16 | LODWICK AND SALMI (Dasilva, 1992). For example, baboons (Papio spp.) display eclectic 1992). They have also been shown to drive socioecological variation and geographically variable diets (Hill & Dunbar, 2002) reflective of within and among closely related species, including differences in local habitat differences (Swedell, 2011), including variations in dispersal patterns (Barton et al., 1996; Boinski, 1999), feeding altitude, climate, vegetation, food quality, and predation risk and ranging behavior (Chapman et al., 2004; Harris & Chapman, (Altmann, 1998; Barton, Byrne, & Whiten, 1996; Byrne, Whiten, 2007), and female sociality (Barton et al., 1996; Borries, Sommer, & Henzi, & McCulloch, 1993). In some populations, fruit and seeds Srivastava, 1991; Koenig, Beise, Chalise, & Ganzhorn, 1998). Differences accounted for more than half of baboon feeding time (e.g., P. anubis in in food quality among sites may also drive variation in primate group Ghana and Ethiopia; P. cynocephalus in Tanzania), whereas in others size, as suggested in black‐and‐white colobus monkeys (Fimbel, Vedder, underground plant parts composed the bulk of feeding time (e.g., P. Dierenfeld, & Mulindahabi, 2001). To enhance our understanding of cynocephalus in Kenya; P. ursinus in South Africa: Altmann, 1998). how nutritional variation may underpin ecologically‐driven differences While variation in primate diets is well‐documented, the in primate life history and socioecology, we compare the dietary nutritional consequences of such variation may vary greatly, ranging composition and macronutrient intake between two closely related from minimal to pronounced, depending on differences in food species, the western gorilla (WG: G. gorilla) and the mountain gorilla quality. Although blue monkeys (Cercopithecus mitis stuhlmanni) and (MG: G. b. beringei). Gorillas present an ideal taxon for studying how golden monkeys (C. m. kandti) exhibited habitat and dietary ecological variability leads to variation in primate socioecology and life differences in Uganda, the macronutrient content of their 10 most history because they occupy a range of habitats at varying altitudes, commonly eaten foods was remarkably similar (Twinomugisha, resulting in striking environmental differences among sites (Doran & Chapman, Lawes, Worman, & Danish, 2006). Correspondingly, for McNeilage, 2001; Robbins, 2010; Robbins & Robbins, 2018; Rothman, two savannah baboon species in close geographic proximity to one Nkurunungi, Shannon, & Bryer, 2013; Rothman, Pell, Nkurunungi, & another (i.e., P. anubis at Laikipia; P. cynocephalus at Amboseli), as well Dierenfeld, 2006). as groups of black‐and‐white colobus monkeys (Colobus angolensis at The eastern gorilla (Gorilla beringei, incl. MGs) diverged recently Diani Forest) and red colobus monkeys (Procolobus rufomitratus at from the WG (Scally et al., 2012; Thalmann, Fischer, Lankester, Kibale) inhabiting areas with differing degrees of disturbance, dietary Pääbo, & Vigilant, 2006; Xue et al., 2015; Zinner, Groeneveld, Keller, flexibility did not translate to nutritional differences (Altmann, Post, & Roos, 2009). There are two populations of MG situated in close & Klein, 1987; Barton, Whiten, Byrne, & English, 1993; Dunham, proximity (25 km) to one another in the herbaceous highlands of East 2017; Ryan, Chapman, & Rothman, 2012). Nonetheless, when field Africa. The best known population, studied at Karisoke, resides in sites are separated by wide geographic distances and/or diverge in high altitude (2500–3700 m) montane forest of the Virunga their altitude, climate, plant composition, and resource character- Mountains (Harcourt & Stewart, 2007; Robbins, Sicotte, & Stewart, istics, then the macronutrient composition of primate diets may 2001; Watts, 1984). The second population of MGs occupies differ. For example, in a comparison of two Bornean orangutans intermediate‐to‐high altitude (2100–2500 m) areas of the Bwindi (Pongo pygmaeus) populations living in hydrologically distinct peat‐ Impenetrable Forest (Goldsmith, 2002; Robbins, 2003; Rothman, swamp forests (separated by only 63 km), the nutritional content of Plumptre, Dierenfeld, & Pell, 2007). WG, by contrast, inhabit the their diets differed markedly as a result of differences in food quality tropical rainforests of Western Central Africa (Doran & McNeilage, between sites (Vogel et al., 2015). Black‐and‐white colobus monkeys 1998), with populations distributed among the region’s lowland (Colobus angolensis) in a degraded forest also differed in their dietary (<800 m) forests (Goldsmith, 2002). composition and macronutrient intake from those in primary forest, a Compared with the highland habitats of MGs, the lowland finding attributed to differences in food quality and availability rainforests of Central Africa contain lower densities of herbs (Ganas, (Dunham & Rodriguez‐Saona, 2018). More broadly, habitat char- Ortmann, & Robbins, 2009; Goldsmith, 2002; Kuroda, Nishihara, acteristics related to climate and forest composition play an Suzuki, & Oko, 1996; Rogers et al., 2004), higher densities of fruiting important role in determining food quality. For example, the diet of trees, more seasonality in fruit availability (Goldsmith, 2002), and olive baboons (P. anubis) inhabiting a tropical forest site in Uganda greater plant diversity (Lieberman, Lieberman, Peralta, & Hartshorn, (Johnson, Swedell, & Rothman, 2012) contained more fibrous foods 1996; Richards, 1952). Furthermore, researchers have documented compared to that of chacma baboons (P. ursinus) at a temperate site interspecific variability in
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