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Tooth Wear and Feeding Ecology in Mountain Gorillas from Volcanoes National Park, Rwanda

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Tooth Wear and Feeding Ecology in Mountain Gorillas from Volcanoes National Park, Rwanda AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 00:00–00 (2015) Tooth Wear and Feeding Ecology in Mountain Gorillas From Volcanoes National Park, Rwanda Jordi Galbany,1* Olive Imanizabayo,2 Alejandro Romero,3 Veronica Vecellio,2 Halszka Glowacka,4 Michael R. Cranfield,5 Timothy G. Bromage,6 Antoine Mudakikwa,7 Tara S. Stoinski,2 and Shannon C. McFarlin1,8 1Center for the Advanced Study of Human Paleobiology, Department of Anthropology, The George Washington University, DC 2Dian Fossey Gorilla Fund International, Atlanta, GA 3Departamento de Biotecnologıa, Universidad de Alicante, Alicante, Spain 4Institute of Human Origins, Arizona State University, Tempe, AZ 5Mountain Gorilla Veterinary Project, University of California at Davis, CA 6Hard Tissue Research Unit, New York University College of Dentistry, NY 7Rwanda Development Board, Department of Tourism and Conservation, Kigali, Rwanda 8Division of Mammals, National Museum of Natural History, Smithsonian Institution, DC KEY WORDS dentine exposure; aging; diet; Gorilla beringei beringei ABSTRACT Objectives: Ecological factors have a dramatic effect on tooth wear in primates, although it remains unclear how individual age contributes to functional crown morphology. The aim of this study is to determine how age and indi- vidual diet are related to tooth wear in wild mountain gorillas (Gorilla beringei beringei) from Volcanoes National Park, Rwanda. Material and Methods: We calculated the percent of dentine exposure (PDE) for all permanent molars (M1–M3) of known-age mountain gorillas (N 5 23), to test whether PDE varied with age using regression analysis. For each molar position, we also performed stepwise multiple linear regression to test the effects of age and percentage of time spent feeding on different food categories on PDE, for individuals subject to long-term observational studies by the Dian Fossey Gorilla Fund International’s Karisoke Research Center. Results: PDE increased significantly with age for both sexes in all molars. Moreover, a significant effect of gritty plant root consumption on PDE was found among individuals. Our results support prior reports indicating reduced tooth wear in mountain gorillas compared to western gorillas, and compared to other known-aged samples of pri- mate taxa from forest and savanna habitats. Discussion: Our findings corroborate that mountain gorillas present very low molar wear, and support the hypothe- sis that age and the consumption of particular food types, namely roots, are significant determinants of tooth wear vari- ation in mountain gorillas. Future research should characterize the mineral composition of the soil in the Virunga habitat, to test the hypothesis that the physical and abrasive properties of gritty foods such as roots influence intra- and interspecific patterns of tooth wear. Am J Phys Anthropol 000:000–000, 2015. VC 2015 Wiley Periodicals, Inc. Primate dental morphology provides evidence of die- tary adaptations, as tooth morphology is designed to Additional Supporting Information may be found in the online accommodate the mechanical properties of foods that are version of this article. processed during mastication and ingestion (Lucas, 2004; Bunn and Ungar, 2009; Guy et al., 2013). The Grant sponsor: National Science Foundation; Grant numbers: functional life of a tooth may be altered mechanically by BCS 0852866, 0964944; Grant sponsors: The Leakey Foundation; National Geographic Society’s Committee for Exploration and wear produced by attrition, or the cumulative loss of Research; the Center and Institute Facilitating Fund of The George enamel and dentine tissues resulting from contact Washington University; the 2010 Max Planck Research Award between opposing teeth, and abrasion, which results endowed by the German Federal Ministry of Education and Research from contact with hard food objects and other particles to the Max Planck Society; Alexander von Humboldt Foundation. ingested during foraging (Lucas, 2004; Guy et al., 2013; Lucas et al., 2013; Romero et al., 2012, 2013). Thus, *Correspondence to: Dr. Jordi Galbany, Center for the Advanced physical properties of food items are critical determi- Study of Human Paleobiology, Department of Anthropology, The nants of macro- and microscale enamel loss associated George Washington University, 800 22nd Street NW, Ste 6000 Washington DC 20052, USA. E-mail: [email protected] with certain dietary behaviors and ecological constraints (Galbany et al., 2011, 2014; Romero et al., 2012; Morse Received 6 May 2015; revised 2 November 2015; accepted 3 et al., 2013; Cuozzo et al., 2014). Because foraging is the November 2015 most important life requirement for primates, tooth wear can have dramatic implications for life history, as DOI: 10.1002/ajpa.22897 the effects on occlusal surface morphology associated Published online 00 Month 2015 in Wiley Online Library with wear may have consequences for individual sur- (wileyonlinelibrary.com). Ó 2015 WILEY PERIODICALS, INC. 2 J. GALBANY ET AL. vival and reproduction (Logan and Sanson, 2002; King reported among great ape taxa, and inform future stud- et al., 2005). ies testing its potential later-life consequences. Numerous studies of dental ecology in the field have Today, gorillas are found in ten central African coun- demonstrated how tooth wear varies as a function of age tries, in a broad diversity of habitats ranging from [e.g., Lemur catta (Cuozzo and Sauther, 2006), Propithe- coastal lowland forests to high altitude afromontain rain cus edwardsi (King et al., 2005), Alouatta palliata (Den- forests, in which they also show significant variation in nis et al., 2004), Papio sp. (Phillips-Conroy et al., 2000; behavior and demography (Doran and McNeilage, 1998). Galbany et al., 2011), Mandrillus sphinx (Galbany et al., Although gorillas are usually classified as folivorous and 2014)]. In addition, wear-related changes in dental func- may consume tough and fibrous fallback foods, signifi- tion can significantly impact the outcome of reproductive cant differences in dietary behavior exist among popula- effort. King et al. (2005) demonstrated that sifaka tions (Doran et al., 2002; Elgart-Berry, 2004). females older than 18 years of age were characterized by Mountain gorillas are only found in two small popula- a significant loss of shearing blade length, suggesting tions at the south sector of the Virunga Volcanoes in loss of dental function. Further, advanced tooth wear in Rwanda, Uganda and Democratic Republic of Congo these older females was associated with a significant (DRC), and the Bwindi Impenetrable National Park in decline in infant survivorship, suggesting that advanced Uganda, located in the Albertine Rift. Whereas western dental wear may have consequences for a female’s abil- gorillas feed on a substantial amount of fruit, mountain ity to provision offspring in long-lived mammals such as gorillas from the Virunga Volcanoes feed mostly on non primates. These findings highlight the potential conse- reproductive plant parts, such as leaves, stems, pith, quences of dental senescence for life history. bark, roots, but very few fruits (Watts, 1998; Grueter In addition to age, tooth wear also reflects the interac- et al., 2013). The Virunga volcanoes region is character- tion between dental tissues and ecological factors, such ized by high-altitude montane forests with a dense herb as feeding behavior and habitat characteristics (Cuozzo layer and low abundance of fruit (Doran and McNeilage, et al., 2014). For example, in Amboseli baboons (Papio 2001). cynocephalus), the percent of dentine exposure on molars Moreover, mountain gorillas show wide dietary flexi- was positively correlated with the percent of time spent bility, which enables them to occupy a variety of habitats consuming gritty grass corms at the individual level within their range (Doran and McNeilage, 2001). In the (Galbany et al., 2011). Further, forest-dwelling mandrills Volcanoes National Park (VNP), the majority of their (Mandrillus sphinx) from Lek edi Park, Gabon, showed diet is composed of the leaves, stems, and pith (85.8%) of significantly higher wear rates for their age than Ambo- plant species, mainly Galium vines, thistles, celery and seli baboons, a finding that was attributed to differences nettles (Watts, 1998; Grueter et al., 2013). The Karisoke in mechanical food properties and soil composition (Gal- study area in particular is characterized by the highest bany et al., 2014). Though these species share similar- gorilla food biomass in the Virungas, and the diet of the ities in molar occlusal morphology and enamel gorillas in this area is composed of at least 54 plant spe- thickness, a high percentage of the mandrill diet year- cies (Watts, 1984; Grueter et al., 2013), with six species round is comprised of hard fruits and seeds, and the soil accounting for the 87% of the diet: vines (Galium spp.), from their habitat is comparatively rich in quartz, which thistles (Carduus nyassanus), wild celery (Peucedanum may contribute to the abrasiveness of their diet (Gal- linderi), bamboo (Yushania alpina), blackberries (Rubus bany et al., 2014). Thus, when abrasive particles in the spp.), and nettles (Laportea alatipes). Food availability diet are considered, they show a significant effect on and growth rate of vegetation does not vary seasonally, enamel loss that is independent of age (Galbany et al., with the exception of bamboo shoots (Fossey and Har- 2011, 2014). court, 1977; Watts, 1984). Mountain gorillas usually Another example of the interaction between dental tis-
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