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Dietary Flexibility and Feeding Strategies of Eulemur Western University Scholarship@Western Anthropology Publications Anthropology Department 12-10-2015 Dietary Flexibility and Feeding Strategies of Eulemur: A Comparison with Propithecus Hiroki Sato Primate Research Institute, Kyoto University, Japan, [email protected] Luca Santini Department of Biology and Biotechnologies, Sapienza Università di Roma Erik R. Patel Duke Lemur Center, Duke University, Durham, NC, USA Marco Campara Nocturnal Primate Research Group, Dept. of Social Sciences, Oxford Brookes University, Oxford, UK Nayuta Yamashita Institute for Population Genetics, University of Veterinary Medicine, Vienna, Austria See next page for additional authors Follow this and additional works at: https://ir.lib.uwo.ca/anthropub Part of the Anthropology Commons, Behavior and Ethology Commons, Biodiversity Commons, Other Animal Sciences Commons, and the Zoology Commons Citation of this paper: Sato, Hiroki; Santini, Luca; Patel, Erik R.; Campara, Marco; Yamashita, Nayuta; Colquhoun, Ian C.; and Donati, Giuseppe, "Dietary Flexibility and Feeding Strategies of Eulemur: A Comparison with Propithecus" (2015). Anthropology Publications. 60. https://ir.lib.uwo.ca/anthropub/60 Authors Hiroki Sato, Luca Santini, Erik R. Patel, Marco Campara, Nayuta Yamashita, Ian C. Colquhoun, and Giuseppe Donati This article is available at Scholarship@Western: https://ir.lib.uwo.ca/anthropub/60 Int J Primatol (2016) 37:109–129 DOI 10.1007/s10764-015-9877-6 Dietary Flexibility and Feeding Strategies of Eulemur: A Comparison with Propithecus Hiroki Sato1 & Luca Santini2 & Erik R. Patel3 & Marco Campera4 & Nayuta Yamashita5,6 & Ian C. Colquhoun7 & Giuseppe Donati4 Received: 20 May 2015 /Accepted: 7 September 2015 /Published online: 10 December 2015 # Springer Science+Business Media New York 2015 Abstract Despite the great variety of habitats in Madagascar, Eulemur has success- fully populated most forested habitats on the island. Although the high dietary flexi- bility of Eulemur is often credited as one of the drivers of its evolutionary success, other behavioral evidence suggests a limited capacity for dietary switching. To shed light on the feeding strategies of Eulemur, we compared the dietary flexibility between popu- lations of this genus with that of another widespread lemur taxon, Propithecus.We hypothesized that Eulemur would show greater dietary flexibility than Propithecus, which has a digestive system specialized for folivory, and that Eulemur living in dry forests would switch its diet from fruit to other food seasonally. To examine these hypotheses, we performed a phylogenetic least-squares analysis on 10 populations of Eulemur and 7 of Propithecus to assess the contribution of environmental variables and body mass on their dietary flexibility while controlling for phylogenetic relatedness. Eulemur relied heavily on fruit and did not show large variations in primary food over the year. Propithecus consumed leaves and fruits equally and exhibited considerable * Hiroki Sato [email protected] 1 Primate Research Institute, Kyoto University, 41-2 Kanrin, Inuyama, Aichi 484-8506, Japan 2 Department of Biology and Biotechnologies, Sapienza Università di Roma, Viale dell’Università 32, 00185 Rome, Italy 3 Duke Lemur Center, 3705 Erwin Road, Durham, NC 27705, USA 4 Nocturnal Primate Research Group, Department of Social Sciences, Oxford Brookes University, Oxford OX3 0BP, UK 5 Institute for Population Genetics, University of Veterinary Medicine, Vienna, Josef Baumann Gasse 1, 1210 Vienna, Austria 6 Austrian Academy of Sciences, Dr. Ignaz Seipel-Platz 2, 1010 Vienna, Austria 7 Department of Anthropology and The Centre for Environment & Sustainability, University of Western Ontario, London, Ontario N6A 5C2, Canada 110 H. Sato et al. flexibility across seasons. Therefore, in contrast to our predictions, the anatomical specialization for fiber digestion heightens dietary flexibility in Propithecus.Atthe intrageneric level, we found similar ecogeographic variation; populations of both genera with heavier body mass consumed more fruit. As we predicted, Eulemur in drier habitats switched the diet from fruit to alternative food more frequently. To compensate for low dietary flexibility, Eulemur mostly adopts a power-feeding strategy by which it increases energy expenditure to acquire patchily distributed fruit resources. Keywords Anatomical adaptation . Behavioral flexibility. Diet . Feeding strategies . Sifakas . True lemurs Introduction Dietary switching, i.e., feeding on alternative resources, is the most common primate response to spatial and temporal variations in food availability (Hemingway and Bynum 2005). Dietary flexibility has been defined B…as the capacity to adjust digestive strategy according to the chemical and structural quality of the foods available^ (Chapman et al. 2002, p. 344). Therefore, such flexibility is determined primarily by anatomical and physiological adaptations, e.g., mechanisms of mastication and digestion (Chivers 1994;Kinzey1992;Lambert1998; Rylands 1993). However, even when anatomical specializations are present, many species still show greater variability in diet than what would be expected by their gut adaptations (Chapman and Chapman 1990). Comparative analyses between different taxa with distinct ana- tomical adaptations have been performed to understand the degree of dietary flexibility of primates (Milton 1998; Simmen and Sabatier 1996; Tsuji et al. 2013; Yamagiwa and Basabose 2006). For example, cercopithecines with simple digestive tracts exhibit greater dietary diversity and more frequent dietary switching than do colobines, which have specialized stomachs for fiber digestion (Lambert 2002). In Madagascar, climatic seasonality and unpredictability caused by tropical mon- soons (Dewar and Richard 2007;Jury2003) strongly influence phenological patterns and, thus, the food available to lemurs (Bollen and Donati 2005; Ganzhorn et al. 1999; Wright 1999). Moreover, the climate varies dramatically across the island, particularly between the evergreen rain forests of the east and northeast coasts and the dry deciduous and xerophytic forest formations of the west and south (Jury 2003). One of the most successful primate radiations on the island is the true lemur group (Eulemur spp.), as shown by the presence of one or two species in all forested habitats (Tattersall 1982). Previous field studies focused on the temporal variations in feeding patterns of Eulemur spp. at single sites (Andrews and Birkinshaw 1998;Andriamaharoaet al. 2010; Birkinshaw 1995;Curtis2004; Donati et al. 2007a; Freed 1996;Overdorff1993; Rasmussen 1999;Satoet al. 2014; Tarnaud 2006; Vasey 2000), whereas only a few studies have explored regional variations among species or populations (Donati et al. 2009;Johnson2006; Ossi and Kamilar 2006; Tattersall and Sussman 1998). Based on these studies, the Eulemur complex is identified as semifrugivorous with relatively greater dietary flexibility than the mainly frugivorous Varecia spp., which are found only in the eastern humid forests (Balko and Underwood 2005;Britt2000; Vasey 2000). Generally, diets of Eulemur tend to be higher in fruit in the eastern region Dietary Flexibility and Feeding Strategies of Eulemur 111 (Donati et al. 2007a;Overdorff1993), whereas a higher degree of folivory has been recorded in some western populations (Colquhoun 1997; Curtis et al. 1999; Sussman 1977). Thus, overall this genus is considered very flexible, and its capacity for dietary switching is often mentioned as one of the main traits that contributed to the success of the Eulemur radiation (Ossi and Kamilar 2006). However, during periods of fruit scarcity, Eulemur adopts several behavioral strat- egies to pursue fruit, an approach that dietary shifters do not usually rely on (Colquhoun 1993;Donatiet al. 2007a; Overdorff 1993). Among the strategies ob- served have been prolonged feeding activities over a 24-h period without shifting food categories (Donati et al. 2007a, 2009); increased ranging efforts (Overdorff 1993;Sato 2013a; Volampeno et al. 2011); reduced cohesion, or fission, of large groups to mitigate scramble competition (Colquhoun 1993;Donatiet al. 2011; Freed 1996; Overdorff and Johnson 2003); and, in several Eulemur species, a seasonal shift to an Benergy- minimizing strategy^ in which animals modify behavioral patterns to minimize energy expenditure (sensu Albert et al. 2013;Camperaet al. 2014)byprolongingresting (E. macaco: Colquhoun 1993, 1997) or decreasing daily traveling (E. collaris: Campera et al. 2014). In primates, such flexible and dynamic behavioral strategies often compensate for limited dietary flexibility (limited physio-anatomical flexibility). Thus, there is an apparent inconsistency between traditional knowledge about the dietary flexibility of Eulemur and their observed behavioral flexibility in pursuing primary food resources. One way to clarify the dietary flexibility of Eulemur is to compare this group with another lemur group that successfully radiated in Madagascar, Propithecus,whichis traditionally considered more specialized in terms of its physio-anatomical adaptation for digestion (Campbell et al. 2000;Hill1953; Richard 1977). The genus Propithecus has extensive molar crests for fracturing leaf material and masticating seeds (Yamashita 1998) and a specialized gut with high fiber digestibility via microbial fermentation (Campbell et al. 2000, 2004b;Hill1953). Eulemur and Propithecus have been thought to fill similar dietary niches as those filled by cercopithecines and colobines
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