Feeding strategies of primates in temperate and alpine forests: comparison of Asian macaques and colobines

Abstract

We analyzed regional variation in the diets of two primate clades, Asian macaques and colobines, whose distributions include temperate-alpine forests. We addressed feeding strategies that enabled them to adapt to harsh environments characterized by relatively low mean temperatures and strong seasonality in both temperature and food availability. Macaques in tropical-lowland forests feed mainly on fruit and animal matter whereas populations in temperate-alpine forests feed more on foliage and on such items as bark and fungi. In comparison, colobines in tropical-lowland forests feed more on fruit and foliage whereas populations in temperate-alpine forests feed less on flowers and more on lichens. Annual precipitation and mean temperature, both of which reflect primary production, had the most significant effects on the feeding behavior of the macaques, whereas only mean temperature had a significant effect on that of colobines. We found two behavioral strategies used by both clades to cope with severe environmental conditions in temperate-alpine forests--shifting to other food items and adjusting feeding plasticity for fruit and foliage. Macaques responded to latitudinal changes by use of both strategies whereas the colobines adapted by using the latter only. By contrast, changes in altitude resulted in the macaques' using the latter strategy and colobines' using both. The different current distributions of Asian macaques and colobines could be attributed to differences in their feeding strategies originating in their digestive systems.

A Short Cut to Mushrooms – Red Langur (Presbytis rubicunda) Consumption of Terrestrial Fungus

“…This could be explained by the distribution of the edible mushrooms, the fact that only adult females have been seen to consume mushrooms and/or the placement of the camera traps (which are placed to focus on clouded leopards (Neofelis diardi) [Cheyne et al, 2013] Mushrooms provide little energy for most animals as they are difficult to digest [Claridge et al, 1999]. Yet foregut fermenters are able to extract more of the mushrooms' protein [Grueter et al, 2009;Tsuji et al, 2013], as is the case in marsupials [Claridge and Cork, 1994;McIlwee and Johnson, 1998] and it would be interesting to compare the diet of sympatric primates, e.g., orang-utans (Pongo pygmaeus), which are regularly seen to consume mushrooms in Sebangau and other sites [Galdikas, 1988;Harrison, 2009;Russon et al, 2009].…”

“…The subfamily Colobinae consists of predominantly leaf-eating primates [Chivers and Hladik, 1980;Oates et al, 1980;Kool, 1986;Duc et al, 2009;Matsuda et al, 2009] and has evolved gastro-intestinal adaptations to exploit this abundant resource [Bauchop and Martucci, 1968;Chivers, 1994]. A multi-chambered stomach containing a microbe suspension in the foregut, plus a capacious stomach chamber and elongated caecum simultaneously neutralize toxins and effectively break down plant wall cellulose, facilitating digestion of the high quantities of fibre, protein and vitamins generally contained within leaves and other less digestible foods [Bauchop and Martucci, 1968;Kay et al, 1976;Chivers, 1994;Kay and Davies, 1994;Tsuji et al, 2013].…”

“…Mushrooms have been observed to be part of the diet for Germain's langur (Trachypithecus germaini [de Groot and Nekaris, 2016]), and Tsuji et al [2013] have compared the diets of Asian colobines where fungi are included as a food item, though the authors group fungi with bark, stem, sap, soil, seaweed and unidentified materials, and do not highlight fungus consumption specifically. These authors indicate the fungi could be consumed by 20 Asian species: Rhinopithecus bieti (black snub-nosed monkey), R. roxellana (golden snub-nosed monkey), R. brelichi (grey snub-nosed monkey), R. avunculus (Tonkin snub-nosed monkey), Semnopithecus entellus (Northern Plains gray langur), Trachypithecus vetulus (purple-faced langur), T. johnii (Nilgiri langur), T. obscurus (spectacled leaf monkey), T. pileatus (capped langur), T. geei (Gee's golden langur), T. francoisi (François's langur), T. leucocephalus (whiteheaded langur), Presbytis rubicunda (red langur), P. thomasi (Thomas's langur), P. comata (Javan surili), Pygathrix nigripes (black-shanked douc langur), Pygathrix nemaeus (red-shanked douc langur), P. cinerea (grey-shanked douc langur), Nasalis larvatus (proboscis monkey) and Simias concolor (pig-tailed snub-nosed monkey), though terrestrial consumption of mushrooms is only discussed for Rhinopithecus bieti [Grueter et al, 2009].…”

Group Composition and Monandry in Grizzled Langurs, Presbytis comata, on Java

“…For 3 decades after Ruhiyat [1983] had published the results of his fieldwork, his findings were often the only ones used for P. comata in comparative studies [e.g., van Schaik and Hörstermann, 1994;Bennett and Davies, 1994;Wright and Willis, 2012;Tsuji et al, 2013]. Other studies that were published on P. comata in mainstream scientific journals over this period that contained primary data dealt with distribution, conservation, or taxonomy [Weitzel and Groves, 1985;Melish and Dirgayusa, 1996;Nijman, 1997a, b;Nijman and van Balen, 1998;Meyer et al, 2011;Supartono et al, 2016]; the few ecological studies that were conducted either appeared in Indonesian journals, internal reports or remained hidden in unpublished theses [Sujatnika, 1992;Wedana, 1993;Nurdiana, 1997;Sugarjito et al, 1997;Nurjaman et al, 2002;Heriyanto and Iskandar, 2004;Suryana, 2010;Sawitri et al, 2010;Syarifah, 2013;Hidayat, 2016].…”

Effect of habitat quality on diet flexibility in Barbary macaques

“…Studies on non-human primates have shown that they may respond to a reduction in food availability by incorporating scarce but high-return foods or by optimizing their food intake on abundant but low-quality food [Hill et al, 2003;Sayers & Norconk, 2008;Tsuji et al, 2013;van Doorn et al, 2010;Wrangham et al, 1998]. The strategy they adopt may lead them to a diet including low profitability (e.g., energy/handling time) items (like Himalayan gray langurs, Semnopithecus entellus, in winter [Sayers et al, 2010] Most species of primates exhibit some degree of diet flexibility that allows them to cope with seasonality of resource availability or with intersite differences of habitat quality due to altitude, latitude, habitat fragmentation/loss, or habitat degradation [Campbell-Smith et al, 2011;Chaves & Bicca-Marques, 2013;Chaves et al, 2012;NaughtonTreves et al, 1998;Quéméré et al, 2013;Riley, 2007;Singh et al, 2001;Tsuji et al, 2013;Xiang et al, 2007]. Even species broadly and stereotypically described as dietary specialists are able to modify their dietary composition in response to habitat change (folivores such as colobines, [Grueter et al, 2009b;Koenig & Borries, 2001;Sayers & Norconk, 2008;Sayers et al, 2010;Xiang et al, 2007], or frugivores [Russo et al, 2005;Wieczkowski & Kinnaird, 2008]).…”