Obligate exudativory characterizes the diet of the pygmy slow loris Nycticebus pygmaeus

Abstract

Few primate species are known to excavate plant sources to procure exudates and other foods via active gouging. It is now apparent that slow lorises belong to this rare guild of obligate exudativorous primates. We investigate the diet of the pygmy loris (Nycticebus pygmaeus) in a mixed deciduous forest in the Seima Protection Forest, Eastern Cambodia, and attempted to determine the importance of this resource in their diet. Feeding behaviors of six females and seven males were observed using radio-tracking to facilitate follows, and nine fecal samples were collected in February-May and January-March in 2008 and 2009 respectively. We observed 168 feeding bouts, during which the animals ate exudates (76); fruits (33); arthropods (27); flower parts (21); fungi (3); parts of bamboo culms (7); and reptiles (1). We filmed 19 bouts of exudativory, and observed animals consuming exudates in an orthograde posture, or standing quadrupedally over the exudate source. Pygmy lorises also gouged bamboo to collect lichen and fungi, or broke open dead culms to access invertebrates. Feeding occurred on terminal tree branches (24), tree trunks (21), bamboo (13), the middle of branches (7), and the undergrowth (1). The fecal samples contained plant parts, small-sized arthropods (primarily Coleoptera and Lepidoptera), reptile scales, animal bones, and animal hairs. Pygmy slow lorises are morphologically specialized for processing and digesting exudates, displaying small body sizes, specialized dentitions, elongated, and narrow tongues, large caecums, short duodenums, expanded volar pads, and modified hindlimbs. These features, combined with the prevalence of exudates in their diet across seasons, and ill health when exudates are missing from their diet in captivity, points to this species being an obligate exudativore.

Medicinal plant exudativory by the Bengal slow loris Nycticebus bengalensis

“…Exudates are the main components of diet of the greater slow loris N. coucang (43%), pygmy slow loris N. pygmaeus (63%: reintroduced; 51%: wild) and Javan slow loris N. javanicus (54%) (Streicher 2004, Wiens et al 2006, Starr & Nekaris 2013 (2006) already suggested that the extremely low basal metabolism of slow lorises is an adaptation to digest toxic secondary compounds found in their exudate-based diet. Sequestration of chemicals from secondary metabolites provides an array of known benefits to many taxa, including primates (Huffman 2003).…”

“…Several morphological characters of these nocturnal strepsirrhines suggest the presence of obligate exudativory, including a stout toothcomb, small body size, a large caecum, a long tongue, wide U-shaped legs and enlarged hand pads for gripping (Hladik 1978. Wiens et al (2006), Swapna et al (2009) and Starr & Nekaris (2013) all provided strong evidence that exudates are a preferred food for slow lorises (selected disproportionately often relative to their abundance within the habitat) rather than a fallback food (food used when preferred items are not available; Marshall & Wrangham 2007).…”

“…Exudates are a family of foods including gums and saps that offer a carbohydrate-rich energy source, yet one which at the same time may contain difficult-to-digest secondary metabolites (Heymann & Smith 1999). Only 6 primate genera (Calithrix, Mico, Ce buella, Phaner, Euoticus and Nycticebus) are known to access these foods through active excavation of plant surfaces (Starr & Nekaris 2013). These obligate exudativores include exudates in ≥40% of their feeding time (hereafter referred to as diet; Nash & Burrows 2010).…”

“…Several morphological characters of these nocturnal strepsirrhines suggest the presence of obligate exudativory, including a stout toothcomb, small body size, a large caecum, a long tongue, wide U-shaped legs and enlarged hand pads for gripping (Hladik 1978. Wiens et al (2006), Swapna et al (2009) and Starr & Nekaris (2013) all provided strong evidence that exudates are a preferred food for slow lorises (selected disproportionately often relative to their abundance within the habitat) rather than a fallback food (food used when preferred items are not available; Marshall & Wrangham 2007).The Vulnerable Bengal slow loris Nycticebus bengalensis is the largest (1100 to 2100 g) of the 8 slow loris species and is distributed across Southeast Asia (northeastern India, Myanmar, Bhutan, Bangladesh, Laos, Cambodia, Vietnam, Thailand and China). Three short-term wild studies have provided evidence for exudativory within this widely dispersed species in different habitat types (dry acacia scrub forest, Swapna et al 2010; lowland rainforest mixed with plantations, Pliosungnoen et al 2010; and montane rainforest mixed with grassland, Rogers & Nekaris 2011).…”

A retrospective review of mortality in lorises and pottos in North American zoos, 1980-2010

“…The Mysore slender loris Loris lydekkerianus lydekkerianus feeds almost exclusively on animal prey, many of which are toxic species (Nekaris & Rasmussen 2003). New data from the field has highlighted the importance of nectars and exudates in the slow loris diet (Tan & Drake 2001, Starr & Nekaris 2013; at one study site in India, N. bengalensis fed almost exclusively on exudates during the winter season (Swapna et al 2010). Lorises often obtain gums by gouging at trees, and the lack of opportunities to perform this behavior in captivity may be associated with periodontal disease (Nekaris 2009).…”