Comparative Ecology of Exudate Feeding by Lorises (Nycticebus, Loris) and Pottos (Perodicticus, Arctocebus)

Abstract

Craniomandibular variation characterizes the five species of Asian slow loris (Nycticebus), but until now, few ecological studies have been available to understand the factors that underpin it. Here, we review feeding ecology of Asian lorises and African pottos, with emphasis on the importance of exudate feeding, including several new studies. We then present novel data on this behavior based on a 10-week study of N. coucang at Pusat Penyelamatan Satwa, Lampung, Sumatra, Indonesia. Lorises and pottos range in body size from 100 g (Loris tardigradus) to more than 2 kg (N. bengalensis). Three of the smallest species (Arctocebus calabarensis, A. aureus, L. tardigradus) rely mainly on insects and small invertebrates as dietary staples. Although Perodicticus is known to eat gum only from already open wounds, active gouging of bark to extract exudates or consumption of plant sap has now been observed in all other lorises. Five species (P. potto, N. coucang, N. bengalensis, N. javanicus, N. pygmaeus) rely on exudates as a key food source. Although at all field sites, exudates are eaten all year round, at some, they become a key resource in times of food scarcity. Exudates have been extracted from 14 different plant families; Fabaceae is possibly the most important, currently consumed by all exudativorous species. Despite the lack of keeled nails, gouging behavior of lorises closely resembles that of marmosets and fork-marked lemurs, and involves active breaking of the plant surface; the audible nature of this behavior, as well as the characteristic marks left behind, makes it useful for determining the presence of Nycticebus in a forest. The captive lorises in our study also gouged regularly, recorded 2.9 times per hour for both adults and juveniles. Urine and facial marking accompanied the majority of gouges, a behavior recorded before only for marmosets. The functions of this behavior as a resource sharing strategy are explored. The importance of providing opportunity for gouging for captive lorises is also discussed, as a way to mitigate the periodontal diseases, which plague Nycticebus in captivity. We conclude by discussing the importance of a better understanding of this relatively unique behavior to improve our knowledge of morphological correlates to loris taxonomy and ecology, and captive management via dietary changes and enrichment.

Pygmy slow loris Nycticebus pygmaeus—natural diet replication in captivity

“…Zoos feeding dead mice, dead 1 d old chickens, mealworms and fruits to N. pygmaeus became common practice. Recent studies by Wiens (2002), Nekaris et al (2010) and Streicher et al (2013) suggest that this lorisid species is actually an exudativore. Their wild diet has been reported to reflect the following proportions: gum (30%), other exudates such as sap and nectar (30%) and insects (40%) (Streicher 2009, Nekaris & Bearder 2011.…”

“…Unrefined gum from wild species of trees is said to contain an important amount of calcium, which may be important to balance out the high phosphorous concentration found within the invertebrates that they ingest (Charles-Dominique 1977, Power 2010. Lorises have been recorded feeding from a variety of tree species nightly, specifically Sapindaceae, Euphorbiaceae, Fabaceae, Anarcdiaceae and Burseraceae (Tan & Drake 2001, Nekaris et al 2010, Streicher et al 2013. Their lower canines and incisors (tooth comb) are specialized and used in conjunction with their tusks (specialized procumbent caniniform premolars), which are used to gouge holes in tree bark (Kubota & Iwamoto 1967, Nekaris et al 2010.…”

“…Lorises have been recorded feeding from a variety of tree species nightly, specifically Sapindaceae, Euphorbiaceae, Fabaceae, Anarcdiaceae and Burseraceae (Tan & Drake 2001, Nekaris et al 2010, Streicher et al 2013. Their lower canines and incisors (tooth comb) are specialized and used in conjunction with their tusks (specialized procumbent caniniform premolars), which are used to gouge holes in tree bark (Kubota & Iwamoto 1967, Nekaris et al 2010. The gum pools up within the tree's wound and eventually hardens; N. pygmaeus can then collect the exudate using their long narrow tongue or simply bite it off (Coimbra-Filho & Mittermeier 1978).…”

Do Common Marmosets (Callithrix jacchus) Use Scent to Communicate Information about Food Resources?

“…Interestingly, other exudativores such as the slow loris (Nycticebus coucang) also deposit scent marks during gouging [Nekaris et al, 2010]. These primates can directly manipulate food profitability through re-gouging holes to stimulate continued exudate production.…”

“…observation]. Chemical cues could also aid immatures in learning to select exudate resources [Nekaris et al, 2010]. As such, animals may be selected to scent mark profitable holes to ensure that foraging effort is primarily expended on the most advantageous exudate holes.…”