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Feeding Asian Pangolins: an Assessment of Current Diets Fed in Institutions Worldwide

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Feeding Asian Pangolins: an Assessment of Current Diets Fed in Institutions Worldwide Received: 20 July 2016 | Revised: 24 December 2016 | Accepted: 3 January 2017 DOI 10.1002/zoo.21349 RESEARCH ARTICLE Feeding Asian pangolins: An assessment of current diets fed in institutions worldwide Francis Cabana1 | Amy Plowman2 | Thai Van Nguyen3 | Shih-Chien Chin4 | Sung-Lin Wu4 | Hsuan-Yi Lo4 | Hirofumi Watabe5 | Fujio Yamamoto5 1 Wildlife Nutrition Centre, Wildlife Reserves Singapore, Singapore, Singapore Pangolins are ant specialists which are under intense threat from the illegal wildlife trade. 2 Paignton Zoo Environmental Park, Nutrition has notoriously been their downfall in captivity and is still an issue in regards to rescue Paignton, UK and rehabilitation. We analyzed the nutrient content of diets used by institutions that are 3 Save Vietnam's Wildlife, Cuc Phuong National successfully keeping Asian pangolins and to assess the variety of the ingredients and nutrients, Park, Ha Noi, Vietnam compared these with the nutritional requirements of potential nutritional model species. We 4 Taipei Zoo, Taipei City, Taiwan performed intake studies at five institutions and also had data from three other institutions. We 5 Ueno Zoological Gardens, Tokyo, Japan also analyzed five different wild food items to use as a proxy of wild diet. We observed two Correspondence categories of captive diets: those mostly or completely composed of insects and those high in Francis Cabana, Wildlife Nutrition Centre, Wildlife Reserves Singapore, 80 Mandai Lake commercial feeds or animal meat. Nutrient values were broad and there was no clear rule. The Road, Singapore 729826. non-protein energy to protein energy ratio of the diets were much higher than the wild food Email: [email protected] items, more so for those which receive less insects. The average contribution of carbohydrate, Funding information fat, and protein energy were also further away from the wild samples the less insects they Longleat Safari and Adventure Park contained. The previously suggested nutritional model for pangolins is the domestic dog which is supported by our relatively large nutrient ranges of apparently successful diets, however, due to their highly carnivorous nature; the upper most nutrient intake data are not consistent with this and favor the feline nutrient recommendations. We are unable to render a conclusion of what model is more appropriate based on our data collected. KEYWORDS ants, chitin, insectivore, myrmecophagy, nutritional geometry 1 | INTRODUCTION particularly at risk and ways to protect them in situ are thus far feeble (Challender et al., 2014a, 2014b). Pangolins are myrmecophagous mammals of the order Pholidota, Wild population figures for Asian pangolins are rough estimates at divided into two groups: Asian and African. There are eight species best, although they range over much of Southeast Asia (IUCN, 2008). It of pangolin, four of which are found in Africa (all listed as Vulnerable is believed that high levels of hunting have resulted in a decrease of 80% by the IUCN) and four in Asia: Sunda (M. javanica) and Chinese in the wild over the last 15 years for Asian species and that this decline (M. pentadactyla), both listed as Critically Endangered, and Philippine will continue as hunting spreads throughout the species range (M. culionensis) and Indian (M. craussicaudata), both endangered (Challender et al., 2014a). At present, pangolins are believed to be (Batin & Widmann, 2008; Hoffmann, 2008a, 2008b, 2008c, 2008d; the most heavily trafficked wild mammal globally. When confiscations Molur, 2008). Numbers of all pangolin species have been reduced do occur, the pangolins are in a negative health and welfare state significantly due to extensive hunting for their scales, which are used (Pattnaik, 2008). They are living through psychological stress and suffer in Asian traditional medicine even though there is a lack of evidence many different types of physical wounds, including damage to the on its efficacy, and their meat which is considered a delicacy in digestive tracts which originate either from traders pumping silt and countries such as China and Vietnam (Mahmood, Hussain, Irshad, cement into pangolins to make them heavier and, therefore, fetch a Akrim, & Nadeem, 2012). The Sunda and Chinese pangolins are higher price or from gastric ulcers from not having eaten for an extended Zoo Biology 2017; 9999: 1–7 wileyonlinelibrary.com/journal/zoo © 2017 Wiley Periodicals, Inc. | 1 2 | CABANA ET AL. period of time (Nguyen, pers. comm.). On rare occasions when live TABLE 1 The study population for each institution confiscated animals are received at rescue centers, common practice is Study to release them as quickly as possible because 67% of all captive population Location Common name Scientific name (n = m.f.u) pangolins are reported to die within the period of 10 days after arrival, with more succumbing to malnutrition thereafter (Mohapatra & Panda, WRS Sunda Pangolin M. javanicus 2.2.0 2014). The major causes of death are physical injuries and stress but if SVW Sunda Pangolin M. javanicus 4.7.0 they can be kept alive initially, nutrition is reported to be a major issue Ragunan Sunda Pangolin M. javanicus – (Yang et al., 2007). Their diet is thought of as very specific, termites and Chongqing Sunda Pangolin M. javanicus – ants, yet very little information exists on the species ingested and their Taipei Chinese Pangolin M. pentadactyla 3.7.0 nutrient intake (Lim & Ng, 2008). Ants are difficult to source for Asian Ueno Chinese Pangolin M. pentadactyla 1.1.0 rescue centers and zoos, especially in quantities large enough to feed a Leipzig Chinese Pangolin M. pentadactyla 1.1.0 group of confiscated pangolins arriving at short notice, which also Nandankanan Indian Pangolin M. crassicaudata – explains why so few zoos worldwide exhibit pangolins (Challender, Thai, WRS, Wildlife Reserves Singapore; SVW, Save Vietnam's Wildlife. Jones, & May, 2012). The difficult transition from a wild ant diet to a captive “gruel” type diet and little knowledge to their nutritional requirements is also why providing adequate nutrition is the biggest Leipzig, however, limited data were available from Ragunan and the data hurdle in their captive husbandry (Lissa, 1988; Yang et al., 2007). from Nandankanan zoo and Chongqing were obtained from Mohapatra Investigating an easily accepted, nutritionally appropriate diet for et al. (2013) and Yu, Jiang, Peng, Yin, & Ma (2015), respectively. We pangolins has wide reaching effects: engaging the education capabilities defined the diets used at these institutions as “successful” due to their of zoos by holding pangolins in their collection, improving rescue and diets supporting longevity (institutions keeping pangolins alive for more rehabilitation success rates and furthering our understanding on the use than 5 years) and health (no deaths within the last 5 years). of model species for advising exotic animal nutrition. Nutrient requirements of wild animal species are largely unknown and how they are fed is based on a “model” species for which there is 2.2 | Intake analysis already an understanding of their nutritional needs. Often domestic We observed the diet preparation of each institution's long-term diets models such as dogs (Bellanger et al., 2015), cats (Vester et al., 2010), for 7 days with each ingredient being weighed individually before swine (Tajima & Aminov, 2015), poultry (Wilkinson, Bradbury, being mixed together into a gruel-type mix which made delivery and Thomson, Bedford, & Cowieson, 2014), rat (Robbins, 2012), horse intake easy to quantify. We weighed the total amount of food given to ’ (Hagen et al., 2015; Johnson, 2014), rhesus macaque (O Sullivan et al., each pangolin, as well as the amount of uneaten food. The amount of 2013), duck (Robbins, 2012), mink (Diez-Leon & Mason, 2016), goat uneaten food was adjusted for desiccation (as described in Das et al., (Weiss, Schook, & Wolfe, 2014), and sheep (Gattiker et al., 2014) are 2015) and subtracted from the amount offered to result in a food used. Choice of model species will depend on phylogenetic related- ingested value. If we were unable to weigh any animals during ness, similarity in feeding ecology and/or digestive morphology and the study period, we used their most recent weights provided by the physiology. When it comes to the Pangolin, the giant anteater institution. The pangolins at SVW were kept as wild as possible (Myrmecophaga tridactyla) would appear the valid choice due to pending release and not handled, therefore no weights were available. similarities in feeding ecology (Redford, 1985) and it is the most studied among the myrmecophagous mammals (McNab, 1984). The 2.3 | Nutrient analysis requirements for the giant anteater are generally based on the nutritional model of the domestic dog. For this reason, we aim to We sent every food item to a nutrition laboratory within each characterize the nutritional composition of successfully managed respective country for direct nutrient analysis using the methods pangolin diets across eight successful institutions and discuss the described in Norconk and Conklin-Brittain (2004) for proximate appropriateness of nutritional models. analysis. Acid detergent fiber (ADF) and neutral detergent fiber (NDF) were analyzed as per Van Soest (1994). Water soluble carbohydrates (WSC) and energy were calculated as estimates since laboratory 2 | MATERIALS AND METHODS analyses were not available in each country. WSC were calculated as in Johnson, Raubenheimer, Rothman, Clarke, & Swedell (2013) by subtracting ash, crude protein, crude fat, and NDF from total dry 2.1 | Diet analysis matter. Digestible energy was calculated using the standard values of We collected diet information from Wildlife Reserves Singapore (WRS- 4 kcal/g for crude protein and carbohydrates, and 9 kcal/g for crude Singapore), Ragunan Zoo (Indonesia), Save Vietnam's Wildlife (SVW- fat. We collected five nests of green weaver ants near SVW in Vietnam), Taipei Zoo (Taiwan), Ueno Zoo (Japan), Leipzig Zoo Vietnam, totaling 1,536 g of ant matter. We analyzed a whole nest with (Germany), Nandankanan Zoo (India), and Chongqing Normal University its proportions of adults, eggs and larvae; and the following two (China).
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