Short Communication Tropical Conservation Science Volume 10: 1–7 Insights Into the Chinese Pangolin’s ! The Author(s) 2017 Reprints and permissions: (Manis pentadactyla) Diet in a Peri-Urban sagepub.com/journalsPermissions.nav DOI: 10.1177/1940082917709648 Habitat: A Case Study From Hong Kong journals.sagepub.com/home/trc Roger Ho Lee1, Khan Cheung1, John R. Fellowes, and Benoit Gue´nard1 Abstract Gut content analysis of a juvenile Chinese pangolin revealed eight ant and one termite species being preyed on. The identification of > 26,000 prey items and a comparison with local ant communities suggest a selective foraging behavior and a tendency for direct predation on arboreal or epigaeic ant nests within secondary forest and shrubland habitats. Keywords arboreal ants, conservation, endangered species, gut content analysis, myrmecophagous, subtropical, urban landscape Introduction feeding behavior of Chinese pangolins on a subset of social insects (Wu, Liu, Li, & Sun, 2005), the identifica- The Chinese pangolin (Manis pentadactyla L. 1758) has tion of the specific ant and termite species consumed as experienced a dramatic population decline over the past prey could substantially assist conservation programs. 20 years, leading to its recent reclassification on the However, existing data on diet are scarce and based IUCN Red List from Lower Risk/Near Threatened to mostly on indirect methods, such as inspection of food Critically Endangered (Challender et al., 2014). Despite leftovers at foraging burrows (e.g., Li, Zhou, Guo, Guo, being listed under the second-class national protection & Chen, 2010; Wu et al., 2005). category in China and Appendix II of the Convention As a result of its extensive protected-areas system and on International Trade in Endangered Species of Wild its relatively effective implementation of legislation pro- Fauna and Flora (CITES) in 1988 and 1994 (Wu, Ma, tecting wild animal, Hong Kong Special Administrative Tang, Chen, & Liu, 2002), and upgraded to Appendix I Region is perceived as a relative stronghold for wild (CITES, 2017) respectively, intensive illegal poaching populations of Chinese pangolin (Challender et al., for putative medicinal use (Soewu & Ayodele, 2009; 2014; Figure 1). However, limited knowledge is available Yee, Chu, Xu, & Choo, 2005) and bushmeat consump- on the species’ ecology in this mosaic of peri-urban tion (Challender, Harrop, & MacMillan, 2015) represent and secondary forest habitats. Furthermore, disturbed the main reasons for its population decline through most environments may induce life history shifts in wildlife of its distribution range (Challender et al., 2014). Due to populations, including diet (Ditchkoff, Saalfeld, & their cryptic behavior and low population densities, eco- Gibson, 2006). Thus, gaining dietary information on logical information on the Chinese pangolins is still frag- Chinese pangolin populations in this mosaic is urgently mentary, limiting the prospects for both in situ and ex situ conservation programs. 1School of Biological Sciences, The University of Hong Kong, Hong Kong, Diet composition reflects food preferences and avail- China ability and can also give insights into behavior, foraging Received 21 February 2017; Revised 21 April 2017; Accepted 21 April 2017 ecology, and habitat use of a species (Challender, 2009). Furthermore, information on diet may also be relevant to Corresponding Author: Benoit Gue´nard, School of Biological Sciences, Kadoorie Biological Sciences the conservation of both wild (Yu, Peng, Zeng, Yin, & Building, The University of Hong Kong, Pok Fu Lam Road, Hong Kong SAR, Zhu, 2015) and captive populations of Chinese pangolins China. (Hua et al., 2015). Given indications of the selective Email: [email protected] Creative Commons Non Commercial CC BY-NC: This article is distributed under the terms of the Creative Commons Attribution-NonCommercial 4.0 License (http://www.creativecommons.org/licenses/by-nc/4.0/) which permits non-commercial use, reproduction and distribution of the work without further permission provided the original work is attributed as specified on the SAGE and Open Access pages (https://us.sagepub.com/en-us/nam/open-access-at-sage). 2 Tropical Conservation Science needed. Here, after presenting detailed gut content ana- mounted for identification to species level. The number lysis of a juvenile Chinese pangolin collected in Hong of individuals from each caste (i.e., alates, workers, and Kong and summarizing published diet information, we pupae) in each species was counted. To prevent errors use knowledge of the ecology of its prey species to infer arising from repeated counting of body fragments, only its foraging habits and habitat use. heads were used as counting units. In Formicidae and Isoptera, the head represents a heavily sclerotized body part which is usually preserved during the digestive pro- Methods cess. For each species, five intact individuals were imaged Chinese Pangolin Gut Content Analysis to allow standardized measurements (to the nearest 0.01 mm) of morphological traits including Weber’s A wild juvenile Chinese pangolin, weighing 546 g, length (WL; measured in Formicidae only) and head was found seriously injured by dogs and died shortly width (HW; Figure 2). Dry weights for each species and afterwards on November 24, 2013, in a peri-urban resi- their relative castes and stages were obtained by oven dential area in the New Territories of Hong Kong Special drying five intact individuals of each species at 40C Administrative Region. The animal was sent to the Wild until constant weight was reached and measured with a Animal Rescue Centre of Kadoorie Farm & Botanic microbalance (to the nearest 0.01 mg; Table 1). Garden to extract the gut contents. Gut contents were preserved in 70% ethanol and later examined under a Literature Review on Chinese Pangolin Diet 40 x stereo microscope. Within the gut, only ants and termites were present, and these were sorted based on Prey composition was reviewed through extensive their external morphological characters and point searches on Google Scholar and CNKI, using the key- words ‘‘Chinese pangolin,’’ ‘‘Manis pentadactyla,’’ ‘‘diet,’’ and their corresponding Chinese characters (i.e., ‘‘ ,’’ ‘‘ ,’’ ‘‘ ,’’ and ‘‘ ’’) for pertinent dietary data published before 2017. The compiled species list on diet composition was checked for taxonomic val- idity and compared with the known distribution of each prey species (if scientific name present) within antmap- s.org (Janicki, Narula, Ziegler, Gue´nard, & Economo, 2016) and where necessary revised to reflect the current taxonomic status (Table 2). Insights Into Habitat Use From Ant Prey We used previous data from extensive ant surveys con- ducted in Hong Kong (Fellowes, 1997) to calculate ant species occurrences in different habitats and used these as Figure 1. Picture of a wild Chinese pangolin (Manis pentadactyla) proxies for their local abundance and habitat association. in Hong Kong. Photograph courtesy of Gary Ades. Here again, taxonomy was updated through direct Figure 2. Vectors presenting the ant body measurements taken in mm. (a) Head width (HW) and (b) Weber’s length (WL). Lee et al. 3 Table 1. List of Ant and Termite Prey Species (Worker Caste Unless Otherwise Stated) and Total Number of Individuals Recovered From the Gut of a Juvenile Chinese Pangolin. Body measurements (M Æ SD) Frequency of occurrence (%) No. of individuals Total DW Taxon WL HW DW (% total) (% total) G S F Hymenoptera Formicinae Anoplolepis gracilipes 2.49 Æ 0.08 1.03 Æ 0.04 0.14 Æ 0.04 199 (0.75) 27.02 (0.07) 5.88 23.08 14.81 Camponotus mitis 5.63 Æ 0.14 1.97 Æ 0.08 2.15 Æ 1.36 70 (0.26) 150.51 (0.41) 23.53 46.15 29.63 Camponotus nicobarensis 4.13 Æ 0.39 2.93 Æ 0.87 2.96 Æ 1.45 6804 (25.56) 20122.15 (54.18) 5.88 30.77 22.22 Female alates 27.54 Æ 1.53 79 (0.30) 2175.98 (5.86) Male alates 1.78 Æ 0.43 460 (1.73) 820.09 (2.21) Camponotus variegatus dulcis 4.53 Æ 0.05 1.84 Æ 0.11 1.06 Æ 0.42 121 (0.45) 128.57 (0.35) Polyrhachis demangei 3.08 Æ 0.07 2.33 Æ 0.04 1.24 Æ 0.22 8 (0.03) 9.94 (0.03) 0 7.69 0 Polyrhachis tyrannica 4.64 Æ 0.23 2.79 Æ 0.10 6.74 Æ 3.06 899 (3.38) 6059.44 (16.31) 5.88 61.54 62.96 Myrmicinae Aphaenogaster exasperata 3.60 Æ 0.32 1.80 Æ 0.16 1.01 Æ 0.17 59 (0.22) 59.65 (0.16) 0 0 18.52 Crematogaster dohrni 1.88 Æ 0.32 1.60 Æ 0.32 0.35 Æ 0.07 16500 (62.00) 5827.80 (15.69) 0 0 7.41 Pupae 1.68 Æ 0.86 604 (2.27) 1013.15 (2.73) Isoptera Termitidae Macrotermes barneyi Workers 2.18 Æ 0.65 0.98 Æ 0.09 681 (2.56) 668.20 (1.80) Soldiers 2.37 Æ 0.03 0.60 Æ 0.03 131 (0.49) 79.23 (0.21) Total 26,615 37,141.73 Note. The following average body measurements (ÆSD) were recorded from five individuals of each species: WL ¼Weber’s length (mm); HW ¼ Head width (mm), DW ¼ Dry weight (mg). The frequency of occurrence of each species in three different habitats (G: Grassland, n ¼ 17; S: Shrubland, n ¼ 13; F: Forest, n ¼ 27) in Hong Kong SAR were extracted from Fellowes (1997). examination of the specimens collected to allow taxo- or castes are usually found only within nests and are nomic correspondence between both studies. known to be more nutritious than workers, in particular due to their higher fat content (Redford & Dorea, 1984). Results The large number of individuals recovered (>26,000 indi- viduals) also supports the nest-raiding hypothesis. As a A total of 25,803 ants and 812 termites, comprising six point of comparison on ant abundance in Hong Kong genera and nine species, were recorded.