The Formosan pangolin, Manis pentadactyla pentadactyla Linnaeus (Fig. 1A), was once a commonly seen mammal in Taiwan. They were predominately found in mountainous areas, <1,000 m in altitude (Chao 1989). Due to habitat destruction and over hunting between the 1950s and 1970s (Chao 1989), the species is considered threatened to date (Duckworth et al. 2008) and protected by national law since 1989 (Wang 2008). Efforts have been made for pangolin conservation and fundamental biology in Taiwan (Chang 2003; Fan 2004; Wang 2006; Chan 2008; Wu 2008), but little is known about their food source and sustainable ecosystem.

Termites and ants are believed to be the major food source for all pangolin species. In mainland China, Wu et al. (2005) reported 6 termite species including Coptotermes formosanus Shiraki, Macrotermes barneyi Light, Odontotermes formosanus (Shiraki), O. hainanensis Light, O. zunyiensis Li et Ping, and Pericapritermes nitobei (Shiraki) and five ant species including Camponotus sp., Odontomachus monticola (Emery), Paratrechina bourbonica (Forel), Pheidole sp., and Polyrhachis dives Fr. Smith were food source of the Chinese pangolin, Manis pentadactyla Linnaeus. In Taiwan, several ant species including Ca. friedae Forel, Crematogaster rogenhoferi Mayr, Cr. dohrni fabricans Forel, Ph. yanoi Forel, and Po. dives have been found in their stomachs (Sonan 1912, 1941; Takahasi 1934), but the termite species consumed by Formosan pangolins has remained unknown. In the current study, a field survey of the termites was conducted in a Formosan pangolin habitat. The ecology of these termite species and their potential as a food source of the Formosan pangolins are discussed.

MATERIALS and METHOD

Between 2009 and 2010, radio-tracking results of pangolins' activities at Song-Ling Village, Taitung County, Taiwan (Fig 1B) revealed the presence of 1 male and five females in a 120-ha area (Fig. 1C) (Lin 2011). Their habitat consisted of mosaic vegetation including secondary forest, tree plantation, bamboo forest, grassland, and orchards. A termite survey was conducted in this habitat on May 20 and 21, 2010. Termite samples were collected from soil, dead trees, decayed wood, and dead branches of living trees by using axes and aspirators, and preserved in 85% ethanol. Species identifications were made based on morphological descriptions (Shiraki 1909; Nawa 1911; Oshima 1912; Hozawa 1915) and keys offered by Chung and Chen (1994), as well as Li (2010). The voucher specimens will be deposited at the National Museum of Nature Science, Taichung, Taiwan. The lifetypes and feeding groups of the 7 species are summarized in Table 1 following the categories described by Abe (1987), Donovan et al. (2001), and Eggleton & Tayasu (2001).

RESULTS and DISCUSSION

One hundred and thirty three termite samples were collected from 17 localities (Fig. 1C), representing 7 species in 6 genera and 3 families (Table 1). The ecology of these termite species and their potential as a food source of Formosan pangolins are discussed below. Kalotermitidae was not as well represented in the current survey as Rhinotermitidae and Termitidae (Table 1). Two Glyptotermes species, G. fuscus Oshima and G. satsumensis (Matsumura), were found at five locations in secondary forests. Both species nested in dead trees or dead branches of living trees. Trees infested by several thousand individuals of G. satsumensis were found, but all G. fuscus colonies were small with <1,000 individuals. Extensive galleries of G. satsumensis were observed inside tree trunks, but G. fuscus typically excavates tunnels along the outer layers of tree trunks and branches. Another kalotermitid species, Neotermes koshunensis (Shiraki) was collected at 4 locations in abandoned orchards. Most colonies were found in dead plum trees with high moisture content. The colony size of N. koshunensis can be as large as several thousand individuals (Maki & Abe 1986). Kalotermitidae is a primitive termite family, and sound wood is their primary food source (Krishna 1961). An entire colony is usually restricted to a single piece of wood, hence, it is called a “single-piece nester” (Eggleton & Tayasu 2001). To collect kalotermitids, tools such as axes were usually required. Therefore, we speculated that it would be difficult for pangolins to excavate the infested dry wood for kalotermitids. Due to nesting in sound wood and their small colony size, the 3 kalotermitid species are less likely to be the food source of pangolins.

Fig. 1.

Formosan pangolin, M. pentadactyla pentadactyla (A) is commonly found at Song-Ling Village in southeast of Taiwan (B); current termite survey was conducted in 6 pangolin habitats (C) (gray area). The largest territory occupied by a male pangolin overlapped with small territories of five female individuals. Closed circles represent termite collection sites.

TABLE 1.

TERMITE SPECIES RECORDS FROM SONG-LING VILLAGE ALPHABETICALLY BY FAMILY.

Reticulitermes flaviceps (Oshima) was the only rhinotermitid species found in the current survey, and it was collected from 12 of the 17 sites. This species was commonly discovered at the interface between decayed wood and wet soil. The colony size of R. flaviceps remains unknown, but Reticulitermes colonies containing several hundred thousand individuals is often reported (Howard et al. 1982; Su et al. 1993; Haagsma & Rust 1995; Haverty et al. 2000). The nest structure of most rhinotermitids consists of a subterranean main nest and some satellite nests located in infested wood or soil. This lifetype was classified as intermediate nester by Abe (1987) and Eggleton & Tayasu (2001). Because R. flaviceps nests in soil and is found in high abundance, it is likely to be a major food source of pangolins.

Three higher termite (Termitidae) species, Nasutitermes parvonasutus (Shiraki), O. formosanus, and P. nitobei, were found in the current survey, and their lifetypes and food sources are quite different (Table 1). Na. parvonasutus was collected at 12 of the 17 collection sites, usually in wooded areas. Shelter tubes made of mud on the surface of wood was observed for this species, and hence it was speculated that several nesting sites may be connected by foraging tubes of a single colony. Nasutitermes were classified as intermediate nesters by Eggleton & Tayasu (2001). Even though Na. parvonasutus is abundant, it may be difficult for pangolins to excavate their nests from the infested wood. O. formosanus is the most abundant species found in the current survey. Forty colony samples were collected from 12 of the 17 collection sites. O. formosanus is a fungus growing termite species, and has a complex subterranean nest system consisting of a major chamber and multiple small chambers (Tsai 1965; Huang 2004). O. formosanus was found inside wood and in foraging tubes on the surface of tree trunks, dead grass, fallen tree branches, etc. O. formosanus does not nest in its food sources, hence, it belongs to a separate-piece nester classified by Eggleton & Tayasu (2001). The colony size of an O. formosanus can be as large as 2,000,000 termite individuals (Huang et al. 1989). Because O. formosanus is the most abundant species with large colony sizes and a soil-nesting behavior, we speculate that O. formosanus is most likely a major food source of pangolins. Another termitid species, P. nitobei, is a soil feeding termite, only found at 3 of the 17 collection sites. This species built small soil chambers under stones and grass roots with <100 individuals in each chamber. According to the observations by Tu (1954) and Hsueh (1998), these small chambers were interconnected with tunnels. The central chamber of a mature colony could be as deep as 1 m (Hsueh 1998), and no large colony exceeding a thousand individuals has ever been reported. Because P. nitobei feeds on organic matter close to the ground surface, pangolins should be able to excavate topsoil or flip over small stones to intercept P. nitobei. However, its low abundance would decrease the interception rate.

Based on abundance, colony size, and lifetype, we concluded that O. formosanus and R. flaviceps are likely to be the major termite species consumed by Formosan pangolins. The wood nesting species, including the 3 kalotermitids and Na. parvonasutus, are not likely to be available for pangolin predation.