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Philippine pangolin Manis culionensis (de Elera, 1915)
C H A P T E R
7 Philippine pangolin Manis culionensis (de Elera, 1915) Sabine Schoppe1,2, Lydia K.D. Katsis2, Dexter Alvarado1 and Levita Acosta-Lagrada2,3 1
Katala Foundation Inc., El Rancho, Puerto Princesa City, Philippines 2IUCN SSC Pangolin Specialist Group, N Zoological Society of London, Regent’s Park, London, United Kingdom 3Palawan Council for Sustainable Development Staff (PCSDS), Puerto Princesa City, Philippines O U T L I N E Taxonomy
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Ontogeny and reproduction
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Description
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Population
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Distribution
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Status
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Habitat
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Threats
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Ecology
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References
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Behavior
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Taxonomy Previously included in the genus Pholidotus (de Elera, 1915) and subgenus Paramanis (Schlitter, 2005), the species is here included in the genus Manis based on morphological and genetic evidence (Gaubert et al., 2018; Chapter 2). Despite early classification as a distinct species (de Elera, 1915; Lawrence, 1939;
Pangolins DOI: https://doi.org/10.1016/B978-0-12-815507-3.00007-1
Sanborn, 1952), much of the subsequent literature did not distinguish this species from the Sunda pangolin (Manis javanica), or considered it to be a subspecies (Corbet and Hill, 1992; Heaney et al., 1998; Pocock, 1924; Taylor, 1934). Feiler (1998) proposed a series of morphological characteristics distinguishing the two species, but did not consider many of the observations made by Lawrence (1939).
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7. Philippine pangolin Manis culionensis
Gaubert and Antunes (2005) classified this species as distinct from the Sunda pangolin based on six discrete morphological characters. They include (1) the number of scale rows across the middle of the back (following a line perpendicular to the anteroposterior axis): 1921 in the Philippine, and 1518 in the Sunda pangolin (though see Description); (2) uniformly small scales in the nuchal, scapular, and postscapular regions in the Philippine pangolin, which are larger in the Sunda species; (3) the ratio of the nasal bone to total skull length, which is smaller in the Philippine (,1/3) and larger ( . 1/3) in the Sunda pangolin; (4) the posterior region of the palatine bone which is weaker in the Philippine pangolin, i.e., is not ventrally inflated and has short lateral walls: it is strong, ventrally inflated and has large lateral walls in the Sunda pangolin; (5) the posterior extension of the zygomatic process, which is short and not posterior to the sphenopalatine foramen in the Philippine, but long and posterior to the sphenopalatine foramen in the Sunda pangolin; and (6) the ratio of head and body to tail length, which is smaller in the Philippine (1.11 6 0.03, mean 6 SD, n 5 5) compared to the Sunda pangolin (1.25 6 0.13, n 5 20; though see Description). Feiler (1998) and Lawrence (1939) suggested 15 additional morphological features to distinguish the two species, but Gaubert and Antunes (2005) did not support their utility. Delimitation of the Philippine from the Sunda pangolin was supported by genetic analyses (see Gaubert et al., 2018). The species is monotypic. Records from archeological sites on Palawan Island date back 50007000 years (Gaubert, 2011). The split between the Philippine and Sunda pangolin is speculated to have occurred when Early Pleistocene land bridges between Borneo and Palawan were submerged by rising sea levels about 500,000800,000 years ago (Gaubert and Antunes, 2005).
Etymology: Manis (see Chapter 4); the epithet culionensis references the island of Culion in the Philippines.
Description The Philippine pangolin is a medium-sized mammal, typically weighing 47 kg, and reaches a total length of 100130 cm (Table 7.1). The species appears to be sexually dimorphic, with males larger and heavier than females (Schoppe et al., in prep. a; Table 7.1). Morphologically, the species is very similar to the Sunda pangolin. The body is covered in keratinous, overlapping scales, which grow from the skin and are rounded. Exceptions include the ventral surface, inner sides of the limbs, and parts of the head and face which are pinkish in color and covered in dense white hair (Fig. 7.1). A small number of thick hairs or bristles grow from the base of the scales. The tail is approximately 90% of head-body length (Gaubert and Antunes, 2005) and is covered in scales both dorsally and ventrally. An exception is the tail tip on the ventral side, which lacks a median scale and is replaced by a cutaneous pad. There are 1921 transversal scale rows on the body (Gaubert and Antunes, 2005), and 2832 rows of scales on the tail margins (Table 7.1). Total scales number approximately 8501000 (Table 7.1) and vary in size and shape. Scales on the dorsum are broad and rhomboid-shaped, and twice as wide as the first row of postscapular scales (Gaubert, 2011). On the limbs, scales are graduated and the hindlimbs have a central keel terminating in a sharp point: the scales on the tail margins are also sharply pointed. Like in other Asian pangolins, the medio-dorsal scale row continues to the tail tip (Jentink, 1882). Scale color varies from creamy-orange, dirty yellowish-white to dark brown (Fig. 7.1), and may be uniform or individuals may possess scales of variable color (Gaubert and Antunes, 2005), which is
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Description
TABLE 7.1 Philippine pangolin morphometrics. Measurement Weight
Body
Vertebrae
Skull
Scales
Country
Source(s)
Weight (R)
4.9 (2.77.3) kg, n 5 9
Philippines
S. Schoppe, unpubl. data
Weight (Q)
3.2 (33.5) kg, n 5 4
Philippines
S. Schoppe, unpubl. data
Weight unsexed
3.6 (2.25.9) kg, n 5 21
Philippines
A. Ponzo and S. Schoppe, unpubl. data
Total length (R)
1067 (8401330) mm, n 5 8
Philippines
S. Schoppe, unpubl. data
Total length (Q)
961 (8281030) mm, n 5 4
Philippines
S. Schoppe, unpubl. data
Head-body length (R)
582 (450740) mm, n 5 8
Philippines
S. Schoppe, unpubl. data
Head-body length (Q)
533 (470563) mm, n 5 4
Philippines
S. Schoppe, unpubl. data
Tail length (R)
486 (3959) mm, n 5 8
Philippines
S. Schoppe, unpubl. data
Tail length (Q)
428 (358470), n 5 4
Philippines
S. Schoppe, unpubl. data
Total number of vertebrae
No data
Cervical
No data
Thoracic
No data
Lumbar
No data
Sacral
No data
Caudal
2930
Length (unsexed)
6095 mm
Breadth across zygomatic processes
No data
Total number of scales
Gaubert, 2011 Philippines
Gaubert, 2011
940 (854999), n 5 3
Philippines
Ullmann et al., 2019
No. of scale rows (transversal, body)
1921, n 5 9
Philippines
Gaubert and Antunes, 2005
No. of scale rows (longitudinal, body)
No data
No. of scales on outer margins of tail
2832, n 5 4
Philippines
L. Katsis and D. Challender unpubl. data; T. Ullmann, unpubl. data
No. of scales on median row of tail
2832, n 5 4
Philippines
L. Katsis and D. Challender unpubl. data; T. Ullmann, unpubl. data
Scales (wet) as proportion of body weight
No data
Scales (dry) as proportion of body weight
No data
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7. Philippine pangolin Manis culionensis
FIGURE 7.1 Adult female Philippine pangolin: this species is semi-arboreal. Photo credit: Dexter Alvarado.
sometimes limited to scale margins and/or the tip (e.g., darker at the tip; L. Katsis, pers. obs.). Observations indicate that juveniles may possess several white-translucent scales on the distal part of the tail, which may darken with age (D. Alvarado, pers. obs.). The head is conical in shape and largely naked, with the exception of small scales on the forehead, which extend anteriorly and terminate before the rhinarium. The face is pinkish-gray and the rhinarium is a darker pink-brown. Ear pinnae are present, but like in the Sunda pangolin comprise a subvertical ridge of integument posterior to the auditory orifice, and are less pronounced than in the Chinese pangolin (M.
pentadactyla). The eyes are small with a dark iris and surrounded by thick swollen eyelids. As with all pangolins, this species lacks teeth and has a long tongue that retracts into a pouch in the throat. The oral cavity is small. The species is pentadactylous with five digits on the fore- and hindfeet. Each digit terminates with a claw, the largest (and strongest) of which is the middle. The second and fourth claws are smaller but of approximately equal size. The first and fifth digits (and claws) are vestigial and essentially non-functional. Digit and claw length and disposition on the hindfeet approximates the forefeet. It is presumed that the species possesses a pair of anal glands in the circumanal
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Distribution
area. The genetalia are similar to the Sunda pangolin; females have two pectoral mammae. The Philippine pangolin is easily confused with the Sunda pangolin and the two species are hard to differentiate. Gaubert and Antunes (2005) posited that the species can be distinguished by a number of characteristics (see Taxonomy), including the number of transversal scale rows: 1921 in the Philippine and 1518 in the Sunda pangolin. However, other sources (Frechkop, 1931; Mohr, 1961; Wu et al., 2004; L. Katsis and D. Challender, unpubl. data) indicate that the Sunda pangolin possesses 1519 transversal scale rows i.e., there is overlap between the species. Gaubert and Antunes (2005) also assert that the ratio of head-body to tail length is a diagnostic characteristic, but the ratio of individuals measured for this chapter (1.21 6 0.06; mean 6 SD, n 5 12; see Table 7.1), more closely approximates that of the Sunda pangolin (see Gaubert and Antunes, 2005). Number of transversal scale rows (assuming they do not number 19), combined with the size of scales in the nuchal, scapular and postscapular regions (see Gaubert and Antunes, 2005) may be used to differentiate the species. The number of scales on the margins of the tail, if they number 3132, is also a diagnostic characteristic of the Philippine pangolin: the Sunda pangolin possesses up to 30 scale rows on the tail margins. These parameters are based on a small sample size (n 5 10) for the Philippine pangolin, and further research could reveal greater variation in scale number, and potentially greater overlap with the Sunda pangolin. Dependent on the purpose of differentiation between the species, DNA-based methods may be appropriate (see Luczon et al., 2016). The Philippine pangolin may also be confused with the Chinese pangolin. Distinguishing features of the former include smaller and less prominent ear pinnae, smaller and shorter claws on the forefeet, which are noticeably larger in the Chinese species, and the number of transversal scale rows and scales on the tail margins, which
number 1418 and 1420 on the Chinese species respectively (see Chapter 4), and are more numerous in the Philippine pangolin (Table 7.1).
Distribution Endemic to the Palawan faunal region in the Philippines, including Palawan Island, the Calamian Islands, and smaller surrounding islands (Fig. 7.2; Bourns and Worcester, 1894; de Elera, 1915; Everett, 1889; Heaney et al., 1998; Lawrence, 1939). Records from mainland Palawan include fossils found in the north of the island from the Terminal Pleistocene to Late Holocene (Lewis et al., 2008; Piper et al., 2011). The species occurs on Dumaran Island (Schoppe and Alvarado, 2016) and Batas Island in Taytay (Acosta and Schoppe, 2018; Schoppe et al., 2017) and Indigenous peoples indicate that the species occurs on islands off El Nido, including Lagen Island, Tagnipa, and Nagbilisong Islands in San Vicente (Acosta and Schoppe, 2018). The species has apparently been introduced to Apulit Island in El Nido, and possibly Lagen Island (S. Schoppe, unpubl. data). Within the Calamian Islands, north of mainland Palawan, the species occurs on Culion (de Elera, 1915; Heaney et al., 1998; Hollister, 1913), Busuanga (Hoogstraal, 1951), and Calauit Islands (Alviola, 1998). Interviews with local communities conducted between 2010 and 2015 confirmed the species’ presence on Busuanga, Culion, Calauit and Maglalambay (Paguntalan et al., 2010, 2012, 2015). Similarly, in interviews conducted in 2006 local people suggested that the species occurs on 12 islands dispersed across Busuanga, Calauit, and Culion, and at least nine smaller islands from the Calamian island group (Rico and Oliver, 2006). The species is apparently absent from Coron Island (Acosta and Schoppe, 2018; Rico and Oliver, 2006; Paguntalan et al., 2010, 2012, 2015) but is distributed in the municipality of Coron on Busuanga Island.
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7. Philippine pangolin Manis culionensis
FIGURE 7.2 Philippine pangolin distribution. Source: Schoppe et al., 2019.
There is uncertainty over distribution on Balabac Island, south of Palawan. Steere (1888) reported that the species was absent and there are no records in the literature. Indigenous peoples from southern Palawan also refuted the species’ occurrence on the island (Acosta and Schoppe, 2018). However, hunters in the Palawan tribe and local people from Balabac report that the species is present but in very low numbers (Schoppe and Cruz, 2008).
Habitat The Philippine pangolin primarily inhabits primary and secondary lowland forests
(Heaney et al., 1998; Hoogstraal, 1951), but uses a diverse range of habitats (Fig. 7.3). It has been recorded in lowland grassland-forest mosaics and logged-over lowland forest, in which most of the merchantable timber had been extracted (Esselstyn et al., 2004), agricultural ecosystems (Acosta-Lagrada, 2012; Schoppe and Cruz, 2009), coastal areas near beach forest and mangroves, and in riverine forest (Marler, 2016). There are records from up to 2015 m asl (Acosta-Lagrada, 2012). The species is thought to have an affinity to strangler figs (Ficus spp.) as the fruits of these trees attract ants, and the roots provide structures that pangolins can use for shelter
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Ecology
blocks of heavily modified habitats (e.g., monoculture plantations).
Ecology
FIGURE 7.3 The Philippine pangolin inhabits primary and secondary lowland forest but uses a diverse range of habitats including grassland-forest mosaics and beach forest. Photo credit: Dexter Alvarado.
(Schoppe and Cruz, 2009). The species has been found burrowing under other tree species, including bishop wood (Bischofia javanica) and Dysoxylum spp. (Acosta-Lagrada, 2012). The diverse range of habitats used suggests that the species is adaptable to habitat degradation and modification providing there is an adequate prey base (Acosta-Lagrada, 2012): this is similar to the Sunda pangolin, which persists in highly degraded forest (see Chapters 6 and 26). Acosta-Lagrada (2012) suggested that the species may occur at higher densities in primary forest but this requires further research and verification (see Chapter 34), as does the ability of the species to persist long-term in isolated
The species is semi-arboreal but there is little knowledge of its ecology, and most of what is known is based on research conducted between 2010 and 2018. The species likely lives in relatively stable home ranges. Minimum Convex Polygon (MCP) home range estimates for three males were 59, 96, and 120 ha (mean 5 61.6 ha) with core areas (where individuals spent $ 50% of the time) of 29, 45, and 68 ha respectively (mean 5 47.3 ha; Schoppe and Alvarado, 2016; Schoppe et al., 2017; in prep. b). The smallest home range estimate was for a young male that weighed 1.5 kg (and was likely recently independent see Chapter 6) at the onset of monitoring. Home ranges did not overlap, suggesting males are territorial (Schoppe et al., in prep. b). Equivalent estimates for two females based on 257 days of radio-tracking were 47 and 75 ha, with core areas of 12 and 18 ha, respectively. During the wet season (JuneNovember), home ranges of two females and a young male did not overlap, but did partially during the dry season (DecemberMay), which may be related to access to permanent water sources (Schoppe and Alvarado, 2016; Schoppe et al., in prep. b). Males traveled a mean distance of 4.2 6 0.6 km (range 35.3 km) within a 24 h period, and females, 3.1 6 0.6 km (range 04 km; Schoppe et al., 2017; in prep. b). Research using radiotelemetry on six wild-caught individuals has provided initial insights into homing behavior. Three males (including one young male; weight 5 1.5 kg) and three females were released 1.13.7 km away from sites of capture. After release, the three females and the young male established new home ranges near the release site, whereas the two adult males returned to their respective home ranges
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(Schoppe and Alvarado, 2016; Schoppe et al., 2017; in prep. b). Shelter takes the form of burrows on the forest floor, tree hollows (or in the fork of tree branches), between tree buttresses or roots, and dens under or between large rocks. AcostaLagrada (2012) suggested that dens are located in areas away from human disturbance, on slopes of 36 to .50 and 100200 m from water sources, which is similar to the Chinese pangolin (Wu et al., 2003; see Chapter 4). Observations suggest that the species prefers arboreal resting sites during the wet season and terrestrial sites during the dry season, which is potentially related to avoiding dens being flooded in the former (Schoppe et al., in prep. b). There is little knowledge of shelter use (e.g., site fidelity) but a male pangolin was observed to return to the same den for 23 consecutive nights before moving to another site, eventually returning to the previous den after about a week (S. Schoppe, unpubl. data). The Philippine pangolin is known to forage both terrestrially and in trees but there is little knowledge of prey species or foraging behavior. Acosta-Lagrada (2012) recorded consumption of two ant species, Odontomachus infandus and Diacamma sp., and one termite species, Nasutitermes sp. Schoppe and Alvarado (2015a) observed the species predating frequently on the weaver ant (Oecophylla smaragdina), a species preferred by the Sunda pangolin (Lim, 2007; see Chapter 6). Lim (2007) noted that the Sunda pangolin predated on 11 ant genera, which do occur in the Philippines (General and Alpert, 2012), and it is likely that the diet is similar to the Sunda pangolin, though only two of these genera are known to occur in Palawan, Polyrhachis and Oecophylla. Predators likely include pythons (e.g., reticulated python [Malayopython reticulatus]; Lim and Ng, 2008). Ecto-parasites include the tick Amblyomma javanense (Corpuz-Raros, 1993; Jaffar et al., 2018), and preliminary research
indicates that 86% of Philippine pangolins host this species (n 5 14; S. Schoppe, unpubl. data).
Behavior Solitary and predominantly nocturnal, the species rests during the day and is active at night (Schoppe and Alvarado, 2015a, 2016; Schoppe et al., in prep. b). Based on research using telemetry, peak activity for six study animals over an 11-day period was 23000400 (Schoppe et al., in prep. b). A young, independent male monitored for 42 days had an identical peak activity period, and was active for 12 hours a day (mean), and traveled a mean distance of 3.6 6 1.1 km (range 05 km) within a 24 hour period (Schoppe and Alvarado, 2015a, 2016; Schoppe et al., in prep. b). Preliminary research suggests that activity patterns may be influenced by the lunar phase, with individuals being active for longer periods during full moon (Schoppe and Alvarado, 2015a). Schoppe and Alvarado (2015a) note that a young male emerged from its den as early as 1200 noon during the new moon and returned by midnight, but during full moon (and between first and last quarter) emerged at dusk and returned in the early hours of the morning. In the dry season, individuals will immediately search for water after emerging from a burrow or other resting place, and drink prior to foraging; during the wet season, individuals will forage first before drinking and retreating to a resting place (Schoppe et al., in prep. b). In the dry season, an individual was observed to stand in a stream and drink for 3060 min before returning to its resting place (Schoppe et al., in prep. b). The species is quadrupedal. When walking the head and tail are held below the level of the body, and the forelimbs face inward with the claws perpendicular to the ground, and the weight is taken on the knuckles and outer margins of the claws (i.e., folded up wrists). Semi-
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FIGURE 7.4 Philippine pangolins are adept climbers and use their strong tail for support. Photo credit: Dexter Alvarado.
arboreal, the species is an adept climber, using its long tail as an extra limb (Fig. 7.4). Like the Sunda pangolin, the species moves its limbs in pairs when climbing tree trunks, the incredibly strong tail providing grip and bearing weight, and the species will descend trees head first (Fig. 7.4). The Philippine pangolin predates on ants and termites, both in trees and on the ground, and locates prey using its acute olfactory senses (Acosta-Lagrada, 2012; Schoppe and Alvarado, 2015a; Schultze, 1914). Having located an ant nest or termitaria the strong forelimbs are used to break into these structures and the long tongue is used to extract ants or termites of all life stages (e.g., eggs, adults). The nests are not destroyed, enabling insect colonies to recover, but feeding sites
are returned to during consecutive nights (Schoppe et al., in prep. b). In addition to searching for ant nests and termitaria, the species will search for prey among leaf litter and rotten wood on the forest floor. Schultze (1914) suggested that the Philippine pangolin may have a higher reliance on arboreal termite nests in the dry season, and terrestrial termite nests in the wet season, as terrestrial nests may be difficult to penetrate during the dry season; however, this requires verification. The species is sensitive to human presence and typically responds by fleeing (Schoppe et al., in prep. b). Otherwise, when sensing a threat, Philippine pangolins will flee if the threat is distant, or roll up into a ball if it is in close proximity (Fig. 7.5).
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likely strong similarities with the Sunda pangolin. Adult sex ratios at six sites in Palawan ranged from 1:0.6 to 1:1, with an average of 1:0.8 in favor of males (Schoppe et al., in prep. a).
Population
FIGURE 7.5 A male Philippine pangolin assessing whether it is safe to uncurl: like all pangolins, this species curls up into a ball when threatened. Photo credit: Sabine Schoppe.
Vocalizations are limited to a “hissing” sound when individuals are threatened (Schultze, 1914; Schoppe et al., in prep. a).
Ontogeny and reproduction Much of what is known is based on anecdotal evidence or presumed similarities with the Sunda pangolin (see Chapter 6). The Indigenous people of the Tagbanua, Batak and Palawan tribes report that the species has one offspring, but two fetuses have occasionally been encountered when the animals have been slaughtered (Acosta and Schoppe, 2018). It is presumed that breeding is aseasonal like the Sunda pangolin (Schoppe et al., in prep. a). However, local farmers in the species’ range have reported that females with young are typically seen in August (Schoppe and Cruz, 2009). In a telemetry study, a pregnant female was caught in September and observed with the young in November (Schoppe and Alvarado, 2016). There is little knowledge of estrus cycles, gestation, young development and maternal care, weaning, age at sexual maturity or population structure, which requires research, but there are
There is limited knowledge of, and quantitative data on, Philippine pangolin populations. Schoppe et al. (in prep. a) estimated density at six sites representing northeastern islands, central Palawan, and southern Palawan, using systematic searches of direct signs, primarily with dogs. Across these sites, estimated mean adult density was 2.5 6 1.4 adults/km2 (mean 6 SD). Population density was highest (3.5 and 4.0 adults/km2) on the islands in northeastern Palawan, which is potentially due to the remoteness of the islands and their protected status (Schoppe et al., in prep. a). Three central Palawan (Puerto Princesa City) sites had a mean adult density of 1.8 6 1.61 adult/km2 (Schoppe et al., in prep. a) and included one site where the species was not recorded (Schoppe and Alvarado, 2015b); mean density in Rizal in southern Palawan was 2 adults/km2. Other evidence indicates that the species is not evenly distributed across its range, is increasingly rare, and declining (Bayron, 2014; Schoppe et al., 2017; in prep. a). Indigenous peoples report the species was common in the late 1960s when human population density was lower and forest cover much higher (Acosta and Schoppe, 2018). Pangolins were frequently seen in the 1970s1980s, particularly in coastal and lowland areas, including in Aborlan (J. Fabello, pers. comm.). Rabor (1965) and Heaney et al. (1998) noted that the species was rare. Interview-based research indicates population declines. Multiple Indigenous peoples groups from the Tagbanua, Batak and Palaw’an Tribes, and Cuyunon communities from Palawan and the Calamian Islands
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Threats
estimated population declines of 85% in the south of the species’ range and 95% in the north between 1980 and 2018 (Acosta and Schoppe, 2018). Interviews with hunters and traders indicate the species is rare in southern Palawan and more common in the north (Schoppe and Cruz, 2009), while ethno-biological surveys and similar research suggests the species is increasingly rare and that sightings are uncommon (Acosta-Lagrada, 2012; Rico and Oliver, 2006). Local hunters report a decline in the number of pangolins caught per unit effort compared to the 1970s (Schoppe, 2013). One hunter in Brooke’s Point, southern Palawan, reported that in 1992 it was possible to catch 34 pangolins a week, but in 2012, similar effort resulted in only one pangolin a month (Acosta-Lagrada, 2012). Bayron (2014) reported similar results in Roxas, Puerto Princesa City and Quezon.
Status The Philippine pangolin is listed as Critically Endangered on The IUCN Red List of Threatened Species (Schoppe et al., 2019) and available evidence indicates declines across its range (see Population). However, there is a lack of quantitative data on populations. The species is listed as Critically Endangered in Palawan Province and Endangered at the national level in the Philippines. It is afforded protection under the Philippine Wildlife Act 9147, which prohibits the exploitation of threatened species, including by indigenous peoples for traditional use. The entirety of Palawan Province was declared a game refuge and bird sanctuary in 1969 and the species occurs in a number of protected areas, including the Mount Mantalingahan Protected Landscape and Puerto Princesa Underground River National Park. The species is included in CITES Appendix I.
Threats The principle threat to the Philippine pangolin is overexploitation. This includes local use and consumption and international trafficking and use of the species and its body parts, and is compounded by the species’ restricted geographic range. Habitat loss poses an additional, indirect threat. Pangolins have been hunted on Palawan for at least 6000 years (Lewis et al., 2008) and Indigenous peoples have traditionally used, and continue to use the species for subsistence, medicinal, and ritualistic purposes. This includes the consumption of meat as a protein source, often with perceived health benefits including the treatment of gastrointestinal diseases, inflammation, asthma, and flatulence (Eder, 1987; Esselstyn et al., 2004; Estrada et al., 2015). The scales are used (in powered form) to treat asthma (Esselstyn et al., 2004) and prostate-related illnesses (Acosta-Lagrada, 2012), while the Palaw’an in Bataraza use the scales on belts to treat back pain, and multiple Indigenous communities use them to deter bad spirits (see Chapter 12; Acosta and Schoppe, 2018; Bayron, 2014; Estrada et al., 2015). In Narra, burnt scales are used to treat mothers who have just given birth, and to stop thunder (Acosta-Lagrada, 2012; Acosta and Schoppe, 2018). At Brooke’s Point, Indigenous peoples will drink the blood for its believed rejuvenation properties (Acosta-Lagrada, 2012). The species is poached for trade in its blood, meat, skin and scales within the Philippines (Cruz et al., 2007; Esselstyn et al., 2004). Bayron (2014) reported that poaching levels were particularly high in northern Palawan, and estimated that 448 pangolins were poached in three municipalities (Puerto Princesa City, Roxas and Quezon) in Palawan in 2012 alone. Poaching takes place by local people, but also by individuals from neighboring areas (barangays),
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including with the use of dogs (Acosta and Schoppe, 2018; Bayron, 2014). It takes place to meet consumer demand in major cities, and analysis of seizure data suggests there is substantial domestic demand for pangolin meat and scales in cities including Metro Manila (Gomez and Sy, 2018). Indications from trade research and insights from indigenous peoples are that exploitation for domestic and international trade is the main, contemporary driver of pangolin offtake, as opposed to local use (Lacerna and Widmann, 2008; Schoppe and Cruz, 2009). The CITES trade data indicate that approximately 10,000 pangolins, in the form of skins, that were traded internationally in the 1980s, originated in or were exported from the Philippines. Despite a decline in international trade in pangolin skins post-2000 (see Chapter 16), international trade has otherwise continued, albeit illegally. Gomez and Sy (2018) report that during 20012017 at least 39 seizures took place in which the Philippines was implicated as a source country or place of seizure. This included an estimated 667 Philippine pangolins, primarily comprising quantities of meat and scales, and dead individuals, though actual illegal trade volumes were likely higher. Most of these seizures took place in Palawan, but seizures were also made on Luzon, Mindoro, Negros and Tablas (Gomez and Sy, 2018). Exact trafficking routes are not well documented but the species is illegally traded to East Malaysia (e.g., Kudat, Sandakan) and Peninsular Malaysia for subsequent export to China, including for use in traditional medicines (Pantel and Anak, 2010; Schoppe and Cruz, 2009). However, it is suspected that Philippine pangolin scales may be exported and then subsequently imported after processing into Traditional Chinese Medicine (TCM) for domestic consumption (E. Sy, pers. comm.). The Philippines has further been implicated in highly organized international pangolin trafficking (see Luczon et al., 2016). There remains a strong financial incentive for local people and indigenous peoples to poach
and sell pangolins into illegal trade, which is apparently exacerbated by issues over their legitimate access to, and use of, non-timber forest products for livelihood purposes. This is compounded by law enforcement being a low priority for enforcement and judicial agencies in the Philippines, combined with a lack of human and technical resources, resulting in little deterrent to would-be poachers and traffickers, and the perception that illegal trade in pangolins is low risk. Habitat loss poses an indirect threat. It results in the opening up of previously inaccessible areas through the creation of road networks for commercial concessions, which in turn makes pangolins susceptible to hunting and poaching: it also increases the likelihood of roadkill. As with the Sunda pangolin, there is a need for research into how the Philippine pangolin uses natural and modified habitats (e.g., monoculture plantations) and the ability of the species to persist in highly modified isolated habitat blocks in the long-term.
References Acosta-Lagrada, L.S., 2012. Population density, distribution and habitat preferences of the Palawan Pangolin, Manis culionensis (de Elera, 1915). M.Sc. Thesis, University of the Philippines Los Ban˜os, Laguna, Philippines. Acosta, D., Schoppe, S., 2018. Proceedings of the Stakeholder Workshop on the Palawan Pangolin Balintong, Bulwagang Princesa Tourist Inn, Puerto Princesa City, 17 February 2018, Katala Foundation Inc, Puerto Princesa City, Palawan, Philippines, pp. 110. Alviola, P.L. III, 1998. Land vertebrates of Calauit Island, Palawan, Philippines. Asia Life Sci. 7 (2), 157170. Bayron, A.C., 2014. Trade dynamics of Palawan pangolin Manis culionensis. B.Sc. Thesis, Western Philippines University, Palawan, Philippines. Bourns, F.S., Worcester, D.C., 1894. Preliminary Notes on the Birds and Mammals Collected by the Menage Scientific Expedition to the Philippine Islands. Minnesota Academy of Sciences, Minneapolis. Corbet, G.B., Hill, J.E., 1992. The Mammals of the Indomalayan Region: A Systematic Review. Oxford University Press, Oxford.
I. What is a Pangolin?
References
Corpuz-Raros, L.A., 1993. A checklist of Philippine mites and ticks (Acari) associated with vertebrates and their nests. Asia Life Sci. 2 (2), 177200. Cruz, R.M., van den Beukel, D.V., Lacerna-Widmann, I., Schoppe, S., Widmann, P., 2007. Wildlife trade in Southern Palawan, Philippines. Banwa 14 (1), 1226. de Elera, C.D., 1915. Contribucio´n a la Fauna Filipina. Colegio de Santo Toma´s, Manila. Eder, J.F., 1987. On the Road to Tribal Extinction: Depopulation, Deculturation, and Adaptive Well-Being Among the Batak of the Philippines. University of California Press, Berkeley. Esselstyn, J.A., Widmann, P., Heaney, L.R., 2004. The mammals of Palawan Island, Philippines. Proc. Biol. Soc. Washington 117 (3), 271302. Estrada, Z.J.G., Panolino, J.G., De Mesa, T.K.A., Abordo, F. C.B., Labao, R.N., 2015. An ethnozoological study of the medicinal animals used by the Tagbanua tribe in Sitio Tabyay, Cabigaan, Aborlan, Palawan. In: Matulac, J.L.S., Cabrestante, M.P., Palon, M.P., Regoniel, P.A., Gonzales, B.J., Devanadera, N.P. (Eds.), Proceedings of the 2nd Palawan Research Symposium 2015. National Research Forum on Palawan Sustainable Development: Science, Technology and Innovation for Sustainable Development, 910 December, Puerto Princesa City, Palawan, Philippines, pp. 123128. Everett, A.H., 1889. Remarks on the zoo-geographical relationships of the island of Palawan and some adjacent islands. J. Zool. 57 (2), 220228. Feiler, A., 1998. Das Philippinen-Schuppentier, Manis culionensis Elera, 1915, eine fast vergessene Art (Mammalia: Pholidota: Manidae). Zoologische Abhandlungen Staatliches Museum Fu¨r Tierkunde Dresden 50, 161164. Frechkop, S., 1931. Notes sur les mammife`res. VI. Quelques observations sur la classification des pangolins (Manidae). Bull. du Musee royal d0 Histoire naturelle de Belgique VII (22), 114. Gaubert, P., 2011. Family Manidae. In: Wilson, D.E., Mittermeier, R.A. (Eds.), Handbook of the Mammals of the World, vol. 2. Hoofed Mammals. Lynx Edicions, Barcelona, pp. 82103. Gaubert, P., Antunes, A., 2005. Assessing the taxonomic status of the Palawan pangolin Manis culionensis (Pholidota) using discrete morphological characters. J. Mammal. 86 (6), 10681074. Gaubert, P., Antunes, A., Meng, H., Miao, L., Peigne, S., Justy, F., et al., 2018. The complete phylogeny of pangolins: scaling up resources for the molecular tracing of the most trafficked mammals on earth. J. Hered. 109 (4), 347359. General, D.M., Alpert, G.D., 2012. A synoptic review of the ant genera (Hymenoptera, Formicidae) of the Philippines. ZooKeys 200, 1111. Gomez, L., Sy, E.Y., 2018. Illegal pangolin trade in the Philippines. TRAFFIC Bull. 30 (1), 3740.
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Heaney, L.R., Balete, D.S., Dollar, M.L., Alcala, A.C., Dans, A.T.L., Gonzales, P.C., et al., 1998. A synopsis of the mammalian fauna of the Philippine Islands. Fieldiana (Zool.) 88, 161. Hollister, N., 1913. A review of the Philippine land mammals in the United States National Museum. Proc. United States Natl. Mus. 46, 299341. Hoogstraal, H., 1951. Philippine zoological expedition, 19461947. Narr. Itinerary. Fieldiana (Zool.) 33, 186. Jaffar, R., Low, M.R., Maguire, R., Anwar, A., Cabana, F., 2018. WRS Husbandry Manual for the Sunda Pangolin (Manis javanica), first ed. Wildlife Reserves Singapore, Singapore. Jentink, F.A., 1882. Note XXV. Revision of the Manidae in the Leyden Museum. Notes from the Leyden Museum IV, 193209. Lacerna, I.D., Widmann, P., 2008. Biodiversity utilization in a Tagbanua community, Southern Palawan, Philippines. In: Widmann, I.L., Widmann, P., Schoppe, S., van den Beukel, D.V., Espeso, M. (Eds.), Conservation Studies on Palawan Biodiversity: A Compilation of Researches Conducted in Cooperation With or Initiated by Katala Foundation Inc. Katala Foundation Inc, Puerto Princesa City, Palawan, pp. 158170. Lawrence, B.L., 1939. Collections from the Philippine Islands. Mammals. Bull. Mus. Comp. Zool. 86, 2873. Lewis, H., Paz, V., Lara, M., Barton, H., Piper, P., Ochoa, J., et al., 2008. Terminal Pleistocene to mid-Holocene occupation and an early cremation burial at Ille Cave, Palawan, Philippines. Antiquity 82 (316), 318335. Lim, N.T.-L, 2007. Autoecology of the Sunda Pangolin (Manis javanica) in Singapore. M.Sc. Thesis, National University of Singapore, Singapore. Lim, N.T.-L., Ng, P.K.L., 2008. Predation on Manis javanica by Python reticulatus in Singapore. Hamadryad 32 (1), 6265. Luczon, A.U., Ong, P.S., Quilang, J.P., Fontanilla, I.K.C., 2016. Determining species identity from confiscated pangolin remains using DNA barcoding. Mitochondrial DNA Part B 1 (1), 763766. Marler, P.N., 2016. Camera trapping the Palawan Pangolin Manis culionensis (Mammalia: Pholidota: Manidae) in the wild. J. Threat. Taxa 8 (12), 94439448. Mohr, E., 1961. Schuppentiere. Neue Brehm-Bucherei. A. Ziemsen Verlag, Wittenberg Lutherstadt. Paguntalan, L.J., Gomez, R.K., Oliver, W., 2010. Threatened Species of the Calamian Islands: Developing an Integrated Regional Biodiversity Conservation Strategy in a Global Priority Area, Phase II - Biological Survey. Philippines Biodiversity Conservation Foundation. Katala Foundation Inc., and National Geographic Society Conservation Trust. Paguntalan, L.J., Jakosalem, P.G., Oliver, W., 2012. Threatened Species of the Calamian Islands: Developing an Integrated Regional Biodiversity Conservation Strategy in a Global Priority Area, Phase
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II - Biological Survey. A report submitted to National Geographic Society. Paguntalan, L.J., Jakosalem, P.G., Oliver, W., Reintar, A.R., Doble, K.J., 2015. Threatened Species of the Calamian Islands: Developing an Integrated Regional Biodiversity Conservation Strategy in a Global Priority Area, Phase II - Follow-up Biological Survey. A report submitted to Community Centered Conservation and GIZ - Protected Areas Management Enhancement Project (GIZPAME). Pantel, S., Anak, A.N., 2010. A preliminary assessment of Sunda pangolin trade in Sabah. TRAFFIC Southeast Asia, Petaling Jaya, Selangor, Malaysia. Pocock, R.I., 1924. The external characters of the pangolins (Manidae). Proc. Zool. Soc. Lond. 94 (3), 707723. Piper, P.J., Ochoa, J., Robles, E.C., Lewis, H., Paz, V., 2011. Palaeozoology of Palawan Island, Philippines. Quat. Int. 233 (2), 142158. Rabor, D.S., 1965. Threatened species of small mammals in tropical South East Asia. The problem in the Philippines. In: Talbot, L.M., Talbot, M.H. (Eds.), Proceedings of the Conference on Conservation of Nature and Natural Resources in Tropical South East Asia, Bangkok, Thailand, 29 November 4 December 1965. IUCN, Morges, Switzerland, pp. 272277. Rico, E., Oliver, W., 2006. Threatened Species of the Calamian Islands: Developing an Integrated Regional Biodiversity Conservation Strategy in a Global Priority Area, Phase I, Findings and Recommendations of an Islands-Wide Ethnobiological Survey. A report submitted to National Geographic Society. Sanborn, C.C., 1952. Philippine zoological expedition 19461947. Mammals. Fieldiana (Zool.) 33, 89158. Schlitter, D.A., 2005. Order Pholidota. In: Wilson, D.E., Reeder, D.M. (Eds.), Mammal Species of the World: A Taxonomic and Geographic Reference, third ed. Johns Hopkins University Press, Baltimore, pp. 530531. Schoppe, S., 2013. Catch me if you can! How can we monitor populations of the Philippine Pangolin? Oral presentation, 1st IUCN SSC Pangolin Specialist Group Conservation Conference, 24 27 June 2013, Wildlife Reserves Singapore, Singapore. Schoppe, S., Cruz, R., 2008. Armoured but endangered: Galvanizing action to mitigate the illegal trade in Asian Pangolins: The situation in Palawan, Philippines. A report submitted to TRAFFIC by Katala Foundation Incorporated, pp. 116. Schoppe, S., Cruz, R., 2009. The Palawan Pangolin Manis culionensis. In: Pantel, S., Chin, S.-Y., (Eds.), Proceedings of the Workshop on Trade and Conservation of Pangolins Native to South and Southeast Asia, 30 June 2 July 2008, Singapore Zoo, Singapore.
TRAFFIC Southeast Asia, Petaling Jaya, Selangor, Malaysia, pp. 176188. Schoppe, S., Alvarado, D., 2015a. Conservation Needs of the Palawan Pangolin Manis culionensis Phase II (Extension), Final Scientific and Financial Report Submitted to Wildlife Reserves Singapore. Katala Foundation Inc, Puerto Princesa City, Palawan, Philippines, pp. 136. Schoppe, S., Alvarado, D., 2015b. Conservation Needs of the Palawan Pangolin Manis culionensis Phase I. Final Scientific and Financial Report to Wildlife Reserves Singapore. Katala Foundation Inc, Puerto Princesa City, Palawan, Philippines, pp. 130. Schoppe, S., Alvarado, D., 2016. Movements of the Palawan Pangolin Manis culionensis Final Project Report Submitted to Wildlife Reserves Singapore. Katala Foundation Inc, Puerto Princesa City, Palawan, Philippines, pp. 116. Schoppe, S., Alvarado, D., Luz, S., 2017. Movement patterns of the Palawan Pangolin Manis culionensis. Poster presentation at 26th Philippine Biodiversity Symposium, 1821 July 2017, Ateneo de Manila University, Quezon City, Philippines. Schoppe, S., Katsis, L., Lagrada, L., 2019. Manis culionensis. The IUCN Red List of Threatened Species 2019: e.T136497A 123586862. Available from: , http://dx.doi.org/10.2305/ IUCN.UK.2019-3.RLTS.T136497A123586862.en . . Schoppe, S., Alvarado, D., Luz, S., in prep. a. First data on the population density of the Palawan Pangolin Manis culionensis from Palawan, Philippines. Katala Foundation Inc., Puerto Princesa City, Palawan, Philippines. Schoppe, S., Alvarado, D., Luz, S. in prep. b. Home range and homing of the Palawan Pangolin Manis culionensis. Katala Foundation Inc., Puerto Princesa City, Palawan, Philippines. Schultze, W., 1914. Notes on the Malay pangolin, Manis javanica Desmarest. Philippine J. Sci. 1, 93. Steere, J.B., 1888. A month in Palawan. Am. Nat. 22 (254), 142145. Taylor, E.H., 1934. Philippine land mammals. Bur. Sci. Mongr. (Manila) 30, 1548. Ullmann, T., Verı´ssimo, D., Challender, D.W.S., 2019. Evaluating the application of scale frequency to estimate the size of pangolin scale seizures. Ecol. Conserv. 20, e00776. Wu, S.B., Liu, N.F., Ma, G.Z., Xu, Z.R., Chen, H., 2003. Studies on habitat selection by Chinese pangolin (Manis pentadactyla) in winter in Dawuling Natural Reserve. Acta Ecol. Sin. 23 (6), 10791086. [In Chinese]. Wu, S., Liu, N., Zhang, Y., Ma, G., 2004. Physical measurement and comparison for two species of pangolins. Acta Theriol. Sin. 24 (4), 361364. [In Chinese].
I. What is a Pangolin?
7 Philippine pangolin Manis culionensis (de Elera, 1915) Sabine Schoppe1,2, Lydia K.D. Katsis2, Dexter Alvarado1 and Levita Acosta-Lagrada2,3 1
Katala Foundation Inc., El Rancho, Puerto Princesa City, Philippines 2IUCN SSC Pangolin Specialist Group, N Zoological Society of London, Regent’s Park, London, United Kingdom 3Palawan Council for Sustainable Development Staff (PCSDS), Puerto Princesa City, Philippines O U T L I N E Taxonomy
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Ontogeny and reproduction
118
Description
110
Population
118
Distribution
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Status
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Habitat
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Threats
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Ecology
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References
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Behavior
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Taxonomy Previously included in the genus Pholidotus (de Elera, 1915) and subgenus Paramanis (Schlitter, 2005), the species is here included in the genus Manis based on morphological and genetic evidence (Gaubert et al., 2018; Chapter 2). Despite early classification as a distinct species (de Elera, 1915; Lawrence, 1939;
Pangolins DOI: https://doi.org/10.1016/B978-0-12-815507-3.00007-1
Sanborn, 1952), much of the subsequent literature did not distinguish this species from the Sunda pangolin (Manis javanica), or considered it to be a subspecies (Corbet and Hill, 1992; Heaney et al., 1998; Pocock, 1924; Taylor, 1934). Feiler (1998) proposed a series of morphological characteristics distinguishing the two species, but did not consider many of the observations made by Lawrence (1939).
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7. Philippine pangolin Manis culionensis
Gaubert and Antunes (2005) classified this species as distinct from the Sunda pangolin based on six discrete morphological characters. They include (1) the number of scale rows across the middle of the back (following a line perpendicular to the anteroposterior axis): 1921 in the Philippine, and 1518 in the Sunda pangolin (though see Description); (2) uniformly small scales in the nuchal, scapular, and postscapular regions in the Philippine pangolin, which are larger in the Sunda species; (3) the ratio of the nasal bone to total skull length, which is smaller in the Philippine (,1/3) and larger ( . 1/3) in the Sunda pangolin; (4) the posterior region of the palatine bone which is weaker in the Philippine pangolin, i.e., is not ventrally inflated and has short lateral walls: it is strong, ventrally inflated and has large lateral walls in the Sunda pangolin; (5) the posterior extension of the zygomatic process, which is short and not posterior to the sphenopalatine foramen in the Philippine, but long and posterior to the sphenopalatine foramen in the Sunda pangolin; and (6) the ratio of head and body to tail length, which is smaller in the Philippine (1.11 6 0.03, mean 6 SD, n 5 5) compared to the Sunda pangolin (1.25 6 0.13, n 5 20; though see Description). Feiler (1998) and Lawrence (1939) suggested 15 additional morphological features to distinguish the two species, but Gaubert and Antunes (2005) did not support their utility. Delimitation of the Philippine from the Sunda pangolin was supported by genetic analyses (see Gaubert et al., 2018). The species is monotypic. Records from archeological sites on Palawan Island date back 50007000 years (Gaubert, 2011). The split between the Philippine and Sunda pangolin is speculated to have occurred when Early Pleistocene land bridges between Borneo and Palawan were submerged by rising sea levels about 500,000800,000 years ago (Gaubert and Antunes, 2005).
Etymology: Manis (see Chapter 4); the epithet culionensis references the island of Culion in the Philippines.
Description The Philippine pangolin is a medium-sized mammal, typically weighing 47 kg, and reaches a total length of 100130 cm (Table 7.1). The species appears to be sexually dimorphic, with males larger and heavier than females (Schoppe et al., in prep. a; Table 7.1). Morphologically, the species is very similar to the Sunda pangolin. The body is covered in keratinous, overlapping scales, which grow from the skin and are rounded. Exceptions include the ventral surface, inner sides of the limbs, and parts of the head and face which are pinkish in color and covered in dense white hair (Fig. 7.1). A small number of thick hairs or bristles grow from the base of the scales. The tail is approximately 90% of head-body length (Gaubert and Antunes, 2005) and is covered in scales both dorsally and ventrally. An exception is the tail tip on the ventral side, which lacks a median scale and is replaced by a cutaneous pad. There are 1921 transversal scale rows on the body (Gaubert and Antunes, 2005), and 2832 rows of scales on the tail margins (Table 7.1). Total scales number approximately 8501000 (Table 7.1) and vary in size and shape. Scales on the dorsum are broad and rhomboid-shaped, and twice as wide as the first row of postscapular scales (Gaubert, 2011). On the limbs, scales are graduated and the hindlimbs have a central keel terminating in a sharp point: the scales on the tail margins are also sharply pointed. Like in other Asian pangolins, the medio-dorsal scale row continues to the tail tip (Jentink, 1882). Scale color varies from creamy-orange, dirty yellowish-white to dark brown (Fig. 7.1), and may be uniform or individuals may possess scales of variable color (Gaubert and Antunes, 2005), which is
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TABLE 7.1 Philippine pangolin morphometrics. Measurement Weight
Body
Vertebrae
Skull
Scales
Country
Source(s)
Weight (R)
4.9 (2.77.3) kg, n 5 9
Philippines
S. Schoppe, unpubl. data
Weight (Q)
3.2 (33.5) kg, n 5 4
Philippines
S. Schoppe, unpubl. data
Weight unsexed
3.6 (2.25.9) kg, n 5 21
Philippines
A. Ponzo and S. Schoppe, unpubl. data
Total length (R)
1067 (8401330) mm, n 5 8
Philippines
S. Schoppe, unpubl. data
Total length (Q)
961 (8281030) mm, n 5 4
Philippines
S. Schoppe, unpubl. data
Head-body length (R)
582 (450740) mm, n 5 8
Philippines
S. Schoppe, unpubl. data
Head-body length (Q)
533 (470563) mm, n 5 4
Philippines
S. Schoppe, unpubl. data
Tail length (R)
486 (3959) mm, n 5 8
Philippines
S. Schoppe, unpubl. data
Tail length (Q)
428 (358470), n 5 4
Philippines
S. Schoppe, unpubl. data
Total number of vertebrae
No data
Cervical
No data
Thoracic
No data
Lumbar
No data
Sacral
No data
Caudal
2930
Length (unsexed)
6095 mm
Breadth across zygomatic processes
No data
Total number of scales
Gaubert, 2011 Philippines
Gaubert, 2011
940 (854999), n 5 3
Philippines
Ullmann et al., 2019
No. of scale rows (transversal, body)
1921, n 5 9
Philippines
Gaubert and Antunes, 2005
No. of scale rows (longitudinal, body)
No data
No. of scales on outer margins of tail
2832, n 5 4
Philippines
L. Katsis and D. Challender unpubl. data; T. Ullmann, unpubl. data
No. of scales on median row of tail
2832, n 5 4
Philippines
L. Katsis and D. Challender unpubl. data; T. Ullmann, unpubl. data
Scales (wet) as proportion of body weight
No data
Scales (dry) as proportion of body weight
No data
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7. Philippine pangolin Manis culionensis
FIGURE 7.1 Adult female Philippine pangolin: this species is semi-arboreal. Photo credit: Dexter Alvarado.
sometimes limited to scale margins and/or the tip (e.g., darker at the tip; L. Katsis, pers. obs.). Observations indicate that juveniles may possess several white-translucent scales on the distal part of the tail, which may darken with age (D. Alvarado, pers. obs.). The head is conical in shape and largely naked, with the exception of small scales on the forehead, which extend anteriorly and terminate before the rhinarium. The face is pinkish-gray and the rhinarium is a darker pink-brown. Ear pinnae are present, but like in the Sunda pangolin comprise a subvertical ridge of integument posterior to the auditory orifice, and are less pronounced than in the Chinese pangolin (M.
pentadactyla). The eyes are small with a dark iris and surrounded by thick swollen eyelids. As with all pangolins, this species lacks teeth and has a long tongue that retracts into a pouch in the throat. The oral cavity is small. The species is pentadactylous with five digits on the fore- and hindfeet. Each digit terminates with a claw, the largest (and strongest) of which is the middle. The second and fourth claws are smaller but of approximately equal size. The first and fifth digits (and claws) are vestigial and essentially non-functional. Digit and claw length and disposition on the hindfeet approximates the forefeet. It is presumed that the species possesses a pair of anal glands in the circumanal
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Distribution
area. The genetalia are similar to the Sunda pangolin; females have two pectoral mammae. The Philippine pangolin is easily confused with the Sunda pangolin and the two species are hard to differentiate. Gaubert and Antunes (2005) posited that the species can be distinguished by a number of characteristics (see Taxonomy), including the number of transversal scale rows: 1921 in the Philippine and 1518 in the Sunda pangolin. However, other sources (Frechkop, 1931; Mohr, 1961; Wu et al., 2004; L. Katsis and D. Challender, unpubl. data) indicate that the Sunda pangolin possesses 1519 transversal scale rows i.e., there is overlap between the species. Gaubert and Antunes (2005) also assert that the ratio of head-body to tail length is a diagnostic characteristic, but the ratio of individuals measured for this chapter (1.21 6 0.06; mean 6 SD, n 5 12; see Table 7.1), more closely approximates that of the Sunda pangolin (see Gaubert and Antunes, 2005). Number of transversal scale rows (assuming they do not number 19), combined with the size of scales in the nuchal, scapular and postscapular regions (see Gaubert and Antunes, 2005) may be used to differentiate the species. The number of scales on the margins of the tail, if they number 3132, is also a diagnostic characteristic of the Philippine pangolin: the Sunda pangolin possesses up to 30 scale rows on the tail margins. These parameters are based on a small sample size (n 5 10) for the Philippine pangolin, and further research could reveal greater variation in scale number, and potentially greater overlap with the Sunda pangolin. Dependent on the purpose of differentiation between the species, DNA-based methods may be appropriate (see Luczon et al., 2016). The Philippine pangolin may also be confused with the Chinese pangolin. Distinguishing features of the former include smaller and less prominent ear pinnae, smaller and shorter claws on the forefeet, which are noticeably larger in the Chinese species, and the number of transversal scale rows and scales on the tail margins, which
number 1418 and 1420 on the Chinese species respectively (see Chapter 4), and are more numerous in the Philippine pangolin (Table 7.1).
Distribution Endemic to the Palawan faunal region in the Philippines, including Palawan Island, the Calamian Islands, and smaller surrounding islands (Fig. 7.2; Bourns and Worcester, 1894; de Elera, 1915; Everett, 1889; Heaney et al., 1998; Lawrence, 1939). Records from mainland Palawan include fossils found in the north of the island from the Terminal Pleistocene to Late Holocene (Lewis et al., 2008; Piper et al., 2011). The species occurs on Dumaran Island (Schoppe and Alvarado, 2016) and Batas Island in Taytay (Acosta and Schoppe, 2018; Schoppe et al., 2017) and Indigenous peoples indicate that the species occurs on islands off El Nido, including Lagen Island, Tagnipa, and Nagbilisong Islands in San Vicente (Acosta and Schoppe, 2018). The species has apparently been introduced to Apulit Island in El Nido, and possibly Lagen Island (S. Schoppe, unpubl. data). Within the Calamian Islands, north of mainland Palawan, the species occurs on Culion (de Elera, 1915; Heaney et al., 1998; Hollister, 1913), Busuanga (Hoogstraal, 1951), and Calauit Islands (Alviola, 1998). Interviews with local communities conducted between 2010 and 2015 confirmed the species’ presence on Busuanga, Culion, Calauit and Maglalambay (Paguntalan et al., 2010, 2012, 2015). Similarly, in interviews conducted in 2006 local people suggested that the species occurs on 12 islands dispersed across Busuanga, Calauit, and Culion, and at least nine smaller islands from the Calamian island group (Rico and Oliver, 2006). The species is apparently absent from Coron Island (Acosta and Schoppe, 2018; Rico and Oliver, 2006; Paguntalan et al., 2010, 2012, 2015) but is distributed in the municipality of Coron on Busuanga Island.
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7. Philippine pangolin Manis culionensis
FIGURE 7.2 Philippine pangolin distribution. Source: Schoppe et al., 2019.
There is uncertainty over distribution on Balabac Island, south of Palawan. Steere (1888) reported that the species was absent and there are no records in the literature. Indigenous peoples from southern Palawan also refuted the species’ occurrence on the island (Acosta and Schoppe, 2018). However, hunters in the Palawan tribe and local people from Balabac report that the species is present but in very low numbers (Schoppe and Cruz, 2008).
Habitat The Philippine pangolin primarily inhabits primary and secondary lowland forests
(Heaney et al., 1998; Hoogstraal, 1951), but uses a diverse range of habitats (Fig. 7.3). It has been recorded in lowland grassland-forest mosaics and logged-over lowland forest, in which most of the merchantable timber had been extracted (Esselstyn et al., 2004), agricultural ecosystems (Acosta-Lagrada, 2012; Schoppe and Cruz, 2009), coastal areas near beach forest and mangroves, and in riverine forest (Marler, 2016). There are records from up to 2015 m asl (Acosta-Lagrada, 2012). The species is thought to have an affinity to strangler figs (Ficus spp.) as the fruits of these trees attract ants, and the roots provide structures that pangolins can use for shelter
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Ecology
blocks of heavily modified habitats (e.g., monoculture plantations).
Ecology
FIGURE 7.3 The Philippine pangolin inhabits primary and secondary lowland forest but uses a diverse range of habitats including grassland-forest mosaics and beach forest. Photo credit: Dexter Alvarado.
(Schoppe and Cruz, 2009). The species has been found burrowing under other tree species, including bishop wood (Bischofia javanica) and Dysoxylum spp. (Acosta-Lagrada, 2012). The diverse range of habitats used suggests that the species is adaptable to habitat degradation and modification providing there is an adequate prey base (Acosta-Lagrada, 2012): this is similar to the Sunda pangolin, which persists in highly degraded forest (see Chapters 6 and 26). Acosta-Lagrada (2012) suggested that the species may occur at higher densities in primary forest but this requires further research and verification (see Chapter 34), as does the ability of the species to persist long-term in isolated
The species is semi-arboreal but there is little knowledge of its ecology, and most of what is known is based on research conducted between 2010 and 2018. The species likely lives in relatively stable home ranges. Minimum Convex Polygon (MCP) home range estimates for three males were 59, 96, and 120 ha (mean 5 61.6 ha) with core areas (where individuals spent $ 50% of the time) of 29, 45, and 68 ha respectively (mean 5 47.3 ha; Schoppe and Alvarado, 2016; Schoppe et al., 2017; in prep. b). The smallest home range estimate was for a young male that weighed 1.5 kg (and was likely recently independent see Chapter 6) at the onset of monitoring. Home ranges did not overlap, suggesting males are territorial (Schoppe et al., in prep. b). Equivalent estimates for two females based on 257 days of radio-tracking were 47 and 75 ha, with core areas of 12 and 18 ha, respectively. During the wet season (JuneNovember), home ranges of two females and a young male did not overlap, but did partially during the dry season (DecemberMay), which may be related to access to permanent water sources (Schoppe and Alvarado, 2016; Schoppe et al., in prep. b). Males traveled a mean distance of 4.2 6 0.6 km (range 35.3 km) within a 24 h period, and females, 3.1 6 0.6 km (range 04 km; Schoppe et al., 2017; in prep. b). Research using radiotelemetry on six wild-caught individuals has provided initial insights into homing behavior. Three males (including one young male; weight 5 1.5 kg) and three females were released 1.13.7 km away from sites of capture. After release, the three females and the young male established new home ranges near the release site, whereas the two adult males returned to their respective home ranges
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(Schoppe and Alvarado, 2016; Schoppe et al., 2017; in prep. b). Shelter takes the form of burrows on the forest floor, tree hollows (or in the fork of tree branches), between tree buttresses or roots, and dens under or between large rocks. AcostaLagrada (2012) suggested that dens are located in areas away from human disturbance, on slopes of 36 to .50 and 100200 m from water sources, which is similar to the Chinese pangolin (Wu et al., 2003; see Chapter 4). Observations suggest that the species prefers arboreal resting sites during the wet season and terrestrial sites during the dry season, which is potentially related to avoiding dens being flooded in the former (Schoppe et al., in prep. b). There is little knowledge of shelter use (e.g., site fidelity) but a male pangolin was observed to return to the same den for 23 consecutive nights before moving to another site, eventually returning to the previous den after about a week (S. Schoppe, unpubl. data). The Philippine pangolin is known to forage both terrestrially and in trees but there is little knowledge of prey species or foraging behavior. Acosta-Lagrada (2012) recorded consumption of two ant species, Odontomachus infandus and Diacamma sp., and one termite species, Nasutitermes sp. Schoppe and Alvarado (2015a) observed the species predating frequently on the weaver ant (Oecophylla smaragdina), a species preferred by the Sunda pangolin (Lim, 2007; see Chapter 6). Lim (2007) noted that the Sunda pangolin predated on 11 ant genera, which do occur in the Philippines (General and Alpert, 2012), and it is likely that the diet is similar to the Sunda pangolin, though only two of these genera are known to occur in Palawan, Polyrhachis and Oecophylla. Predators likely include pythons (e.g., reticulated python [Malayopython reticulatus]; Lim and Ng, 2008). Ecto-parasites include the tick Amblyomma javanense (Corpuz-Raros, 1993; Jaffar et al., 2018), and preliminary research
indicates that 86% of Philippine pangolins host this species (n 5 14; S. Schoppe, unpubl. data).
Behavior Solitary and predominantly nocturnal, the species rests during the day and is active at night (Schoppe and Alvarado, 2015a, 2016; Schoppe et al., in prep. b). Based on research using telemetry, peak activity for six study animals over an 11-day period was 23000400 (Schoppe et al., in prep. b). A young, independent male monitored for 42 days had an identical peak activity period, and was active for 12 hours a day (mean), and traveled a mean distance of 3.6 6 1.1 km (range 05 km) within a 24 hour period (Schoppe and Alvarado, 2015a, 2016; Schoppe et al., in prep. b). Preliminary research suggests that activity patterns may be influenced by the lunar phase, with individuals being active for longer periods during full moon (Schoppe and Alvarado, 2015a). Schoppe and Alvarado (2015a) note that a young male emerged from its den as early as 1200 noon during the new moon and returned by midnight, but during full moon (and between first and last quarter) emerged at dusk and returned in the early hours of the morning. In the dry season, individuals will immediately search for water after emerging from a burrow or other resting place, and drink prior to foraging; during the wet season, individuals will forage first before drinking and retreating to a resting place (Schoppe et al., in prep. b). In the dry season, an individual was observed to stand in a stream and drink for 3060 min before returning to its resting place (Schoppe et al., in prep. b). The species is quadrupedal. When walking the head and tail are held below the level of the body, and the forelimbs face inward with the claws perpendicular to the ground, and the weight is taken on the knuckles and outer margins of the claws (i.e., folded up wrists). Semi-
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FIGURE 7.4 Philippine pangolins are adept climbers and use their strong tail for support. Photo credit: Dexter Alvarado.
arboreal, the species is an adept climber, using its long tail as an extra limb (Fig. 7.4). Like the Sunda pangolin, the species moves its limbs in pairs when climbing tree trunks, the incredibly strong tail providing grip and bearing weight, and the species will descend trees head first (Fig. 7.4). The Philippine pangolin predates on ants and termites, both in trees and on the ground, and locates prey using its acute olfactory senses (Acosta-Lagrada, 2012; Schoppe and Alvarado, 2015a; Schultze, 1914). Having located an ant nest or termitaria the strong forelimbs are used to break into these structures and the long tongue is used to extract ants or termites of all life stages (e.g., eggs, adults). The nests are not destroyed, enabling insect colonies to recover, but feeding sites
are returned to during consecutive nights (Schoppe et al., in prep. b). In addition to searching for ant nests and termitaria, the species will search for prey among leaf litter and rotten wood on the forest floor. Schultze (1914) suggested that the Philippine pangolin may have a higher reliance on arboreal termite nests in the dry season, and terrestrial termite nests in the wet season, as terrestrial nests may be difficult to penetrate during the dry season; however, this requires verification. The species is sensitive to human presence and typically responds by fleeing (Schoppe et al., in prep. b). Otherwise, when sensing a threat, Philippine pangolins will flee if the threat is distant, or roll up into a ball if it is in close proximity (Fig. 7.5).
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likely strong similarities with the Sunda pangolin. Adult sex ratios at six sites in Palawan ranged from 1:0.6 to 1:1, with an average of 1:0.8 in favor of males (Schoppe et al., in prep. a).
Population
FIGURE 7.5 A male Philippine pangolin assessing whether it is safe to uncurl: like all pangolins, this species curls up into a ball when threatened. Photo credit: Sabine Schoppe.
Vocalizations are limited to a “hissing” sound when individuals are threatened (Schultze, 1914; Schoppe et al., in prep. a).
Ontogeny and reproduction Much of what is known is based on anecdotal evidence or presumed similarities with the Sunda pangolin (see Chapter 6). The Indigenous people of the Tagbanua, Batak and Palawan tribes report that the species has one offspring, but two fetuses have occasionally been encountered when the animals have been slaughtered (Acosta and Schoppe, 2018). It is presumed that breeding is aseasonal like the Sunda pangolin (Schoppe et al., in prep. a). However, local farmers in the species’ range have reported that females with young are typically seen in August (Schoppe and Cruz, 2009). In a telemetry study, a pregnant female was caught in September and observed with the young in November (Schoppe and Alvarado, 2016). There is little knowledge of estrus cycles, gestation, young development and maternal care, weaning, age at sexual maturity or population structure, which requires research, but there are
There is limited knowledge of, and quantitative data on, Philippine pangolin populations. Schoppe et al. (in prep. a) estimated density at six sites representing northeastern islands, central Palawan, and southern Palawan, using systematic searches of direct signs, primarily with dogs. Across these sites, estimated mean adult density was 2.5 6 1.4 adults/km2 (mean 6 SD). Population density was highest (3.5 and 4.0 adults/km2) on the islands in northeastern Palawan, which is potentially due to the remoteness of the islands and their protected status (Schoppe et al., in prep. a). Three central Palawan (Puerto Princesa City) sites had a mean adult density of 1.8 6 1.61 adult/km2 (Schoppe et al., in prep. a) and included one site where the species was not recorded (Schoppe and Alvarado, 2015b); mean density in Rizal in southern Palawan was 2 adults/km2. Other evidence indicates that the species is not evenly distributed across its range, is increasingly rare, and declining (Bayron, 2014; Schoppe et al., 2017; in prep. a). Indigenous peoples report the species was common in the late 1960s when human population density was lower and forest cover much higher (Acosta and Schoppe, 2018). Pangolins were frequently seen in the 1970s1980s, particularly in coastal and lowland areas, including in Aborlan (J. Fabello, pers. comm.). Rabor (1965) and Heaney et al. (1998) noted that the species was rare. Interview-based research indicates population declines. Multiple Indigenous peoples groups from the Tagbanua, Batak and Palaw’an Tribes, and Cuyunon communities from Palawan and the Calamian Islands
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Threats
estimated population declines of 85% in the south of the species’ range and 95% in the north between 1980 and 2018 (Acosta and Schoppe, 2018). Interviews with hunters and traders indicate the species is rare in southern Palawan and more common in the north (Schoppe and Cruz, 2009), while ethno-biological surveys and similar research suggests the species is increasingly rare and that sightings are uncommon (Acosta-Lagrada, 2012; Rico and Oliver, 2006). Local hunters report a decline in the number of pangolins caught per unit effort compared to the 1970s (Schoppe, 2013). One hunter in Brooke’s Point, southern Palawan, reported that in 1992 it was possible to catch 34 pangolins a week, but in 2012, similar effort resulted in only one pangolin a month (Acosta-Lagrada, 2012). Bayron (2014) reported similar results in Roxas, Puerto Princesa City and Quezon.
Status The Philippine pangolin is listed as Critically Endangered on The IUCN Red List of Threatened Species (Schoppe et al., 2019) and available evidence indicates declines across its range (see Population). However, there is a lack of quantitative data on populations. The species is listed as Critically Endangered in Palawan Province and Endangered at the national level in the Philippines. It is afforded protection under the Philippine Wildlife Act 9147, which prohibits the exploitation of threatened species, including by indigenous peoples for traditional use. The entirety of Palawan Province was declared a game refuge and bird sanctuary in 1969 and the species occurs in a number of protected areas, including the Mount Mantalingahan Protected Landscape and Puerto Princesa Underground River National Park. The species is included in CITES Appendix I.
Threats The principle threat to the Philippine pangolin is overexploitation. This includes local use and consumption and international trafficking and use of the species and its body parts, and is compounded by the species’ restricted geographic range. Habitat loss poses an additional, indirect threat. Pangolins have been hunted on Palawan for at least 6000 years (Lewis et al., 2008) and Indigenous peoples have traditionally used, and continue to use the species for subsistence, medicinal, and ritualistic purposes. This includes the consumption of meat as a protein source, often with perceived health benefits including the treatment of gastrointestinal diseases, inflammation, asthma, and flatulence (Eder, 1987; Esselstyn et al., 2004; Estrada et al., 2015). The scales are used (in powered form) to treat asthma (Esselstyn et al., 2004) and prostate-related illnesses (Acosta-Lagrada, 2012), while the Palaw’an in Bataraza use the scales on belts to treat back pain, and multiple Indigenous communities use them to deter bad spirits (see Chapter 12; Acosta and Schoppe, 2018; Bayron, 2014; Estrada et al., 2015). In Narra, burnt scales are used to treat mothers who have just given birth, and to stop thunder (Acosta-Lagrada, 2012; Acosta and Schoppe, 2018). At Brooke’s Point, Indigenous peoples will drink the blood for its believed rejuvenation properties (Acosta-Lagrada, 2012). The species is poached for trade in its blood, meat, skin and scales within the Philippines (Cruz et al., 2007; Esselstyn et al., 2004). Bayron (2014) reported that poaching levels were particularly high in northern Palawan, and estimated that 448 pangolins were poached in three municipalities (Puerto Princesa City, Roxas and Quezon) in Palawan in 2012 alone. Poaching takes place by local people, but also by individuals from neighboring areas (barangays),
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including with the use of dogs (Acosta and Schoppe, 2018; Bayron, 2014). It takes place to meet consumer demand in major cities, and analysis of seizure data suggests there is substantial domestic demand for pangolin meat and scales in cities including Metro Manila (Gomez and Sy, 2018). Indications from trade research and insights from indigenous peoples are that exploitation for domestic and international trade is the main, contemporary driver of pangolin offtake, as opposed to local use (Lacerna and Widmann, 2008; Schoppe and Cruz, 2009). The CITES trade data indicate that approximately 10,000 pangolins, in the form of skins, that were traded internationally in the 1980s, originated in or were exported from the Philippines. Despite a decline in international trade in pangolin skins post-2000 (see Chapter 16), international trade has otherwise continued, albeit illegally. Gomez and Sy (2018) report that during 20012017 at least 39 seizures took place in which the Philippines was implicated as a source country or place of seizure. This included an estimated 667 Philippine pangolins, primarily comprising quantities of meat and scales, and dead individuals, though actual illegal trade volumes were likely higher. Most of these seizures took place in Palawan, but seizures were also made on Luzon, Mindoro, Negros and Tablas (Gomez and Sy, 2018). Exact trafficking routes are not well documented but the species is illegally traded to East Malaysia (e.g., Kudat, Sandakan) and Peninsular Malaysia for subsequent export to China, including for use in traditional medicines (Pantel and Anak, 2010; Schoppe and Cruz, 2009). However, it is suspected that Philippine pangolin scales may be exported and then subsequently imported after processing into Traditional Chinese Medicine (TCM) for domestic consumption (E. Sy, pers. comm.). The Philippines has further been implicated in highly organized international pangolin trafficking (see Luczon et al., 2016). There remains a strong financial incentive for local people and indigenous peoples to poach
and sell pangolins into illegal trade, which is apparently exacerbated by issues over their legitimate access to, and use of, non-timber forest products for livelihood purposes. This is compounded by law enforcement being a low priority for enforcement and judicial agencies in the Philippines, combined with a lack of human and technical resources, resulting in little deterrent to would-be poachers and traffickers, and the perception that illegal trade in pangolins is low risk. Habitat loss poses an indirect threat. It results in the opening up of previously inaccessible areas through the creation of road networks for commercial concessions, which in turn makes pangolins susceptible to hunting and poaching: it also increases the likelihood of roadkill. As with the Sunda pangolin, there is a need for research into how the Philippine pangolin uses natural and modified habitats (e.g., monoculture plantations) and the ability of the species to persist in highly modified isolated habitat blocks in the long-term.
References Acosta-Lagrada, L.S., 2012. Population density, distribution and habitat preferences of the Palawan Pangolin, Manis culionensis (de Elera, 1915). M.Sc. Thesis, University of the Philippines Los Ban˜os, Laguna, Philippines. Acosta, D., Schoppe, S., 2018. Proceedings of the Stakeholder Workshop on the Palawan Pangolin Balintong, Bulwagang Princesa Tourist Inn, Puerto Princesa City, 17 February 2018, Katala Foundation Inc, Puerto Princesa City, Palawan, Philippines, pp. 110. Alviola, P.L. III, 1998. Land vertebrates of Calauit Island, Palawan, Philippines. Asia Life Sci. 7 (2), 157170. Bayron, A.C., 2014. Trade dynamics of Palawan pangolin Manis culionensis. B.Sc. Thesis, Western Philippines University, Palawan, Philippines. Bourns, F.S., Worcester, D.C., 1894. Preliminary Notes on the Birds and Mammals Collected by the Menage Scientific Expedition to the Philippine Islands. Minnesota Academy of Sciences, Minneapolis. Corbet, G.B., Hill, J.E., 1992. The Mammals of the Indomalayan Region: A Systematic Review. Oxford University Press, Oxford.
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TRAFFIC Southeast Asia, Petaling Jaya, Selangor, Malaysia, pp. 176188. Schoppe, S., Alvarado, D., 2015a. Conservation Needs of the Palawan Pangolin Manis culionensis Phase II (Extension), Final Scientific and Financial Report Submitted to Wildlife Reserves Singapore. Katala Foundation Inc, Puerto Princesa City, Palawan, Philippines, pp. 136. Schoppe, S., Alvarado, D., 2015b. Conservation Needs of the Palawan Pangolin Manis culionensis Phase I. Final Scientific and Financial Report to Wildlife Reserves Singapore. Katala Foundation Inc, Puerto Princesa City, Palawan, Philippines, pp. 130. Schoppe, S., Alvarado, D., 2016. Movements of the Palawan Pangolin Manis culionensis Final Project Report Submitted to Wildlife Reserves Singapore. Katala Foundation Inc, Puerto Princesa City, Palawan, Philippines, pp. 116. Schoppe, S., Alvarado, D., Luz, S., 2017. Movement patterns of the Palawan Pangolin Manis culionensis. Poster presentation at 26th Philippine Biodiversity Symposium, 1821 July 2017, Ateneo de Manila University, Quezon City, Philippines. Schoppe, S., Katsis, L., Lagrada, L., 2019. Manis culionensis. The IUCN Red List of Threatened Species 2019: e.T136497A 123586862. Available from: , http://dx.doi.org/10.2305/ IUCN.UK.2019-3.RLTS.T136497A123586862.en . . Schoppe, S., Alvarado, D., Luz, S., in prep. a. First data on the population density of the Palawan Pangolin Manis culionensis from Palawan, Philippines. Katala Foundation Inc., Puerto Princesa City, Palawan, Philippines. Schoppe, S., Alvarado, D., Luz, S. in prep. b. Home range and homing of the Palawan Pangolin Manis culionensis. Katala Foundation Inc., Puerto Princesa City, Palawan, Philippines. Schultze, W., 1914. Notes on the Malay pangolin, Manis javanica Desmarest. Philippine J. Sci. 1, 93. Steere, J.B., 1888. A month in Palawan. Am. Nat. 22 (254), 142145. Taylor, E.H., 1934. Philippine land mammals. Bur. Sci. Mongr. (Manila) 30, 1548. Ullmann, T., Verı´ssimo, D., Challender, D.W.S., 2019. Evaluating the application of scale frequency to estimate the size of pangolin scale seizures. Ecol. Conserv. 20, e00776. Wu, S.B., Liu, N.F., Ma, G.Z., Xu, Z.R., Chen, H., 2003. Studies on habitat selection by Chinese pangolin (Manis pentadactyla) in winter in Dawuling Natural Reserve. Acta Ecol. Sin. 23 (6), 10791086. [In Chinese]. Wu, S., Liu, N., Zhang, Y., Ma, G., 2004. Physical measurement and comparison for two species of pangolins. Acta Theriol. Sin. 24 (4), 361364. [In Chinese].
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