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Black-bellied pangolin Phataginus tetradactyla (Linnaeus, 1766)
C H A P T E R
8 Black-bellied pangolin Phataginus tetradactyla (Linnaeus, 1766) Maja Gudehus1, Darren W. Pietersen2,3, Michael Hoffmann4, Rod Cassidy1, Tamar Cassidy1, Olufemi Sodeinde5, Juan Lapuente6, Brou Guy-Mathieu Assovi7 and Matthew H. Shirley8 1
Sangha Pangolin Project, Dzanga-Sangha, Central African Republic 2Mammal Research Institute, Department of Zoology and Entomology, University of Pretoria, Hatfield, South Africa 3IUCN SSC Pangolin Specialist Group, N Zoological Society of London, Regent’s Park, London, United Kingdom 4 Conservation and Policy, Zoological Society of London, Regent’s Park, London, United Kingdom 5 Department of Biological Sciences, New York City College of Technology, City University of New York, Brooklyn, NY, United States 6Comoe´ Chimpanzee Conservation Project, Comoe´ Research Station, Coˆte d’Ivoire & Animal Ecology and Tropical Biology, Biozentrum, Universita¨t Wu¨rzburg Tiero¨kologie und Tropenbiologie (Zoologie III), Wu¨rzburg, Germany 7Universite´ Felix Houphoue¨tBoigny, Abidjan, Coˆte d’Ivoire 8Tropical Conservation Institute, Florida International University, North Miami, FL, United States 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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Pangolins DOI: https://doi.org/10.1016/B978-0-12-815507-3.00008-3
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© 2020 Elsevier Inc. All rights reserved.
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8. Black-bellied pangolin Phataginus tetradactyla
Taxonomy Previously included in the genus Manis (Meester, 1972; Schlitter, 2005) and Uromanis (Kingdon, 1997; McKenna and Bell, 1997; Pocock, 1924), the species is here included in Phataginus based on both morphological (Gaudin et al., 2009) and genetic (du Toit et al., 2017; Gaubert et al., 2018; Hassanin et al., 2015) evidence, in agreement with previous authors (Grubb et al., 1998; Kingdon and Hoffmann, 2013). Based on mitogenomic distances between the genera Manis, Smutsia, and Phataginus, and morphological traits unique to Phataginus, P. tetradactyla is included in the subfamily Phatagininae to designate small African pangolin species (Gaubert et al., 2018; see Chapter 2). In much of the early literature, the species name longicaudatus is used, but this name is unavailable (Mohr, 1961). The type locality is “American Australia” (West Africa; Linnaeus, 1766). No subspecies are recognized. There are no data on chromosome number. Synonyms: Pholidotus longicaudatus (Brisson, 1756; unavailable), Pholidotus longicaudatus (Brisson, 1762; unavailable), Manis tetradactylus (Linnaeus, 1766), Manis macroura (Erxleben, 1777), Phataginus ceonyx (Rafinesque, 1820), Manis africana (Desmarest, 1822), Manis tetradactyla (Gray, 1843), Manis guineensis (Fitzinger, 1872), Manis longicauda (Sundevall, 1842), Manis longicaudata (Sundevall, 1842, sic., fide Pocock, 1924), Manis senegalensis (Fitzinger, 1872), Manis hessi (Noack, 1889), Pholidotus tetradactyla (Sclater, 1901), Uromanis longicaudata (Pocock, 1924), and Manis longicaudatus (Rosevear, 1953). Etymology: Phataginus is derived from “phatagen”, an East Indian name for the pangolin; the species name tetradactyla references the four (tetra-) non-vestigial digits (-dactyla) on the feet (Gotch, 1979).
Description The black-bellied pangolin (Phataginus tetradactyla), is a small, arboreal African pangolin
with a body weight of 1.1 3.6 kg and a total body length of up to 120 cm (Table 8.1). The common name stems from the black skin and hairs that cover most of the ventrum, face, inner sides of the limbs and upper forelimbs and forefeet (Hatt, 1934; Jentink, 1882). The extremely long prehensile tail makes up to twothirds of the total body length (55 75 cm; see Table 8.1; Hatt, 1934; Tahiri-Zagre¨t, 1970a). It has a bare, sensitive skin pad on the ventral tip, which is truncated, and the tail easily supports the weight of the animal (Jentink, 1882; Kingdon, 1971; Pocock, 1924). There are 47 caudal vertebrae (Jentink, 1882), a record among extant mammals. Head-body length ranges between 28 and 50 cm (Table 8.1). The species is covered with large, overlapping scales that are dark brown at the base, with yellow or golden edges, and grow from the skin in a grid-like arrangement (Fig. 8.1). Each scale has slight longitudinal striations (Dorst and Dandelot, 1970; Happold, 1987), and are “harder” (i.e., thicker and more robust) than those of the white-bellied pangolin (P. tricuspis) and other similar sized species of pangolin (Tahiri-Zagre¨t, 1970a; M. Shirley and G.-B.M. Assovi, pers. obs.). The scales cover the surface of the body dorsally and laterally but are absent from parts of the face, the throat, ventrum, inner fore- and hindlimbs, and upper portions of the forelimbs (Jentink, 1882; Kingdon, 1971; Pocock, 1924). Scales on the flanks are keeled (Fig. 8.1; Hatt, 1934). No hairs project between the scales. There are 10 13 transversal, and 13 longitudinal scale rows on the body (Table 8.1), the largest of which are on the mid-dorsum and measure up to 67 3 50 mm (O. Sodeinde, unpubl. data). The lower sections of the forelimbs are protected by pairs of very large postscapular scales (Fig. 8.1; Hatt, 1934). The scales on the forehead, fore- and hindlimbs, and median ventral tail row are the smallest. The elongated tail has 42 47 sharply-pointed scales along its edges (Table 8.1). There are 35 41 scales on the median dorsal scale row of the tail
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Description
TABLE 8.1 Black-bellied pangolin morphometrics. Measurement Weight
Country
Source(s)
2.83 (2.2 3.6) kg, n 5 4
Southeast Nigeria
Kingdon and Hoffmann, 2013
1.41 (1.12 1.65) kg, n 5 12
Central African Republic
R. and T. Cassidy, unpubl. data
2.74 (2.6 3.1) kg, n 5 3
Southeast Nigeria
Kingdon and Hoffmann, 2013
1.45 (1.3 1.7) kg, n 5 4
Central African Republic
R. and T. Cassidy, unpubl. data
874 (810 937) mm, n 5 3
Democratic Republic of the Congo
Hatt, 1934
985 (920 1070) mm, n 5 11
Central African Republic
R. and T. Cassidy, unpubl. data
1007 (820 1210) mm, n 5 7
Coˆte d’Ivoire
Tahiri-Zagre¨t, 1970a
851.4 (755 930) mm, n 5 5
Democratic Republic of the Congo
Hatt, 1934
1040 (970 1110) mm, n 5 4
Central African Republic
R. and T. Cassidy, unpubl. data
1015 (930 1100) mm, n 5 2
Coˆte d’Ivoire
Tahiri-Zagre¨t, 1970a
Total length (unsexed)
1115 (1060 1170) mm, n 5 2
Coˆte d’Ivoire
Tahiri-Zagre¨t, 1970a
Head-body length (R)
314 (286 342) mm, n 5 4
Southeast Nigeria
Kingdon and Hoffmann, 2013
398 (370 460) mm, n 5 10
Central African Republic
R. and T. Cassidy, unpubl. data
Head-body length (Q)
302 (292 311) mm, n 5 3
Southeast Nigeria
Kingdon and Hoffmann, 2013
420 (370 500) mm, n 5 4
Central African Republic
R. and T. Cassidy, unpubl. data
Tail length (R)
613.3 (560 645) mm, n 5 3
Democratic Republic of the Congo
Hatt, 1934
641 (594 707) mm, n 5 4
Southeast Nigeria
Kingdon and Hoffmann, 2013
658 (520 690) mm, n 5 10
Central African Republic
R. and T. Cassidy, unpubl. data
643 (600 710) mm, n 5 7
Coˆte d’Ivoire
Tahiri-Zagre¨t, 1970a
560.6 (505 623) mm, n 5 5
Democratic Republic of the Congo
Hatt, 1934
633 (606 670) mm, n 5 3
Southeast Nigeria
Kingdon and Hoffmann, 2013
620 (600 670) mm, n 5 4
Central African Republic
R. and T. Cassidy, unpubl. data
Tail length (unsexed)
705 (660 750) mm, n 5 2
Coˆte d’Ivoire
Tahiri-Zagre¨t, 1970a
Total number of vertebrae
.70
Liberia
Frechkop, 1931; Jentink, 1882
Cervical
7
Liberia
Jentink, 1882
Thoracic
13
Liberia
Jentink, 1882; Mohr, 1961
Weight (R)
Weight (Q)
Body
Total length (R)
Total length (Q)
Tail length (Q)
Vertebrae
(Continued)
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TABLE 8.1 (Continued) Measurement
Skull
Scales
Country
Source(s)
Lumbar
5 6
Liberia
Jentink, 1882; Mohr, 1961
Sacral
2 3
Liberia
Jentink, 1882; Mohr, 1961
Caudal
46 47
Liberia
Frechkop, 1931; Jentink, 1882; Mohr, 1961
Length (R)
70 (69.1 71) mm, n 5 2
Democratic Republic of the Congo
Hatt, 1934
Length (Q)
65.3 (62.1 68.7) mm, n 5 7
Democratic Republic of the Congo
Hatt, 1934
Breadth across zygomatic processes (R)
24 (23.6 24.4) mm, n 5 2
Democratic Republic of the Congo
Hatt, 1934
Breadth across zygomatic processes (Q)
24.5 (22.8 26.9) mm, n 5 7
Democratic Republic of the Congo
Hatt, 1934
Total number of scales
588 (542 637), n 5 10
Cameroon, unknown
Ullmann et al., 2019
No. of scale rows (transversal, body)
10 13
Frechkop, 1931; Mohr, 1961
No. of scale rows (longitudinal, body)
13
Frechkop, 1931; Jentink, 1882
No. of scales on outer margins of tail
42 47
Frechkop, 1931; Jentink, 1882; Mohr, 1961
No. of scales on median row of tail
35 41
Frechkop, 1931; Jentink, 1882
Scales (wet) as proportion of body weight
No data
Scales (dry) as proportion of body weight
No data
which is replaced by two rows of 9 10 scales towards the tail tip (Fig. 8.2; Frechkop, 1931; Jentink, 1882). The total number of scales is 542 637 (Table 8.1). Scales may lack pigmentation, seemingly sporadically, but usually on the tail or flanks (Fig. 8.2; Hatt, 1934). In older
animals, scales (e.g., on the ventral tail surface) may be worn to the point of having no free edge (Hatt, 1934). Observations of aged individuals in the wild with missing tail scales suggests that the species may permanently lose scales as they age (M. Shirley and B.G.-M. Assovi, pers. obs.).
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Description
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FIGURE 8.1 Black-bellied pangolin in Central African Republic. Visible are the large post-scapular scales on the lower forelimbs, and the keeled scales on the left flank and hindlimb. Photo credit: Alex Ley.
Like other pangolins, the skull demonstrates features associated with a myrmecophagous diet (see Chapter 1). Like the white-bellied pangolin, but unlike other pangolins, the lacrimal bone is present (Emry, 1970). The head is long, slender and naked except for scales on the forehead and coarse black hair (5 10 mm) on the cheeks and throat (Gaubert, 2011; Kingdon and Hoffmann, 2013). The snout is naked and nostrils moist and slightly downturned, and similar in color to the face (Kingdon and Hoffmann, 2013). The eyes are large and beady with dark irises, and are protected by thick, swollen eyelids. The blackbellied pangolin has ear pinnae that are greatly reduced in size and comprise fleshly ridges which border the auditory orifices (Kingdon and Hoffmann, 2013). Like other pangolins, the species is edentate (i.e., lacks teeth).
The tongue is 16 18 cm in length and at the distal end is flattened but has an oval crosssection (Gaubert, 2011). The tongue extends anteriorly from the xiphisternum, a bifurcated, cartilaginous structure formed from the last pair of ribs, which is its point of attachment in the abdomen (Doran and Allbrook, 1973; Sikes, 1966). From the posterior border of the ribs the tongue extends along the ventral surface of the body to the right iliac fossa, and from there proceeds dorsally and then anteriorly, ending in a spatulate cartilaginous structure at the dorsal border of the diaphragm (see Chapter 1; Heath, 2013). The tissues in the thorax form a glossal tube in which the tongue is housed, and which proceeds through the neck to the oral cavity (Doran and Allbrook, 1973). The fore- and hindfeet have five digits with strong, curved claws that are specialized for
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8. Black-bellied pangolin Phataginus tetradactyla
FIGURE 8.2 Black-bellied pangolin climbing a tree in Central African Republic. This figure shows the extremely long tail in this species, the termination of the mediodorsal scale row near the distal end of the tail, and several scales that lack pigmentation. Photo credit: Maja Gudehus.
breaking into ant nests. On the forefeet the first digit is vestigial—and essentially functionless —giving the appearance of only four digits, while the fifth digit is nearly as long as the fourth and better developed than in other pangolin species (Pocock, 1924). The third digit and claw is the largest and strongest. The hindfeet are elongated, resembling the forefeet to an extent, with four long, well-developed claws of approximately equal length; the innermost claw is vestigial (Pocock, 1924). Both fore- and hindfeet have well developed skin pads, which in the hindfeet extend from the level of the first digit to the heel (Pocock, 1924).
A pair of anal glands are situated on the lateral borders of the anus and produce a strong, musky scent that may be used in scent-marking, and perhaps in defense when threatened, but this has not been observed (Pocock, 1924). Pangolin hunters in Coˆte d’Ivoire claim to be able to detect black-bellied pangolins via this scent (M. Shirley and B.G.-M. Assovi, unpubl. data). The female’s vulva is situated just anterior to the anus; they have two pectoral nipples. In males, the testes are situated in the inguinal area and do not descend into a scrotum (see Chapter 1). Body temperature is regulated at 30 36 C; average resting metabolic rate has been estimated at 160.2 ml O2/kg/h (Hildwein, 1974). Despite significant differences in appearance, black-bellied pangolins are often confused with the sympatric white-bellied pangolin. They can most easily be distinguished by skin color and scale size and coloration. Scales are proportionally larger on the black-bellied pangolin and dark brown with yellow-golden edging as opposed to gray- or yellowish-brown on the white-bellied pangolin, and the scales may be noticeably longer than they are wide on the latter. The blackbellied pangolin has two very large postscapular scales (Fig. 8.1), which are not enlarged and are inferior in the white-bellied pangolin. The black-bellied pangolin is distinguished from the two terrestrial African pangolins by its smaller size, extremely long tail, skin color, and scale coloration.
Distribution The black-bellied pangolin is distributed throughout the forested regions of West and Central Africa, from Sierra Leone to the eastern limits of the Congo Basin (Fig. 8.3). Grubb et al. (1998) refuted records of the species from west of Sierra Leone, including from Senegal, The Gambia, and Guinea-Bissau (e.g., Frade, 1949; Meester, 1972; Schlitter, 2005), and suggested the most westerly confirmed record is
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FIGURE 8.3 Black-bellied pangolin distribution. Source: Ingram et al., 2019a.
from the Western Area Peninsula Forest National Park in Sierra Leone. Reiner and Simo˜es (1999) considered their presence in Guinea-Bissau possible, but there is no confirmatory evidence. There are confirmed records from a number of forest reserves in southeastern Guinea (Barnett and Prangley, 1997; Barrie and Kante´, 2006), Liberia (Allen and Coolidge, 1930), southern Coˆte d’Ivoire (Rahm, 1956), and southwestern Ghana, west of the Volta (Grubb et al., 1998). The species was recorded in Comoe´ National Park in northern Coˆte d’Ivoire for the first time in 2016 (J. Lapuente and K.E. Linsenmair, unpubl. data) and there are reports of the species occurring at other sites in
northern Coˆte d’Ivoire. If accurate, it is reasonable to assume the species may also occur in northern Ghana. There is then an apparent gap in distribution until southwestern Nigeria (Angelici et al., 2001; Happold, 1987), from where the species ranges eastward through southern Cameroon (Jeannin, 1936) and southwestern Central African Republic to eastern Democratic Republic of the Congo (DRC; Hatt, 1934; Rahm, 1966; Schouteden, 1944), the easternmost limit of their distribution. Blench and Dendo (2007) report that in Nigeria the black-bellied pangolin is more common in the southeast than in the southwest. Southwards the species ranges through Gabon and Republic
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of Congo (Malbrant and MacLatchy, 1949). Further investigation is warranted in the Semuliki Valley of Uganda, a well-known refuge of Congolese fauna and flora in East Africa where both the giant (Smutsia gigantea) and white-bellied pangolin occur. The presence of the species in Angola is unclear, and deserves some brief discussion. There is no mention of the species in several major reference works (Beja et al., 2019; Bocage, 1889, 1890; Hill and Carter, 1941; Machado, 1969; Thomas, 1904). Monard (1935) notes that they should occur south to the Kunene but provides no material basis for this statement. Mohr (1961) noted they occur to Moc¸amedes, but again the basis for this is unclear. Feiler (1990) includes them in his checklist, noting that they were first recorded prior to 1990, but without reference to a specimen or a locality. There are records of the species from the Bas-Congo province of Republic of Congo (Schouteden, 1944), and hence there seems no reason that the species should not occur at least in Cabinda (Kingdon and Hoffmann, 2013; Taylor et al., 2018).
Habitat Specific studies documenting habitat use by the black-bellied pangolin are limited. The species is the most arboreal of the African pangolins and is often found in riparian and swamp forests, typically in habitats dominated by palms (including rattans) and specialized swamp trees, such as Uapaca sp., Pseudospondis sp., and Mitragina sp. (Happold, 1987; Kingdon and Hoffmann, 2013; Page`s, 1970), as well as in primary forests and forest-savanna mosaic. Records in the catalogues of the American Museum of Natural History and the Smithsonian National Museum of Natural History indicate that most individuals in these collections were caught in primary forests. This is also the case in Central African Republic and
northern Coˆte d’Ivoire, where the black-bellied pangolin has most frequently been found in primary, closed canopy forest, away from swamp and riverine forests (R. and T. Cassidy, unpubl. data; J. Lapuente and K.E. Linsenmair, pers. obs.). In the forest-savanna mosaic of Coˆte d’Ivoire’s Comoe´ National Park, the species inhabits forests dominated by Annogeissus leiocarpus, Dialium guineense, Diospyros abissinica, and Drypetes floribunda which are far from rivers and lack palms (J. Lapuente and K.E. Linsenmair, pers. obs.). In contrast, in southern Coˆte d’Ivoire, the species is found in flooded swamp forests dominated by palms, Raphia hookeri and Hallea ledermanii, such as in the Forets des Marais de Tanoe-Ehy and the Reserve Communautaire de Dodo, and in neighboring oil palm and rubber plantations (Fig. 8.4). In these habitats, the black-bellied pangolin can also often be found foraging in the shrubby vegetation at the riverside, not more than a meter above the water (M. Shirley and B.G.-M. Assovi, pers. obs.). In southeastern Nigeria, the species has been recorded in primary and secondary rainforests, in regenerating forests, swamp forests, and farmlands (Angelici et al., 1999, 2001; Luiselli et al., 2015). Hunters and forest workers in southwestern Nigeria report harvesting pangolins, including the blackbellied pangolin on occasion, in abandoned or infrequently harvested oil palm plantations in secondary forests (Sodeinde and Adedipe, 1994). In all forest types, the black-bellied pangolin appears to predominantly use the crown strata more than others, which perhaps contributes to the lack of observations. Preliminary observations suggest that the species is more abundant in less disturbed habitats and those less frequented by people (M. Shirley and B.G.-M. Assovi, pers. obs.). Further research is needed to understand habitat requirements and selection, and their potential influence on the distribution of this species.
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FIGURE 8.4 Adult female black-bellied pangolin in the flooded swamp forests of southeastern Coˆte d’Ivoire. Photo credit: Matthew H. Shirley.
Ecology The black-bellied pangolin is predominantly diurnal, though does demonstrate some nocturnal activity (Booth, 1960; Carpaneto and Germi, 1989; Page`s, 1970; R. and T. Cassidy, unpubl. data). Records of two black-bellied pangolins monitored daily over a period of two years, and post-release observations of eight individuals confiscated from illegal trade in Central African Republic, support the assertion that the species is all but strictly diurnal (R. and T. Cassidy, pers. obs.). Only two efforts have been made to estimate the home range size of the species, one using over two years of near daily follow data for two rehabilitated and released individuals (9 12 months of age) in Central African
Republic (R. and T. Cassidy, unpubl. data), and a nascent study of six radio-tagged individuals tracked for two months in Coˆte d’Ivoire. In Central African Republic the home ranges were very small, comprising 48 and 12 ha (95% and 50% Kernel Use Density [KUD], respectively), and ranged from 36.3 to 56.2 ha (95% KUD) and 7.2 15.01 ha (50% KUD) from the first to second year respectively. In addition to little variation in annual home range, there was little apparent shift in the area of forest used, the individuals ranging over an area of 32.4 ha (95% Minimum Convex Polygon [MCP], roughly 1.2 3 0.5 linear km). In Coˆte d’Ivoire, preliminary individual home ranges for six individuals (comprising both sexes) averaged 9.27 ha (95% MCP), ranging from 0.13 to 25.9 ha (M. Shirley and B.G.-M. Assovi,
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unpubl. data). Within home ranges, individuals appear to use fixed routes and refuge holes on a continuous basis (Page`s, 1970). The species sleeps curled-up in tree hollows, tree ferns, or in tangles of lianas, and occasionally in hollowed-out insect nests. Like all pangolins, the species is myrmecophagous. However, unlike other species, the black-bellied pangolin appears to persist on a diet of tree ants (Fig. 8.5) and does not seem to prey on termites extensively, or even at all (Kingdon and Hoffmann, 2013; R. and T. Cassidy, pers. obs.; M. Shirley and B.G.-M. Assovi, pers. obs.). Crematogaster spp. and Cataulacus spp. have been reported as preferred species (Kingdon and Hoffmann, 2013), while observations in Central African Republic indicate that the species’ diet consists of at least seven different ant species, including Cataulacus guineensis, Oecophylla longinoda and Polyrhachis spp., including their eggs, larval and pupal stages (M. Gudehus, unpubl. data). Sweat bees (Halictidae) are also occasionally taken (R. and T. Cassidy, pers. obs.). The frequency of feeding bouts and proportion of time spent feeding has only been recorded for a period of two weeks, but observations suggest that the black-bellied pangolin spends most of its time resting or foraging for prey (R. and T. Cassidy, pers. obs.).
FIGURE 8.5 Black-bellied pangolin breaking into an arboreal ant nest. This species appears to predate almost exclusively on ants. Photo credit: Michael Lorentz.
The thermal ecology of pangolins in general is not well known, including body temperature and its impact on ecology. Preliminary insights from research in Coˆte d’Ivoire appear to refute the suggestion that the black-bellied pangolin spends time basking at the forest crown for thermoregulatory, or potentially, other reasons. Temperature and light data loggers attached to black-bellied pangolins in 2018 indicated that the tagged animals were exposed to an average of 110 170 lumens during daylight hours, ranging from 0 , 1000, well below ambient luminosity in direct sunlight (3000 4000 lumens) (M. Shirley and B.G.-M. Assovi, unpubl. data). Similarly, the ambient temperature around the tagged animals averaged 30 C, while comparable temperatures under the forest canopy and in direct sunlight averaged 27.5 C and 38 C respectively, suggesting that the species spends virtually all its time below crown level. At night, the ambient temperature around the pangolins ranged from 3 to 8 C higher than the surrounding environment, but dropped 1 4 C below the daytime average, suggesting an elevated microclimate in their den sites (M. Shirley and B.G.-M. Assovi, unpubl. data). These results are preliminary and further research is needed to better understand the thermal ecology of the species. Leopard (Panthera pardus) and spotted hyaena (Crocuta crocuta) are likely the main natural predators, with black-bellied pangolin remains found in leopard scats at several sites in Gabon (Henschel et al., 2005, 2011) and in Comoe´ National Park in northern Coˆte d’Ivoire (J. Lapuente and K.E. Linsenmair, pers. obs.). Diurnal behavior and small size likely make the species vulnerable to predation by raptors and chimpanzees (Pan troglodytes; Kingdon and Hoffmann, 2013), African rock pythons (Python sebae), and ratels (Mellivora capensis), among other species. The tick Amblyomma compressum has been found on individuals in Central African Republic and Coˆte d’Ivoire (Tahiri-Zagre¨t, 1970b, A. Kotze and E. Suleman, pers. comm.) and Ixodes rasus on
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individuals in Gabon (Sikes, 1966; see also Chapter 29).
Behavior There is little knowledge of black-bellied pangolin behavior because the species has been subject to limited study. Like other pangolins, the species is solitary, with the only lasting social bonds occurring between a mother and present offspring. Hunters in Coˆte d’Ivoire occasionally find two individuals together but it is unclear whether they are mother and offspring or a courting pair (M. Shirley and B.G.-M. Assovi, pers. obs.). The black-bellied pangolin is quadrupedal and being almost strictly arboreal, is an excellent climber. The fore- and hindlimbs are moved in pairs as they hump their way up vertical tree trunks quite rapidly, their movement resembling that of a caterpillar. With the clawed forelimbs probing for grip, they grab the tree trunk or branch with the front feet, hook the tail around the trunk or branch and bring up and anchor the hindfeet close behind. The prehensile tail provides a versatile climbing aid, clinging to branches or extending out as an apparent ballast, effectively serving as a fifth limb. In this way, the black-bellied pangolin can stretch across open spaces between branches, often relying on creepers (Fig. 8.6). The long, flat ventral surface of the tail and the sharp marginal points press against tree trunks to support the animal’s weight. When descending trees too large to grip, black-bellied pangolins have been observed descending in spirals head first, aided by the grip provided by the long, keeled tail curled around the trunk (R. and T. Cassidy, pers. obs.). The species may forage preferentially in trees and other vegetation (Fig. 8.4). This contrasts with the sympatric white-bellied pangolin, which is semi-arboreal, nocturnal and forages both in trees and on the ground (Booth, 1960; Carpaneto and Germi, 1989;
FIGURE 8.6 Black-bellied pangolin in Central African Republic. The species uses all four limbs and its very long, prehensile tail when climbing. Photo credit: Maja Gudehus.
Kingdon and Hoffmann, 2013). The blackbellied pangolin appears to use olfactory senses to locate arboreal ant nests, using its strong claws to break open branches and ant nests to access prey (Fig. 8.5). Columns of foraging ants moving along tree branches will also be consumed, the species using its long, salivary-coated tongue to “lick up” the ants (Kingdon and Hoffmann, 2013; R. and T. Cassidy, pers. obs.). There have been few observations of the species drinking, but initial observations indicate that black-bellied pangolins drink from little hollows of collected rain or dew water in trees rather than descending trees to frequent rivers or lakes (R. and T. Cassidy, pers. obs.). The species has been observed walking on the ground in Central African Republic, Republic of Congo, and Coˆte d’Ivoire, but it is unknown how frequently this behavior occurs (Wilderness Wildlife Trust, unpubl. data; R. and T. Cassidy, pers. obs.; J. Lapuente and K. E. Linsenmair, pers. obs.). In Central African Republic, there are observations of individuals crossing roads without overhead connectivity, and walking to the nearest tree after having fallen to the ground (i.e., out of a tree; R. and T. Cassidy, pers. obs.). The crossing of roads has also been observed in females carrying
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young (R. and T. Cassidy, pers. obs.; J. Lapuente and K.E. Linsenmair, pers. obs.). Black-bellied pangolins are known to swim to cross rivers and move from tree to tree in flooded forest habitats where overhead connectivity does not exist (M. Shirley and B.G.M. Assovi, pers. obs.). In Coˆte d’Ivoire, the species has been observed crossing rivers up to 20 m wide (M. Shirley and B.G.-M. Assovi, pers. obs.). When threatened, the species will roll into a ball with the scales acting as armor, and remain motionless, sometimes for up to several hours after sensing a threat (Kingdon and Hoffmann, 2013; R. and T. Cassidy, pers. obs.). They may actively move further into dense vegetation and liana tangles to avoid detection, resuming normal activity when the threat has passed (M. Shirley and B.G.-M. Assovi, pers. obs.). The species is reportedly very shy, and markedly so compared to other pangolin species. However, rescued animals, particularly younger individuals, have occasionally sought contact with other pangolins and human caregivers (R. and T. Cassidy, pers. obs.).
single offspring (Page`s, 1970, 1972b). Kingdon and Hoffmann (2013) report that breeding is aseasonal and continuous and that females conceive within 9 16 days of parturition. Neonate black-bellied pangolins weigh 100 150 g (TahiriZagre¨t, 1970a) and measure 300 350 mm in length (Kingdon and Hoffmann, 2013). Young are born in a tree hole, in which they stay for the first few days, while the mother forages but returns periodically to nurse the young. Thereafter, the juvenile will cling to the base of the mother’s tail and accompany her to another tree hollow and, and as the juvenile grows, will forage for prey with the mother. The young starts ingesting live prey at about two weeks old. Exact weaning age is unknown but juveniles leave their mother on arrival of the next offspring. Page`s (1975) reports that young blackbellied pangolins wander for 4 5 months before establishing a home range. Full adult size is attained at around 15 months (Page`s, 1970, 1972b), and the species is thought to reach sexual maturity at around two years of age. Lifespan in the wild is unknown, and no animals have been maintained long-term in captivity.
Ontogeny and reproduction
Population
Little is known about reproduction. Being solitary, it is assumed that males and females only come together to mate. The species follows urine and glandular scent trails and it is likely that males monitor the condition of females in this way (Kingdon and Hoffmann, 2013). Page`s (1972a) reports that prereproductive behavior simulates aggression, with the male and female standing chest-tochest. This is followed by the female submitting to the male and clinging to his tail (as an infant clings to the mother’s tail) prior to copulation. During copulation, the male and female’s tails are entwined. Gestation period is estimated to be 140 days and the black-bellied pangolin gives birth to
There are no quantitative data on blackbellied pangolin abundance. Whilst not a formal assessment of abundance, six individuals were captured for a radio-telemetry study within a 400 ha area in southern Coˆte d’Ivoire in 2018 2019, suggesting a minimum density of 0.015 individuals/ha in a swamp forest habitat with a low, but constant, level of subsistence hunting pressure (M. Shirley and B.G.-M. Assovi, pers. obs.). Notably, four of these pangolins were caught within one week along a small river less than 750 m apart within a 15 ha area of forest, suggesting that they can occur at higher densities (e.g., 0.26 individual/ha). This is the least frequently recorded of all African pangolin species,
I. What is a Pangolin?
Threats
possibly reflecting its occurrence in littlepenetrated habitats, its selection of canopy habitats, and/or its shy and rare nature and low natural density (Kingdon and Hoffmann, 2013).
Status Due to a dearth of research on the blackbellied pangolin, populations are not known at any scale site, country, or globally. The species is listed as Vulnerable on The IUCN Red List of Threatened Species, with the global population considered to be declining (Ingram et al., 2019a). In 2016, the species was listed as Endangered at the national level in Uganda using the IUCN Red List Categories and Criteria (Kityo et al., 2016). Like other pangolins, this species is included in CITES Appendix I, and all range states are signatories to the Convention. The black-bellied pangolin is afforded protection through national legislation in range states, which typically prohibits exploitation. Exceptions include Gabon, Republic of Congo, and Sierra Leone, where it is legal to hunt and trade this species under certain conditions, including the holding of permits for hunting and transportation, restrictions on location (e.g., not in protected areas), and seasonality (i.e., open vs. closed seasons).
Threats As with other pangolin species, the primary threats facing the black-bellied pangolin are anthropogenic in origin. Habitat loss and degradation have likely posed the greatest threat to this species historically (see Megevand, 2013). Deforestation throughout West Africa, in particular, is rampant with some countries having lost as much as 98% of their natural forest cover (e.g., Coˆte d’Ivoire and Ghana).
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Contemporarily, the rapidly growing human population and land conversion for agriculture, on-going forestry extraction, and increasing access to habitat in West and Central Africa are apparently facilitating increases in poaching rates (Mayaux et al., 2013). Despite being protected by legislation in range countries, law enforcement is typically problematic and ineffective for a number of reasons including a lack of resources and capacity, both human and technical (Challender and Waterman, 2017), and the black-bellied pangolin is threatened by overexploitation. The species has been, and is, extensively hunted and poached for the bushmeat and traditional African medicine trades and openly displayed in markets across its range (see Chapter 15). Anadu et al. (1988) recorded arboreal pangolins being the eighth most preferred mammal among consumers in southwestern Nigeria. Boakye et al. (2016) reported that the blackbellied pangolin comprised 18% of 98 pangolins traded by chop-bar operators, wholesalers and farmer-hunters in Ghana between 2013 and 2014 (see also Chapter 15). In Gabon, the species continues to be hunted and traded and prices are increasing, and there is a persistent demand for arboreal pangolins, including emerging consumption by immigrant Asian populations (Mambeya et al., 2018). There has been little recorded international trade in this species historically, which has been limited to exports of small numbers of live animals and other derivatives (Challender and Waterman, 2017). However, the CITES trade data indicate the export of 200 live blackbellied pangolins from Nigeria to China in 2015 for captive breeding purposes (Chapters 16 and 32). In 2008, intercontinental trafficking of African pangolins to Asia emerged, primarily involving scales, and between 2008 and 2019 it has ostensibly increased, and included the black-bellied pangolin (see Chapter 16: Mwale et al., 2017). Estimating the number of
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individuals involved is problematic, partly because of poor reporting, but scales from this species have been found in major shipments that have been seized en route to Asian markets. For example, in April 2019 12.9 tonnes of scales, involving an estimated ~35,000 African pangolins, were seized in Singapore en route from Nigeria to Vietnam (Liu, 2019; see Chapter 16 for conversion parameters). Cameroon and Nigeria have been implicated as major exporters (Ingram et al., 2019b) and pangolins in West and Central Africa are being targeted specifically for their scales for illegal export to Asia (see Chapter 16). This is a major threat to the species. Illegal trade in the blackbellied pangolin to Europe for bushmeat consumption has also been recorded (Chaber et al., 2010).
References Allen, G.M., Coolidge, H.J. Jr., 1930. Mammals of Liberia. In: Strong, R.P. (Ed.), The African Republic of Liberia and the Belgian Congo, 2. Contributions of the Department of Tropical Medicine and the Institute for Tropical Biology and Medicine, pp. 569 622. Anadu, P.A., Elamah, P.O., Oates, J.F., 1988. The bushmeat trade in southwestern Nigeria: a case study. Human Ecol. 16 (2), 199 208. Angelici, F.M., Grimod, I., Politano, E., 1999. Mammals of the Eastern Niger Delta (Rivers and Bayelsa States, Nigeria): an environment affected by a gas-pipeline. Folia Zool. 48 (4), 249 264. Angelici, F., Egbide, B., Akani, G., 2001. Some new mammal records from the rainforests of south-eastern Nigeria, Hystrix, Ital. J. Mammol. 12 (1), 37 43. Barnett, A.A., Prangley, M.L., 1997. Mammalogy in the Republic of Guinea: an overview of research from 1946 to 1996, a preliminary check-list and a summary of research recommendations for the future. Mammal Rev. 27 (3), 115 164. Barrie, B., Kante´, S., 2006. A rapid survey of the large mammals in De´re´, Die´cke´ and Mt. Be´ro classified forests in Guine´e-Forestie`re, Southeastern Guinea. In: Wright, H.E., McCullough, J., Alonso, L.E., Diallo, M. S. (Eds.), A Rapid Biological Assessment of Three Classified Forests in Southeastern Guinea. RAP Bulletin of Biological Assessment, 40. Conservation International, Washington, D.C., pp. 189 194. Beja, P., Pinto, P.V., Verı´ssimo, L., Bersacola, E., Fabiano, E., Palmeirim, J.M., et al., 2019. The Mammals of
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I. What is a Pangolin?
8 Black-bellied pangolin Phataginus tetradactyla (Linnaeus, 1766) Maja Gudehus1, Darren W. Pietersen2,3, Michael Hoffmann4, Rod Cassidy1, Tamar Cassidy1, Olufemi Sodeinde5, Juan Lapuente6, Brou Guy-Mathieu Assovi7 and Matthew H. Shirley8 1
Sangha Pangolin Project, Dzanga-Sangha, Central African Republic 2Mammal Research Institute, Department of Zoology and Entomology, University of Pretoria, Hatfield, South Africa 3IUCN SSC Pangolin Specialist Group, N Zoological Society of London, Regent’s Park, London, United Kingdom 4 Conservation and Policy, Zoological Society of London, Regent’s Park, London, United Kingdom 5 Department of Biological Sciences, New York City College of Technology, City University of New York, Brooklyn, NY, United States 6Comoe´ Chimpanzee Conservation Project, Comoe´ Research Station, Coˆte d’Ivoire & Animal Ecology and Tropical Biology, Biozentrum, Universita¨t Wu¨rzburg Tiero¨kologie und Tropenbiologie (Zoologie III), Wu¨rzburg, Germany 7Universite´ Felix Houphoue¨tBoigny, Abidjan, Coˆte d’Ivoire 8Tropical Conservation Institute, Florida International University, North Miami, FL, United States O U T L I N E Taxonomy
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Ecology
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Pangolins DOI: https://doi.org/10.1016/B978-0-12-815507-3.00008-3
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Taxonomy Previously included in the genus Manis (Meester, 1972; Schlitter, 2005) and Uromanis (Kingdon, 1997; McKenna and Bell, 1997; Pocock, 1924), the species is here included in Phataginus based on both morphological (Gaudin et al., 2009) and genetic (du Toit et al., 2017; Gaubert et al., 2018; Hassanin et al., 2015) evidence, in agreement with previous authors (Grubb et al., 1998; Kingdon and Hoffmann, 2013). Based on mitogenomic distances between the genera Manis, Smutsia, and Phataginus, and morphological traits unique to Phataginus, P. tetradactyla is included in the subfamily Phatagininae to designate small African pangolin species (Gaubert et al., 2018; see Chapter 2). In much of the early literature, the species name longicaudatus is used, but this name is unavailable (Mohr, 1961). The type locality is “American Australia” (West Africa; Linnaeus, 1766). No subspecies are recognized. There are no data on chromosome number. Synonyms: Pholidotus longicaudatus (Brisson, 1756; unavailable), Pholidotus longicaudatus (Brisson, 1762; unavailable), Manis tetradactylus (Linnaeus, 1766), Manis macroura (Erxleben, 1777), Phataginus ceonyx (Rafinesque, 1820), Manis africana (Desmarest, 1822), Manis tetradactyla (Gray, 1843), Manis guineensis (Fitzinger, 1872), Manis longicauda (Sundevall, 1842), Manis longicaudata (Sundevall, 1842, sic., fide Pocock, 1924), Manis senegalensis (Fitzinger, 1872), Manis hessi (Noack, 1889), Pholidotus tetradactyla (Sclater, 1901), Uromanis longicaudata (Pocock, 1924), and Manis longicaudatus (Rosevear, 1953). Etymology: Phataginus is derived from “phatagen”, an East Indian name for the pangolin; the species name tetradactyla references the four (tetra-) non-vestigial digits (-dactyla) on the feet (Gotch, 1979).
Description The black-bellied pangolin (Phataginus tetradactyla), is a small, arboreal African pangolin
with a body weight of 1.1 3.6 kg and a total body length of up to 120 cm (Table 8.1). The common name stems from the black skin and hairs that cover most of the ventrum, face, inner sides of the limbs and upper forelimbs and forefeet (Hatt, 1934; Jentink, 1882). The extremely long prehensile tail makes up to twothirds of the total body length (55 75 cm; see Table 8.1; Hatt, 1934; Tahiri-Zagre¨t, 1970a). It has a bare, sensitive skin pad on the ventral tip, which is truncated, and the tail easily supports the weight of the animal (Jentink, 1882; Kingdon, 1971; Pocock, 1924). There are 47 caudal vertebrae (Jentink, 1882), a record among extant mammals. Head-body length ranges between 28 and 50 cm (Table 8.1). The species is covered with large, overlapping scales that are dark brown at the base, with yellow or golden edges, and grow from the skin in a grid-like arrangement (Fig. 8.1). Each scale has slight longitudinal striations (Dorst and Dandelot, 1970; Happold, 1987), and are “harder” (i.e., thicker and more robust) than those of the white-bellied pangolin (P. tricuspis) and other similar sized species of pangolin (Tahiri-Zagre¨t, 1970a; M. Shirley and G.-B.M. Assovi, pers. obs.). The scales cover the surface of the body dorsally and laterally but are absent from parts of the face, the throat, ventrum, inner fore- and hindlimbs, and upper portions of the forelimbs (Jentink, 1882; Kingdon, 1971; Pocock, 1924). Scales on the flanks are keeled (Fig. 8.1; Hatt, 1934). No hairs project between the scales. There are 10 13 transversal, and 13 longitudinal scale rows on the body (Table 8.1), the largest of which are on the mid-dorsum and measure up to 67 3 50 mm (O. Sodeinde, unpubl. data). The lower sections of the forelimbs are protected by pairs of very large postscapular scales (Fig. 8.1; Hatt, 1934). The scales on the forehead, fore- and hindlimbs, and median ventral tail row are the smallest. The elongated tail has 42 47 sharply-pointed scales along its edges (Table 8.1). There are 35 41 scales on the median dorsal scale row of the tail
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Description
TABLE 8.1 Black-bellied pangolin morphometrics. Measurement Weight
Country
Source(s)
2.83 (2.2 3.6) kg, n 5 4
Southeast Nigeria
Kingdon and Hoffmann, 2013
1.41 (1.12 1.65) kg, n 5 12
Central African Republic
R. and T. Cassidy, unpubl. data
2.74 (2.6 3.1) kg, n 5 3
Southeast Nigeria
Kingdon and Hoffmann, 2013
1.45 (1.3 1.7) kg, n 5 4
Central African Republic
R. and T. Cassidy, unpubl. data
874 (810 937) mm, n 5 3
Democratic Republic of the Congo
Hatt, 1934
985 (920 1070) mm, n 5 11
Central African Republic
R. and T. Cassidy, unpubl. data
1007 (820 1210) mm, n 5 7
Coˆte d’Ivoire
Tahiri-Zagre¨t, 1970a
851.4 (755 930) mm, n 5 5
Democratic Republic of the Congo
Hatt, 1934
1040 (970 1110) mm, n 5 4
Central African Republic
R. and T. Cassidy, unpubl. data
1015 (930 1100) mm, n 5 2
Coˆte d’Ivoire
Tahiri-Zagre¨t, 1970a
Total length (unsexed)
1115 (1060 1170) mm, n 5 2
Coˆte d’Ivoire
Tahiri-Zagre¨t, 1970a
Head-body length (R)
314 (286 342) mm, n 5 4
Southeast Nigeria
Kingdon and Hoffmann, 2013
398 (370 460) mm, n 5 10
Central African Republic
R. and T. Cassidy, unpubl. data
Head-body length (Q)
302 (292 311) mm, n 5 3
Southeast Nigeria
Kingdon and Hoffmann, 2013
420 (370 500) mm, n 5 4
Central African Republic
R. and T. Cassidy, unpubl. data
Tail length (R)
613.3 (560 645) mm, n 5 3
Democratic Republic of the Congo
Hatt, 1934
641 (594 707) mm, n 5 4
Southeast Nigeria
Kingdon and Hoffmann, 2013
658 (520 690) mm, n 5 10
Central African Republic
R. and T. Cassidy, unpubl. data
643 (600 710) mm, n 5 7
Coˆte d’Ivoire
Tahiri-Zagre¨t, 1970a
560.6 (505 623) mm, n 5 5
Democratic Republic of the Congo
Hatt, 1934
633 (606 670) mm, n 5 3
Southeast Nigeria
Kingdon and Hoffmann, 2013
620 (600 670) mm, n 5 4
Central African Republic
R. and T. Cassidy, unpubl. data
Tail length (unsexed)
705 (660 750) mm, n 5 2
Coˆte d’Ivoire
Tahiri-Zagre¨t, 1970a
Total number of vertebrae
.70
Liberia
Frechkop, 1931; Jentink, 1882
Cervical
7
Liberia
Jentink, 1882
Thoracic
13
Liberia
Jentink, 1882; Mohr, 1961
Weight (R)
Weight (Q)
Body
Total length (R)
Total length (Q)
Tail length (Q)
Vertebrae
(Continued)
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TABLE 8.1 (Continued) Measurement
Skull
Scales
Country
Source(s)
Lumbar
5 6
Liberia
Jentink, 1882; Mohr, 1961
Sacral
2 3
Liberia
Jentink, 1882; Mohr, 1961
Caudal
46 47
Liberia
Frechkop, 1931; Jentink, 1882; Mohr, 1961
Length (R)
70 (69.1 71) mm, n 5 2
Democratic Republic of the Congo
Hatt, 1934
Length (Q)
65.3 (62.1 68.7) mm, n 5 7
Democratic Republic of the Congo
Hatt, 1934
Breadth across zygomatic processes (R)
24 (23.6 24.4) mm, n 5 2
Democratic Republic of the Congo
Hatt, 1934
Breadth across zygomatic processes (Q)
24.5 (22.8 26.9) mm, n 5 7
Democratic Republic of the Congo
Hatt, 1934
Total number of scales
588 (542 637), n 5 10
Cameroon, unknown
Ullmann et al., 2019
No. of scale rows (transversal, body)
10 13
Frechkop, 1931; Mohr, 1961
No. of scale rows (longitudinal, body)
13
Frechkop, 1931; Jentink, 1882
No. of scales on outer margins of tail
42 47
Frechkop, 1931; Jentink, 1882; Mohr, 1961
No. of scales on median row of tail
35 41
Frechkop, 1931; Jentink, 1882
Scales (wet) as proportion of body weight
No data
Scales (dry) as proportion of body weight
No data
which is replaced by two rows of 9 10 scales towards the tail tip (Fig. 8.2; Frechkop, 1931; Jentink, 1882). The total number of scales is 542 637 (Table 8.1). Scales may lack pigmentation, seemingly sporadically, but usually on the tail or flanks (Fig. 8.2; Hatt, 1934). In older
animals, scales (e.g., on the ventral tail surface) may be worn to the point of having no free edge (Hatt, 1934). Observations of aged individuals in the wild with missing tail scales suggests that the species may permanently lose scales as they age (M. Shirley and B.G.-M. Assovi, pers. obs.).
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Description
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FIGURE 8.1 Black-bellied pangolin in Central African Republic. Visible are the large post-scapular scales on the lower forelimbs, and the keeled scales on the left flank and hindlimb. Photo credit: Alex Ley.
Like other pangolins, the skull demonstrates features associated with a myrmecophagous diet (see Chapter 1). Like the white-bellied pangolin, but unlike other pangolins, the lacrimal bone is present (Emry, 1970). The head is long, slender and naked except for scales on the forehead and coarse black hair (5 10 mm) on the cheeks and throat (Gaubert, 2011; Kingdon and Hoffmann, 2013). The snout is naked and nostrils moist and slightly downturned, and similar in color to the face (Kingdon and Hoffmann, 2013). The eyes are large and beady with dark irises, and are protected by thick, swollen eyelids. The blackbellied pangolin has ear pinnae that are greatly reduced in size and comprise fleshly ridges which border the auditory orifices (Kingdon and Hoffmann, 2013). Like other pangolins, the species is edentate (i.e., lacks teeth).
The tongue is 16 18 cm in length and at the distal end is flattened but has an oval crosssection (Gaubert, 2011). The tongue extends anteriorly from the xiphisternum, a bifurcated, cartilaginous structure formed from the last pair of ribs, which is its point of attachment in the abdomen (Doran and Allbrook, 1973; Sikes, 1966). From the posterior border of the ribs the tongue extends along the ventral surface of the body to the right iliac fossa, and from there proceeds dorsally and then anteriorly, ending in a spatulate cartilaginous structure at the dorsal border of the diaphragm (see Chapter 1; Heath, 2013). The tissues in the thorax form a glossal tube in which the tongue is housed, and which proceeds through the neck to the oral cavity (Doran and Allbrook, 1973). The fore- and hindfeet have five digits with strong, curved claws that are specialized for
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FIGURE 8.2 Black-bellied pangolin climbing a tree in Central African Republic. This figure shows the extremely long tail in this species, the termination of the mediodorsal scale row near the distal end of the tail, and several scales that lack pigmentation. Photo credit: Maja Gudehus.
breaking into ant nests. On the forefeet the first digit is vestigial—and essentially functionless —giving the appearance of only four digits, while the fifth digit is nearly as long as the fourth and better developed than in other pangolin species (Pocock, 1924). The third digit and claw is the largest and strongest. The hindfeet are elongated, resembling the forefeet to an extent, with four long, well-developed claws of approximately equal length; the innermost claw is vestigial (Pocock, 1924). Both fore- and hindfeet have well developed skin pads, which in the hindfeet extend from the level of the first digit to the heel (Pocock, 1924).
A pair of anal glands are situated on the lateral borders of the anus and produce a strong, musky scent that may be used in scent-marking, and perhaps in defense when threatened, but this has not been observed (Pocock, 1924). Pangolin hunters in Coˆte d’Ivoire claim to be able to detect black-bellied pangolins via this scent (M. Shirley and B.G.-M. Assovi, unpubl. data). The female’s vulva is situated just anterior to the anus; they have two pectoral nipples. In males, the testes are situated in the inguinal area and do not descend into a scrotum (see Chapter 1). Body temperature is regulated at 30 36 C; average resting metabolic rate has been estimated at 160.2 ml O2/kg/h (Hildwein, 1974). Despite significant differences in appearance, black-bellied pangolins are often confused with the sympatric white-bellied pangolin. They can most easily be distinguished by skin color and scale size and coloration. Scales are proportionally larger on the black-bellied pangolin and dark brown with yellow-golden edging as opposed to gray- or yellowish-brown on the white-bellied pangolin, and the scales may be noticeably longer than they are wide on the latter. The blackbellied pangolin has two very large postscapular scales (Fig. 8.1), which are not enlarged and are inferior in the white-bellied pangolin. The black-bellied pangolin is distinguished from the two terrestrial African pangolins by its smaller size, extremely long tail, skin color, and scale coloration.
Distribution The black-bellied pangolin is distributed throughout the forested regions of West and Central Africa, from Sierra Leone to the eastern limits of the Congo Basin (Fig. 8.3). Grubb et al. (1998) refuted records of the species from west of Sierra Leone, including from Senegal, The Gambia, and Guinea-Bissau (e.g., Frade, 1949; Meester, 1972; Schlitter, 2005), and suggested the most westerly confirmed record is
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FIGURE 8.3 Black-bellied pangolin distribution. Source: Ingram et al., 2019a.
from the Western Area Peninsula Forest National Park in Sierra Leone. Reiner and Simo˜es (1999) considered their presence in Guinea-Bissau possible, but there is no confirmatory evidence. There are confirmed records from a number of forest reserves in southeastern Guinea (Barnett and Prangley, 1997; Barrie and Kante´, 2006), Liberia (Allen and Coolidge, 1930), southern Coˆte d’Ivoire (Rahm, 1956), and southwestern Ghana, west of the Volta (Grubb et al., 1998). The species was recorded in Comoe´ National Park in northern Coˆte d’Ivoire for the first time in 2016 (J. Lapuente and K.E. Linsenmair, unpubl. data) and there are reports of the species occurring at other sites in
northern Coˆte d’Ivoire. If accurate, it is reasonable to assume the species may also occur in northern Ghana. There is then an apparent gap in distribution until southwestern Nigeria (Angelici et al., 2001; Happold, 1987), from where the species ranges eastward through southern Cameroon (Jeannin, 1936) and southwestern Central African Republic to eastern Democratic Republic of the Congo (DRC; Hatt, 1934; Rahm, 1966; Schouteden, 1944), the easternmost limit of their distribution. Blench and Dendo (2007) report that in Nigeria the black-bellied pangolin is more common in the southeast than in the southwest. Southwards the species ranges through Gabon and Republic
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of Congo (Malbrant and MacLatchy, 1949). Further investigation is warranted in the Semuliki Valley of Uganda, a well-known refuge of Congolese fauna and flora in East Africa where both the giant (Smutsia gigantea) and white-bellied pangolin occur. The presence of the species in Angola is unclear, and deserves some brief discussion. There is no mention of the species in several major reference works (Beja et al., 2019; Bocage, 1889, 1890; Hill and Carter, 1941; Machado, 1969; Thomas, 1904). Monard (1935) notes that they should occur south to the Kunene but provides no material basis for this statement. Mohr (1961) noted they occur to Moc¸amedes, but again the basis for this is unclear. Feiler (1990) includes them in his checklist, noting that they were first recorded prior to 1990, but without reference to a specimen or a locality. There are records of the species from the Bas-Congo province of Republic of Congo (Schouteden, 1944), and hence there seems no reason that the species should not occur at least in Cabinda (Kingdon and Hoffmann, 2013; Taylor et al., 2018).
Habitat Specific studies documenting habitat use by the black-bellied pangolin are limited. The species is the most arboreal of the African pangolins and is often found in riparian and swamp forests, typically in habitats dominated by palms (including rattans) and specialized swamp trees, such as Uapaca sp., Pseudospondis sp., and Mitragina sp. (Happold, 1987; Kingdon and Hoffmann, 2013; Page`s, 1970), as well as in primary forests and forest-savanna mosaic. Records in the catalogues of the American Museum of Natural History and the Smithsonian National Museum of Natural History indicate that most individuals in these collections were caught in primary forests. This is also the case in Central African Republic and
northern Coˆte d’Ivoire, where the black-bellied pangolin has most frequently been found in primary, closed canopy forest, away from swamp and riverine forests (R. and T. Cassidy, unpubl. data; J. Lapuente and K.E. Linsenmair, pers. obs.). In the forest-savanna mosaic of Coˆte d’Ivoire’s Comoe´ National Park, the species inhabits forests dominated by Annogeissus leiocarpus, Dialium guineense, Diospyros abissinica, and Drypetes floribunda which are far from rivers and lack palms (J. Lapuente and K.E. Linsenmair, pers. obs.). In contrast, in southern Coˆte d’Ivoire, the species is found in flooded swamp forests dominated by palms, Raphia hookeri and Hallea ledermanii, such as in the Forets des Marais de Tanoe-Ehy and the Reserve Communautaire de Dodo, and in neighboring oil palm and rubber plantations (Fig. 8.4). In these habitats, the black-bellied pangolin can also often be found foraging in the shrubby vegetation at the riverside, not more than a meter above the water (M. Shirley and B.G.-M. Assovi, pers. obs.). In southeastern Nigeria, the species has been recorded in primary and secondary rainforests, in regenerating forests, swamp forests, and farmlands (Angelici et al., 1999, 2001; Luiselli et al., 2015). Hunters and forest workers in southwestern Nigeria report harvesting pangolins, including the blackbellied pangolin on occasion, in abandoned or infrequently harvested oil palm plantations in secondary forests (Sodeinde and Adedipe, 1994). In all forest types, the black-bellied pangolin appears to predominantly use the crown strata more than others, which perhaps contributes to the lack of observations. Preliminary observations suggest that the species is more abundant in less disturbed habitats and those less frequented by people (M. Shirley and B.G.-M. Assovi, pers. obs.). Further research is needed to understand habitat requirements and selection, and their potential influence on the distribution of this species.
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Ecology
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FIGURE 8.4 Adult female black-bellied pangolin in the flooded swamp forests of southeastern Coˆte d’Ivoire. Photo credit: Matthew H. Shirley.
Ecology The black-bellied pangolin is predominantly diurnal, though does demonstrate some nocturnal activity (Booth, 1960; Carpaneto and Germi, 1989; Page`s, 1970; R. and T. Cassidy, unpubl. data). Records of two black-bellied pangolins monitored daily over a period of two years, and post-release observations of eight individuals confiscated from illegal trade in Central African Republic, support the assertion that the species is all but strictly diurnal (R. and T. Cassidy, pers. obs.). Only two efforts have been made to estimate the home range size of the species, one using over two years of near daily follow data for two rehabilitated and released individuals (9 12 months of age) in Central African
Republic (R. and T. Cassidy, unpubl. data), and a nascent study of six radio-tagged individuals tracked for two months in Coˆte d’Ivoire. In Central African Republic the home ranges were very small, comprising 48 and 12 ha (95% and 50% Kernel Use Density [KUD], respectively), and ranged from 36.3 to 56.2 ha (95% KUD) and 7.2 15.01 ha (50% KUD) from the first to second year respectively. In addition to little variation in annual home range, there was little apparent shift in the area of forest used, the individuals ranging over an area of 32.4 ha (95% Minimum Convex Polygon [MCP], roughly 1.2 3 0.5 linear km). In Coˆte d’Ivoire, preliminary individual home ranges for six individuals (comprising both sexes) averaged 9.27 ha (95% MCP), ranging from 0.13 to 25.9 ha (M. Shirley and B.G.-M. Assovi,
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unpubl. data). Within home ranges, individuals appear to use fixed routes and refuge holes on a continuous basis (Page`s, 1970). The species sleeps curled-up in tree hollows, tree ferns, or in tangles of lianas, and occasionally in hollowed-out insect nests. Like all pangolins, the species is myrmecophagous. However, unlike other species, the black-bellied pangolin appears to persist on a diet of tree ants (Fig. 8.5) and does not seem to prey on termites extensively, or even at all (Kingdon and Hoffmann, 2013; R. and T. Cassidy, pers. obs.; M. Shirley and B.G.-M. Assovi, pers. obs.). Crematogaster spp. and Cataulacus spp. have been reported as preferred species (Kingdon and Hoffmann, 2013), while observations in Central African Republic indicate that the species’ diet consists of at least seven different ant species, including Cataulacus guineensis, Oecophylla longinoda and Polyrhachis spp., including their eggs, larval and pupal stages (M. Gudehus, unpubl. data). Sweat bees (Halictidae) are also occasionally taken (R. and T. Cassidy, pers. obs.). The frequency of feeding bouts and proportion of time spent feeding has only been recorded for a period of two weeks, but observations suggest that the black-bellied pangolin spends most of its time resting or foraging for prey (R. and T. Cassidy, pers. obs.).
FIGURE 8.5 Black-bellied pangolin breaking into an arboreal ant nest. This species appears to predate almost exclusively on ants. Photo credit: Michael Lorentz.
The thermal ecology of pangolins in general is not well known, including body temperature and its impact on ecology. Preliminary insights from research in Coˆte d’Ivoire appear to refute the suggestion that the black-bellied pangolin spends time basking at the forest crown for thermoregulatory, or potentially, other reasons. Temperature and light data loggers attached to black-bellied pangolins in 2018 indicated that the tagged animals were exposed to an average of 110 170 lumens during daylight hours, ranging from 0 , 1000, well below ambient luminosity in direct sunlight (3000 4000 lumens) (M. Shirley and B.G.-M. Assovi, unpubl. data). Similarly, the ambient temperature around the tagged animals averaged 30 C, while comparable temperatures under the forest canopy and in direct sunlight averaged 27.5 C and 38 C respectively, suggesting that the species spends virtually all its time below crown level. At night, the ambient temperature around the pangolins ranged from 3 to 8 C higher than the surrounding environment, but dropped 1 4 C below the daytime average, suggesting an elevated microclimate in their den sites (M. Shirley and B.G.-M. Assovi, unpubl. data). These results are preliminary and further research is needed to better understand the thermal ecology of the species. Leopard (Panthera pardus) and spotted hyaena (Crocuta crocuta) are likely the main natural predators, with black-bellied pangolin remains found in leopard scats at several sites in Gabon (Henschel et al., 2005, 2011) and in Comoe´ National Park in northern Coˆte d’Ivoire (J. Lapuente and K.E. Linsenmair, pers. obs.). Diurnal behavior and small size likely make the species vulnerable to predation by raptors and chimpanzees (Pan troglodytes; Kingdon and Hoffmann, 2013), African rock pythons (Python sebae), and ratels (Mellivora capensis), among other species. The tick Amblyomma compressum has been found on individuals in Central African Republic and Coˆte d’Ivoire (Tahiri-Zagre¨t, 1970b, A. Kotze and E. Suleman, pers. comm.) and Ixodes rasus on
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individuals in Gabon (Sikes, 1966; see also Chapter 29).
Behavior There is little knowledge of black-bellied pangolin behavior because the species has been subject to limited study. Like other pangolins, the species is solitary, with the only lasting social bonds occurring between a mother and present offspring. Hunters in Coˆte d’Ivoire occasionally find two individuals together but it is unclear whether they are mother and offspring or a courting pair (M. Shirley and B.G.-M. Assovi, pers. obs.). The black-bellied pangolin is quadrupedal and being almost strictly arboreal, is an excellent climber. The fore- and hindlimbs are moved in pairs as they hump their way up vertical tree trunks quite rapidly, their movement resembling that of a caterpillar. With the clawed forelimbs probing for grip, they grab the tree trunk or branch with the front feet, hook the tail around the trunk or branch and bring up and anchor the hindfeet close behind. The prehensile tail provides a versatile climbing aid, clinging to branches or extending out as an apparent ballast, effectively serving as a fifth limb. In this way, the black-bellied pangolin can stretch across open spaces between branches, often relying on creepers (Fig. 8.6). The long, flat ventral surface of the tail and the sharp marginal points press against tree trunks to support the animal’s weight. When descending trees too large to grip, black-bellied pangolins have been observed descending in spirals head first, aided by the grip provided by the long, keeled tail curled around the trunk (R. and T. Cassidy, pers. obs.). The species may forage preferentially in trees and other vegetation (Fig. 8.4). This contrasts with the sympatric white-bellied pangolin, which is semi-arboreal, nocturnal and forages both in trees and on the ground (Booth, 1960; Carpaneto and Germi, 1989;
FIGURE 8.6 Black-bellied pangolin in Central African Republic. The species uses all four limbs and its very long, prehensile tail when climbing. Photo credit: Maja Gudehus.
Kingdon and Hoffmann, 2013). The blackbellied pangolin appears to use olfactory senses to locate arboreal ant nests, using its strong claws to break open branches and ant nests to access prey (Fig. 8.5). Columns of foraging ants moving along tree branches will also be consumed, the species using its long, salivary-coated tongue to “lick up” the ants (Kingdon and Hoffmann, 2013; R. and T. Cassidy, pers. obs.). There have been few observations of the species drinking, but initial observations indicate that black-bellied pangolins drink from little hollows of collected rain or dew water in trees rather than descending trees to frequent rivers or lakes (R. and T. Cassidy, pers. obs.). The species has been observed walking on the ground in Central African Republic, Republic of Congo, and Coˆte d’Ivoire, but it is unknown how frequently this behavior occurs (Wilderness Wildlife Trust, unpubl. data; R. and T. Cassidy, pers. obs.; J. Lapuente and K. E. Linsenmair, pers. obs.). In Central African Republic, there are observations of individuals crossing roads without overhead connectivity, and walking to the nearest tree after having fallen to the ground (i.e., out of a tree; R. and T. Cassidy, pers. obs.). The crossing of roads has also been observed in females carrying
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young (R. and T. Cassidy, pers. obs.; J. Lapuente and K.E. Linsenmair, pers. obs.). Black-bellied pangolins are known to swim to cross rivers and move from tree to tree in flooded forest habitats where overhead connectivity does not exist (M. Shirley and B.G.M. Assovi, pers. obs.). In Coˆte d’Ivoire, the species has been observed crossing rivers up to 20 m wide (M. Shirley and B.G.-M. Assovi, pers. obs.). When threatened, the species will roll into a ball with the scales acting as armor, and remain motionless, sometimes for up to several hours after sensing a threat (Kingdon and Hoffmann, 2013; R. and T. Cassidy, pers. obs.). They may actively move further into dense vegetation and liana tangles to avoid detection, resuming normal activity when the threat has passed (M. Shirley and B.G.-M. Assovi, pers. obs.). The species is reportedly very shy, and markedly so compared to other pangolin species. However, rescued animals, particularly younger individuals, have occasionally sought contact with other pangolins and human caregivers (R. and T. Cassidy, pers. obs.).
single offspring (Page`s, 1970, 1972b). Kingdon and Hoffmann (2013) report that breeding is aseasonal and continuous and that females conceive within 9 16 days of parturition. Neonate black-bellied pangolins weigh 100 150 g (TahiriZagre¨t, 1970a) and measure 300 350 mm in length (Kingdon and Hoffmann, 2013). Young are born in a tree hole, in which they stay for the first few days, while the mother forages but returns periodically to nurse the young. Thereafter, the juvenile will cling to the base of the mother’s tail and accompany her to another tree hollow and, and as the juvenile grows, will forage for prey with the mother. The young starts ingesting live prey at about two weeks old. Exact weaning age is unknown but juveniles leave their mother on arrival of the next offspring. Page`s (1975) reports that young blackbellied pangolins wander for 4 5 months before establishing a home range. Full adult size is attained at around 15 months (Page`s, 1970, 1972b), and the species is thought to reach sexual maturity at around two years of age. Lifespan in the wild is unknown, and no animals have been maintained long-term in captivity.
Ontogeny and reproduction
Population
Little is known about reproduction. Being solitary, it is assumed that males and females only come together to mate. The species follows urine and glandular scent trails and it is likely that males monitor the condition of females in this way (Kingdon and Hoffmann, 2013). Page`s (1972a) reports that prereproductive behavior simulates aggression, with the male and female standing chest-tochest. This is followed by the female submitting to the male and clinging to his tail (as an infant clings to the mother’s tail) prior to copulation. During copulation, the male and female’s tails are entwined. Gestation period is estimated to be 140 days and the black-bellied pangolin gives birth to
There are no quantitative data on blackbellied pangolin abundance. Whilst not a formal assessment of abundance, six individuals were captured for a radio-telemetry study within a 400 ha area in southern Coˆte d’Ivoire in 2018 2019, suggesting a minimum density of 0.015 individuals/ha in a swamp forest habitat with a low, but constant, level of subsistence hunting pressure (M. Shirley and B.G.-M. Assovi, pers. obs.). Notably, four of these pangolins were caught within one week along a small river less than 750 m apart within a 15 ha area of forest, suggesting that they can occur at higher densities (e.g., 0.26 individual/ha). This is the least frequently recorded of all African pangolin species,
I. What is a Pangolin?
Threats
possibly reflecting its occurrence in littlepenetrated habitats, its selection of canopy habitats, and/or its shy and rare nature and low natural density (Kingdon and Hoffmann, 2013).
Status Due to a dearth of research on the blackbellied pangolin, populations are not known at any scale site, country, or globally. The species is listed as Vulnerable on The IUCN Red List of Threatened Species, with the global population considered to be declining (Ingram et al., 2019a). In 2016, the species was listed as Endangered at the national level in Uganda using the IUCN Red List Categories and Criteria (Kityo et al., 2016). Like other pangolins, this species is included in CITES Appendix I, and all range states are signatories to the Convention. The black-bellied pangolin is afforded protection through national legislation in range states, which typically prohibits exploitation. Exceptions include Gabon, Republic of Congo, and Sierra Leone, where it is legal to hunt and trade this species under certain conditions, including the holding of permits for hunting and transportation, restrictions on location (e.g., not in protected areas), and seasonality (i.e., open vs. closed seasons).
Threats As with other pangolin species, the primary threats facing the black-bellied pangolin are anthropogenic in origin. Habitat loss and degradation have likely posed the greatest threat to this species historically (see Megevand, 2013). Deforestation throughout West Africa, in particular, is rampant with some countries having lost as much as 98% of their natural forest cover (e.g., Coˆte d’Ivoire and Ghana).
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Contemporarily, the rapidly growing human population and land conversion for agriculture, on-going forestry extraction, and increasing access to habitat in West and Central Africa are apparently facilitating increases in poaching rates (Mayaux et al., 2013). Despite being protected by legislation in range countries, law enforcement is typically problematic and ineffective for a number of reasons including a lack of resources and capacity, both human and technical (Challender and Waterman, 2017), and the black-bellied pangolin is threatened by overexploitation. The species has been, and is, extensively hunted and poached for the bushmeat and traditional African medicine trades and openly displayed in markets across its range (see Chapter 15). Anadu et al. (1988) recorded arboreal pangolins being the eighth most preferred mammal among consumers in southwestern Nigeria. Boakye et al. (2016) reported that the blackbellied pangolin comprised 18% of 98 pangolins traded by chop-bar operators, wholesalers and farmer-hunters in Ghana between 2013 and 2014 (see also Chapter 15). In Gabon, the species continues to be hunted and traded and prices are increasing, and there is a persistent demand for arboreal pangolins, including emerging consumption by immigrant Asian populations (Mambeya et al., 2018). There has been little recorded international trade in this species historically, which has been limited to exports of small numbers of live animals and other derivatives (Challender and Waterman, 2017). However, the CITES trade data indicate the export of 200 live blackbellied pangolins from Nigeria to China in 2015 for captive breeding purposes (Chapters 16 and 32). In 2008, intercontinental trafficking of African pangolins to Asia emerged, primarily involving scales, and between 2008 and 2019 it has ostensibly increased, and included the black-bellied pangolin (see Chapter 16: Mwale et al., 2017). Estimating the number of
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8. Black-bellied pangolin Phataginus tetradactyla
individuals involved is problematic, partly because of poor reporting, but scales from this species have been found in major shipments that have been seized en route to Asian markets. For example, in April 2019 12.9 tonnes of scales, involving an estimated ~35,000 African pangolins, were seized in Singapore en route from Nigeria to Vietnam (Liu, 2019; see Chapter 16 for conversion parameters). Cameroon and Nigeria have been implicated as major exporters (Ingram et al., 2019b) and pangolins in West and Central Africa are being targeted specifically for their scales for illegal export to Asia (see Chapter 16). This is a major threat to the species. Illegal trade in the blackbellied pangolin to Europe for bushmeat consumption has also been recorded (Chaber et al., 2010).
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