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Mammalia 2015; aop Morpho-anatomical characteristics of Indian pangolin (


Manis crassicaudata ) from Potohar Plateau, Pakistan

Article  in  Mammalia · February 2015


DOI: 10.1515/mammalia-2014-0179

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Mammalia 2015; aop

Short Note

Nausheen Irshad, Tariq Mahmood* and Muhammad Sajid Nadeem

Morpho-anatomical characteristics of Indian


pangolin (Manis crassicaudata) from Potohar
Plateau, Pakistan

Abstract: We collected 10 live and two dead specimens of occurrence in southwest China and Myanmar (IUCN
of Indian pangolin (Manis crassicaudata) from Potohar 1996). The presence of 11–13 rows of blonde-striated scales
Plateau to record their morpho-anatomical characteris- on the body makes it distinctive among other mammals
tics. The average body weight and length were recorded (Roberts 1997). It has a meager audible range but has a
in three age classes: juvenile, sub-adult and adult. The highly developed sense of smell used for searching food
maximum body weight, body length and tail length was as it snuffles in the air to detect ants and termites (Heath
20 kg, 147.3 cm, and 85.7 cm, respectively. The total num- 1988). Its feet have spongy pads fortified with strong claws
ber of scales was 286±6.4, 271±24 and 294±11.0 in the juve- and digits that are capable of digging burrows.
nile, sub-adult and adult stages, respectively. The size of The body weight of an adult Indian pangolin was
the scales varied on different body regions, with smallest reported to be 8–11 kg and its body length ranged from
being on the head and the largest on the trunk region. The 48 to 75 cm; a long sticky tongue and a highly muscu-
number of scales on the head differed significantly from lar stomach is considered to be a compensation for not
that on the trunk (p < 0.01) and tail (p < 0.05) regions. The having teeth (Prater 1971). The two mammae (5–8 mm) in
number and size of the scales on the fore limbs differed females are positioned in the thoracic region. In males,
significantly (p < 0.05) from those on the hind limbs. The the testes do not descend down into the scrotum but are
relative tongue length constituted 37% of the total body retained in the abdomen. The Indian pangolin produces a
length of the adult specimens. The digestive tract consti- heckling sound when distressed. For defense, it hides its
tuted 7% of the relative body weight and 19%–23% of the soft body parts under hard scales, curls up, and also emits
relative body length, whereas relative length of the repro- some fluid from its anal gland (Roberts 1997).
ductive tract was 12%. The Asian pangolin species have been categorized
under Appendix II of the CITES since 1975 (CITES 2000).
Keywords: anatomy; Indian pangolin; morphometery; However, international trade of these species has been
Pakistan. proscribed as they are assigned zero export quotas in
2000 (Pantel and Chin 2008). The Indian pangolin has
DOI 10.1515/mammalia-2014-0179 recently been listed as “Endangered”, but this change in
Received December 19, 2014; accepted December 19, 2014 conservation status has not deterred the massive illegal
killings of the species in the Potohar Plateau (Mahmood
et  al. 2012). Information about the morphology and
The Indian pangolin (Manis crassicaudata, E. Geoffroy, anatomy of wild Indian pangolin is not well documented
1803) is distributed in South Asia from the eastern parts of because of lack of scientific data about the species in
Pakistan to much of India south of the Himalayas, south- the region. In the present study, we measured the exter-
ern Nepal, Bangladesh and Sri Lanka with historical record nal characteristics and some internal visceral organs of
Indian pangolin specimens collected from the Potohar
*Corresponding author: Tariq Mahmood, Assistant Professor, Plateau, Pakistan.
Department of Wildlife Management, PMAS-Arid Agriculture A total of 10 live and two dead specimens collected
University, Rawalpindi 46300, Pakistan,
from Potohar Plateau (32°33′ and 34°3′ N and 71°89′ and
e-mail: tariqjanjua75@uaar.edu.pk
Nausheen Irshad and Muhammad Sajid Nadeem: Department
73°37′ E, Table 1) were segregated into different age classes
of Wildlife Management, PMAS-Arid Agriculture University, following Lim et al. (2007) with slight modifications. Lim
Rawalpindi 46300, Pakistan et al. (2007) considered Manis javanica with a body mass of

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Table 1 External body measurements of different specimens (n = 12) of Indian pangolin captured/collected from different areas at the Potohar Plateau.

Site of capture/collection   Sex  Body  Body girth  Head-body  Tail length  Total  Snout  Ear length  Limbs length (cm)
weight (kg) (cm) length (cm) (cm) length (cm) length (cm) (cm) 
Fore limbs  Hind limbs

Juveniles specimens
Chakri (Sihal)RWP   Male  0.780  20.32  25.4  16.5  41.6  1.9  0.75  7.6  6.8
Jhelum (Pamal)   Male  2.05  25.4  36.83  22.8  58  3.8  1  12.7  10.16
Chakwal (Murreed)   Male  2  30.48  35.56  27.9  63.5  3.8  1  12.7  10.16
2      N. Irshad et al.: Morpho-anatomy of Indian pangolin

Mean±SE   n = 3  1.61±0.41  25.4±2.9  32.5±3.61  22.4±3.29  54.36±6.57  3.16±0.63  0.91±0.83  11.0±1.70  9.04±1.12

Sub-adult specimens
Islamabad (Malpur)   Female  4.5  38.1  51.81  40.6  92.4  4.3  1  17.78  16.5
Chakwal (Khai)   Female  7.5  66.04  60  53  113  4.8  1  16.51  13.9
Chakri (Sihal)   Male  8  68.58  72.6  85.7  118  4.8  1  15.24  12.7
Mean±SE   n = 3  6.66±1.09  57.57±9.76  61.47±6.04  59.76±13.4  107.8±7.8  4.63±0.1  1.00±0.0  16.51±0.73  14.36±1.12

Adult specimens

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Chakwal (Murreed)   Male  11  50.8  81  53  134  5.08  1.5  15.24  12.7
Islamabad (Lake View park)   Male  15.4  76.2  76.2  71  147.3  5.58  2  17.78  15.24
Chakwal (Jubairpur)   Male  19.3  66.04  84.3  71  137.48  6.35  2  18.28  15.24
Chakri (Mehra)   Female  20  68.58  83.3  53.8  137  8.12  2  17.78  14.7

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Mean±SE   n = 4  16.42±2.0  65.41±5.3  81.2±1.8  62.2±5  138.95±2.8  6.28±0.6  1.88±0.1  17.27±0.60  14.47±0.60

Chakri (Sihal)   Skeleton  –  –  50  30.48  80.4  2.5  –  –  –


Chakri (Sihal)   Skeleton  –  –  43  25.4  68.4  2.5  –  –  –
N. Irshad et al.: Morpho-anatomy of Indian pangolin      3

up to 3.0 kg as juvenile and those weighing more than 3.0 22.40±3.29, 59.76±13.4 and 62.20±5.0 cm for juveniles, sub-
kg as adults. On the basis of body weight, we categorized adults and adults, respectively. Similarly, the average tail
Manis crassicaudata into three age classes: juveniles (  ≤  2.5 length varied among age classes: 22.40±3.29, 59.76±13.4
kg), sub-adults (  ≤  8 kg) and adults ( ≥ 8 kg). The body size and 62.20±5.0  cm for juveniles, sub-adults and adults,
(head to body length) is also an important consideration respectively (Table 1). In all three age classes, we found
in this regard (Table 1). The body weights of the specimens that the fore limbs were larger than the hind limbs; the
were recorded using a digital weighing balance, whereas limbs possessed five digits each, with the central digit
the external body measurements were taken using a meas- being the largest. The average snout length also differed
uring tape. Tail length was recorded by upraising the among the age classes (Table 1).
tail from its base. The size of scales, snout and ears were The total number of body scales among the age
measured using a digital Vernier caliper. The two dead classes also varied (Table 2). The largest and the maximum
specimens were dissected to perform anatomical meas- number of scales were observed on the trunk region, fol-
urements. The weight and length of the visceral organs, lowed by those on the tail region. The scales on the fore
namely, the tongue, heart, lungs, liver and kidney, as well limbs were relatively larger than those on the hind limbs
as the digestive and reproductive systems, were measured. (Figure 1). The number of scales on the head region dif-
The average body weight of juveniles (n = 3), sub- fered significantly from that on the trunk (paired t-test;
adults (n = 3) and adults (n = 4) was 1.61±0.41, 6.66±1.09 and p < 0.01, df = 8, t = -13.19) and tail regions (p < 0.05, df = 8,
16.42±2 kg (Table 1). The average body girth was 25.40±2.9, t = -3.24) (Figure 1), and that on the fore limbs differed
57.57±9.76 and 65.40±5.3 cm for juveniles, sub-adults and significantly (p < 0.05, df = 7, t = 4.08) from that on the
adults, respectively (Table 1). The average body length was hind limbs. The size of scales on the head, trunk and tail

Table 2 Number and size of scales present on different parts of the body of juvenile, sub-adult and adult specimens of the Indian pangolin
collected from the Potohar Plateau (n = 10).

Age classes  Scale number  Scale size (cm)


   
Head  Trunk  Tail  Total  Forelimb  Hind limb Head  Trunk  Tail

Juvenile   58.3±6.0  145±7.2  83.0±2.6  286±6.4  50.3±2.9  46.6±2.4  1.4±1.0  2.9±1.1  1.8±1.1
Sub-adult   63.0±10.5  128±9.9  79.6±4.8  271±24  48.5±0  40±0  0.4±0  3.05±0  1.5±0
Adult   63.5±6.6  146±7.4  84.7±6.9  294±11  51.7±1.7  47±2.9  2±0.4  5.3±0.6  4±1.3

Values presented as mean±SE.

Head (cm) Trunk (cm) Tail (cm)

10
9
8
7
Size of scales

6
5
4
3
2
1
0
Khai Mureed Murreed Jubairpur Sihal Mehra Sihal Pamal Lake Malpur
view park

Chakwal Rawalpindi (Chakri) Jhelum Islamabad


Sites of capture

Figure 1 Relative size of scales (cm) present on different body regions of Indian pangolin. Values presented as mean±SE.

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4      N. Irshad et al.: Morpho-anatomy of Indian pangolin

Table 3 Absolute and relative weight and length of the body organs of two adult dead specimens of the Indian pangolin collected from the
Potohar Plateau.

Body organs   Specimen 1  Specimen 2


   
Absolute  Relative body  Absolute body  Relative body Absolute  Relative body  Absolute  Relative
weight (g) weight (%) length (cm) length (%) weight (g) weight (%) length (cm) length (%)

Gross body   7500  –  112.5  –  4500  –  91  –


Tongue   15  0.2  42.5  37  –  –  –  –
Liver   228  3.04  10  8.8  132  3  7  7.6
Spleen   22  0.29  8  7  17  0.37  5.5  6.04
Heart   43  0.5  5  4.4  26  0.57  4  4.39
Lungs   8  0.1  7  6.2  13  0.28  6  6.59
Kidney   44  0.58  5  4.4  35  0.7  4  4.3
Digestive tract   574  7.6  26  23  340  7.5  18  19.7
Reproductive tract   36  0.48  14  12.4  –  –  –  –

300
300
270

250
Absolute lengths (cm)

200

150

100

50 35
15 12.5 12
1 0.3 5 7 4 1.25
0
Stomach Small Large Ovary Oviduct Uterus Cervix Vagina
intestine intestine

Digestive system Reproductive system


Body organs

Figure 2 Relative size of different parts of the digestive and reproductive tracts of two dead specimens of Indian pangolin recovered as
roadkills from the Potohar Plateau.

regions also differed significantly (ANOVA Single factor; The body mass was found to be positively corre-
p < 0.05, df = 2, F Crit. = 3.46). lated with the body length (r2 = 0.89), snout (r2 = 0.93) and
Anatomical measurements for the two dead speci- ear (r2 = 0.94) (Figure 3). Similarly, the body length was
mens found as roadkills are given in Table 3 and Figure 2. positively correlated with body girth (r2 = 0.85), snout
The tongue constituted 37% of the total body length of the length (r2 =0.75) and ear length (r2 = 0.77) (Figure 4). The
adult (specimen 1). The digestive tract comprised 7% of body girth and snout length were also positively corre-
the relative body weight and 19%–23% of the relative body lated (r2 = 0.78).
length, whereas the relative length of the reproductive In Pakistan, the Indian pangolin is patchily distributed
tract was 12% (Table 3). The length of the ovary, oviduct, in sub-tropical thorn forests, dry deciduous scrub forests,
uterus, cervix and vagina were 0.3, 5, 7, 4 and 1.25 cm, the Indus plains, etc. Despite its recently revised status as
respectively. The two mammae were located in the ventral “Endangered” (IUCN 2004), it is illegally hunted and used
thoracic region, and the length of each mammary gland as source of human food (in some countries, but not in
was 0.5 cm for the sub-adult female and 2 cm for the male Pakistan except for a few five-star hotels and restaurants
prepuce (juvenile). in the capital city Islamabad where this species is served).

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N. Irshad et al.: Morpho-anatomy of Indian pangolin      5

Body mass (kg) Total body length (cm)


A 180
160
147.3
140
134 137.48 137
120 118
Ascending level

113
100
92.4
80
63.5
60
58
40 41.6

20
4.5 7.5 19.3 20
0.78 2.05 2 11 15.4
0 8
1 2 3 4 5 6 7 8 9 10
-20

Body mass (kg) Snout length


B 35

30
Body mass (kg) and snout length (cm)

8.12

25 6.35

20 5.58
19.3 20
5.08 15.4
15
4.8
4.8
10 11
4.3
3.8 3.8 7.5 8
5
1.9 4.5
2.05
0.78 2
0
1 2 3 4 5 6 7 8 9 10

Body mass (kg) Ear length


C 25

20
20
19.3
Ascending level

15 15.4

11
10
7.5
8
5
2.05 2 4.5 2 2 2
1 1 1 1.5
1 1
0 0.78
1 2 3 4 5 6 7 8 9 10
Numbers of specimens of Indian pangolin

Figure 3 Strong positive correlation of body mass (kg) of Indian pangolin with its: A) body length (cm; r2 = 0.89); B) snout length (cm; r2 = 0.93);
and C) ear length (cm; r2 = 0.94) (n = 10). Values presented as mean±SE.

Moreover, its skin is used to make boots and shoes, and its pangolin is highly beneficial to man. The direct economic
body scales are highly prized in traditional Chinese medi- damage caused by termites both to agriculture and build-
cine. Because of its specialized feeding habits, Indian ings must amount to many hundred thousand rupees

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6      N. Irshad et al.: Morpho-anatomy of Indian pangolin

Total body length (cm) Body girth


A 180
160
147.3
140 137
134 137.48
120
118
Ascending level

113
100
92.4
80 76.2
68.58 68.58
60 63.5 66.04 66.04
58
50.8
40 41.6
38.1
30.48
20 25.4
20.32
0
1 2 3 4 5 6 7 8 9 10

Total body length (cm) Snout length


B 180
160
147.3
140
134 137.48 137
120
118
Ascending level

113
100
92.4
80

60 63.5
58
40 41.6

20
3.8 4.8 4.8 5.08 5.58 6.35 8.12
1.9 3.8 4.3
0
1 2 3 4 5 6 7 8 9 10

Total body length (cm) Ear length


C 180
160
147.3
140
134 137.48 137
120
Ascending level

118
113
100
92.4
80
60 63.5
58
40 41.6

20
0.75 1 1 1 1 1 1.5 2 2 2
0
1 2 3 4 5 6 7 8 9 10
Numbers of specimens of Indian pangolin

Figure 4 Strong positive correlation of the body length (cm) of the Indian pangolin with its: A) body girth (cm; r2 = 0.85); B) snout length (cm;
r2 = 0.75); and C) ear length (cm; r2 = 0.77) (n = 10). Values presented as mean±SE.

annually in Pakistan. Unfortunately, Indian pangolin is data on the Indian pangolin and thus its ecology is poorly
often killed when encountered (Roberts 1997). With the known.
exception of a few anecdotal reports found on the Web In the present study, we measured some morpho-
and the information provided by Roberts (1997) about the metrical and anatomical characteristics of the Indian pan-
species in Pakistan, there is a dearth of relevant scientific golin collected from the Potohar Plateau. The maximum

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N. Irshad et al.: Morpho-anatomy of Indian pangolin      7

body weight was found to be up to 20 kg, body length up 0.23  kg. Roberts (1997) reported a newborn Indian pan-
to 147.3  cm and tail length up to 85.7 cm. Roberts (1997) golin weighing 0.45  kg. Lim and Peter (2007) recorded a
reported that females are generally smaller in build than 15-day old African pangolin (Manis javanica) measuring
males, but documented that an exceptionally large male 30–35  cm long, which increased to 43  cm after one and
killed on the road near Kohat weighed as much as 11.3 kg. a half month. Menzies (1967) reported that a new born
Minton (1981) also reported an adult male weighing as Manis tricuspis weighed 0.1 kg at birth. Heath and Vander-
much as 38 lbs (17 kg). In this context, the 20 kg male lip (1988) reported that two individuals of Manis pentada-
reported herein is the heaviest to be documented. cytala weighed 0.09 kg and measured 20 cm in length at
The average head and body length was 58 cm, whereas the time of their birth.
the average tail length was 46 cm with a ratio of 46:54. In
comparison, Prater (1971) and Roberts (1997) reported a
tail-to-body-length ratio of 70:30. The dorsal body surface, References
as well as the fore and hind limbs, of the Indian pangolin
Acharjyo, L.N. and R. Misra. 1972. Birth of an Indian pangolin
were covered over by hard scales. The number of scales
(Manis crassicaudata) in captivity. J. Bomb. Nat. Hist. Soc. 69:
present on the head region differed significantly from that 174–175.
on the trunk (p < 0.01) and tail (p < 0.05) regions. Similarly, CITES. 2000. Proposal 11.3. Transfer of Manis crassicaudata,
significant difference in the number of scales on fore and M. pentadactyla, M. javanica from Appendix II to Appendix I:
hind limbs was found (p < 0.05). The scales on head, trunk CITES.
and tail regions were of different sizes, with those on trunk Doran, G.A. and D.B. Allbrook. 1973. The tongue and associ-
ated structures in two species of African pangolins, Manis
being the largest. On average, size of the scales differed
gigantean and Manis tricuspis. J. Mammal. 54: 887–899.
significantly among the three body regions (p < 0.05). The Heath, M.E. and S.L. Vanderlip. 1988. Biology, husbandry, and
scales on head region were relatively smaller than those veterinary care of captive Chinese pangolins (Manis pentadac-
on the trunk and tail regions, whereas those on fore limbs tyla). Zoo. Biol. 7: 293–312.
were larger than those on hind limbs. These findings are IUCN. 1996. IUCN Red List of Threatened Animals. IUCN, Gland,
Switzerland.
supported by Roberts (1997), but no other published sci-
IUCN. 2004. IUCN Red List of Threatened Species 2014.3. Available
entific data are available for comparison. from <www.iucnredlist.org>. Downloaded on 20 January 2015.
With regard to the anatomical characteristics of the Kaunitz, H.C., C.A. Slanetz, R.E. Johnson and J. Guiman. 1956. Influ-
Indian pangolin, the tongue, which measured 42.5  cm in ence of diet comparison on caloric requirements, water intake
length on average, constituted 37% of the total body length. and organ weights of rats during restricted food intake. J. Nutr.
Roberts (1997) had described tongue of this species as cylin- 60: 221–228.
Krumholz, L.A. 1956. Observations on the fish population of a lake
drical, long and narrow, that can protrude for 25.25 cm (10
contaminated by radioactive wastes. Bull. Am. Museum. Nat.
in). The length of the tongue of other pangolin species is Hist. 110: 283–367.
70 cm in Manis gigantea (Illiger 1815) and 30–66.38 cm in Latimer, H.B. and P.B. Sawin. 1961. Morphogenetic studies of the
M. tricuspis (Rafinesque 1821) (Doran and Allbrook 1973, rabbit XXX. Measurements of the digestive tube and of its parts
Ozegbe et al. 2002). The ratio of weight of various organs in race III rabbits. Anat. Rec. 141: 267–274.
Lim, N.T., L. Peter and K.L. Ng. 2007. Home range, activity cycle
to that of body serves as a practical tool in nutritional and
and natal den usage of a female Sunda pangolin Manis
toxicological studies of animals (Kaunitz et al. 1956, Krum- javanica (Mammalia:Pholidota) in Singapore. Endang. Sp.
holz 1956). These ratios have proved to be a useful param- Res. 3: 1–8.
eter for studies involving laboratory animals (Latimer and Mahmood, T., R. Hussain, N. Irshad, F. Akrim and M.S. Nadeem.
Sawin 1961), but they have not yet been documented for 2012. Illegal mass killing of Indian pangolin (Manis
any wild pangolin species. In the present study, we found crassicaudata) in Potohar region, Pakistan. Pak. J. Zool. 44:
1457–1461.
relative weight of the liver, spleen, heart, lungs and kidneys
Menzies, J.I. 1967. A preliminary note on the birth and development
as 3%, 0.29%–0.37%, 0.5%, 0.1%–0.2% and 0.58%–0.70%, of a small-scaled tree pangolin Manis tricuspis at Ife University
respectively, in relation to total body weight. Zoo. International Zoo Yearbook 7: 114.
One young pangolin captured from the Chakri site Ogilvie, P.W. and D.D. Bridgewater. 1967. Notes on the breeding of
(Rawalpindi district) on December 3, 2011 weighed 0.78 kg an Indian pangolin (Manis crassicaudata) at Oklahoma Zoo.
International Zoo Yearbook 7: 116–118.
and measured 41  cm in length. Ogilvie and Bridgewa-
Ozegbe, P.C., A.O. Ogunsanmi and E.O. Ogunjobi. 2002. Weights
ter (1967) reported a baby Indian pangolin measuring and linear measurements of the body and some organs of the
43.5  cm. Acharjyo and Misra (1972) documented a baby adult male and female African white bellied tree pangolins
pangolin measuring 30  cm in length and weighing Manis tricuspis. Nig. Vet. J. 23: 54–60.

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8      N. Irshad et al.: Morpho-anatomy of Indian pangolin

Pantel, S. and S.Y. Chin. 2008. Proceedings of the workshop on Prater, S.H. 1971. The book of Indian animals, 3rd edition (revised).
trade and conservation of pangolins native to south and south- Bombay Natural History Society, Bombay. pp. 302–303.
east Asia. Singapore Zoo, TRAFFIC Southeast Asia, Petaling Roberts, T.J. 1997. Mammals of Pakistan. Oxford University Press,
Jaya, Selangor, Malaysia. Karachi, Pakistan. pp. 525.

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