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Habitat preference and population estimates of Indian ( crassicaudata) in district of Potohar Plateau,

Article in Russian Journal of Ecology · January 2014 Impact Factor: 0.39 · DOI: 10.1134/S1067413614010081

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All in-text references underlined in blue are linked to publications on ResearchGate, Available from: Tariq Mahmood letting you access and read them immediately. Retrieved on: 21 June 2016 ISSN 10674136, Russian Journal of Ecology, 2014, Vol. 45, No. 1, pp. 70–75. © Pleiades Publishing, Ltd., 2014.

Habitat Preference and Population Estimates of Indian Pangolin (Manis crassicaudata) in District Chakwal of Potohar Plateau, Pakistan1 Tariq Mahmood, Nausheen Irshad, and Riaz Hussain Department of Wildlife Management, PMAS—Arid Agriculture University, , 46300 Pakistan email: [email protected], [email protected] Received October 18, 2012

Abstract—Indian pangolin (Manis crassicaudata) is a fossorial, “Near threatened” mammalian species occurring in Pakistan and facing a risk of endangerment in its wild habitat. Being nocturnal, ecological data of the species is lacking in the country and in south Asia as well. The current study investigated some ecolog ical parameters of the species like, distribution, habitat analysis, population and food habits in district Chak wal of Potohar Plateau. Illegal trapping and killing by professional nomads for its scales is the main threat to the species in the study area.

Keywords: Chakwal, diet, habitat, Indian pangolin, Pakistan, population DOI: 10.1134/S1067413614010081

1 INTRODUCTION information about its ecology and biology including habitat preferences and population estimates. So Pangolin, the “scaly anteater”, has a distinguishing keeping in view the importance of Potohar plateau as characteristic of unique body scales (Aktin, 2004) and an important habitat of the Indian pangolin in the same character is reflected by the name of its order country, the present study assessed its habitat require Pholidota, meaning “the scaled ”. There are ments and population estimates in the study area. seven extant species of pangolin; three occur in Asia (Manis pentadactyla, Manis crassicauduta and Manis javanica) while the remaining four (Manis gigantea, MATERIALS AND METHODS Manis longicaudata, Manis tricuspis and Manis tem minckii) are found in Africa (Emry, 1970). Indian The current study was conducted in district Chak pangolin (Manis crassicaudata) is the only member of wal of Potohar Plateau, that comprises of arid environ Pholidota found in Pakistan. It occurs in and around ment with an average annual rainfall 350–500 mm , and Gujrat districts in the northwest (Quershi et al. 2009). It is bound by Rawalpindi and of the and extends across the into districts in the north, Jhelum in the east, district, and also from upto Mar in the south and in the west. The dan and in the Khyber Pakhtoonkhawah study district includes four smaller administrative (KPK) province. It is also reported from Dadu and units (Tehsils); Chakwal, , Choa Saidan Shah Lerkana districts of , and Mekran and Lasbela and . The total area of the district is districts of Baluchistan (Roberts, 1997). 6609 square kilometers and it lies between 32°56′ north ° ′ Indian pangolin plays vital economic role in the and 72 54 east. food web by feeding upon : a serious insect For determination of the distribution of animal pest of agricultural crops and buildings (Roberts, species in the study area, standard ecological methods 1997). Besides, it is hunted for its flesh, skin and scales (linetransects, field sightings and records of signs) (Nowak, 1991). Despite of great significances, Indian and secondary data collection methods (interviews pangolin is one of the least studied species in the coun with local people and hunters) were employed. Exten try and it faces high risk of extinction in wild habitat sive surveys of the open wild areas of the district were (Wu et al., 2004). Without conservation efforts, its conducted through motor vehicle for presence or population is expected to keep on declining and the absence of animal. Habitat of Indian pangolin was vital species may very soon be lost. For the conserva analyzed at two selected study sites (around Jubair Pur tion of this species, it is mandatory to have baseline and Murreed village) by quantifying trees, shrubs and herbs. The Importance value Index (IVI), for tree spe 1 The article is published in the original. cies was calculated by using “Point Centered Quarter”

70 HABITAT PREFERENCE AND POPULATION ESTIMATES OF INDIAN PANGOLIN 71

33°0′0′′N 2 3 1 6 5 10 7 8 4 11 13 9 12 32°40′0′′N Ch ina

Legend an N st ani fg Study Area Sites WE A Pakistan

Chakwal Distric ia 32°20′0′′N d Iran n S I Decimal Degrees 0 0.15 0.30 0.60

72°0′0′′E 72°20′0′′E 72°40′0′′E 72°0′0′′E 72°20′0′′E

Fig. 1. Map of Pakistan showing location (circle) of the study district Chakwal and distribution of Indian pangolin in the different areas of the study district. Numbers representing the different areas where the animal was found distributed during surveys: 1. Chakwal , 2. Talagang road (M–2), 3. Talagang road, 4. Kallar Kahar road, 5. Bhaun, 6. Jabairpur, 7.Choa Saidan Shah, 8. Sehgal Abad, 9. Kallar kahar, 10. Bhaun Chowk, 11. Zer dam, 12.Basharat Hills, 13. Talagang. method following Cottom and Cartis (1956) while Overall, the animal species was found evenly distrib “Quadrate Method” (Emlen 1956 and Schemnitz uted in probably due to some partic 1980), was used for estimating shrubs and herbs spe ular ecological features which were noticeable includ cies (transect length of 100 m long and 25 m wide on ing firstly, the soil of the area was soft and semisandy either side for tree species, quadrate of 4 × 4 m for and suitable for digging burrows. Secondly, and shrub species and 1 × 1 m for herb species were estab termites colonies were found abundantly in all study lished). The population of Indian pangolin was esti sites which are the main prey items of Indian pangolin. mated at seven selected sites, in the established Thirdly, some water source was definitely present in transects by counts of active living permanent burrows the area in the form of freshwater streams and ponds of the animal (Southwood, 1966 and Begon 1979). where the animal species was recorded. There is little Burrow characteristics like average diameter and known about the natural history of Indian pangolin, depth of both feeding and living burrows were also but records are from various types of tropical forests, recorded. open land, grasslands, in addition to in close proximity to villages (Zoological Survey of India, 1994). Habitat of the Jubairpur site (study site–I) was of RESULTS AND DISCUSSION mixed type, consisting of cultivated lands as well as As shown in distribution map, the animal species is wild areas. A total of six tree species were recorded found uniformly distributed in district Chakwal, with maximum Importance Value Index (IVI) for Aca including all four Tehsils; Chakwal, Kallar kahar, sia nilotica (IVI = 96.61) while least for Eucalyptus Choa saiden Shah and Talagang (Fig. 1). While In species (IVI = 18.93) (Table 1). At study siteII (Mur areas of Tehsil Choa Saiden Shah, especially around reed site), habitat consisted of large cultivated fields and Basharat hills, its occurrence was recorded at high ele some wild area around. Most dominating tree spp. was vations approximately at 2300 ft asl (above seas level). Ziziphus mauritiana having an IVI = 128.60, and least According to Roberts (1997), Indian pangolin is well IVI (12.79) was found for Capparis decidua (Table 1). adapted to desert regions but is locally distributed in Three shrub species were recorded at Jubair pur site Pakistan and it prefers more barren hilly districts. (site–I) where Ziziphus nummularia constituted high It occurs in the subtropical thorn forests of Potohar (60.5) relative cover (Table 1). Whereas, five shrub spe Plateau as well as the Salt Range and extends up to cies occurred at siteII (Murreed) with highest relative 2500 ft elevation in the Rawalpindi foothills. Whereas cover (42.5) for Ziziphus nummularia (Table 1). At Hutton, (1949) had reported the occurrence of JubairPur (site–I), the vegetation cover of seven herb pangolin at the elevation of 2300 m (7545 ft) in India. species was found with Cyprus rotundus having maxi

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Table 1. Density (per ha for trees, per 4 m2 for shrubs and per m2 for herb species), frequency, relative cover and IVI of trees, shrubs and herb species analysed at two selected study sites (Jubairpur and Mureed) in the habitat of Indian pangolin (Manis crassicaudata) in district Chakwal SITEI (Jub airpur) Plant Sr. Relative Relative Relative Tree species Density IVI species No. Density Frequency Cover 1 Ziziphus mauritiana 1.97 25 25 23.63 73.63 Trees 2 Dalbergia sissoo 0.66 10 16.6 9.62 36.2 3 Acasia nilotica 2.96 30 25 41.61 96.61 4 Euclyptus 0.33 5 8.3 5.63 18.93 5 Tamarix aphylla 0.33 10 8.3 9.62 27.92 6 Acasia modesta 1.65 20 16.6 10 46.6 Mean 1.31 ± 0.43 14.2 ± 4.0 16.6 ± 3.02 14.30 ± 5.5 49.9 ± 12 Shrubs 1 Zizyphus nummularia 0.83 54.5 42.8 60.5 157.8 2 Prosopis cimreria 0.66 36.3 32.7 32.7 101.7 3 Calotropis procera 0.33 9.09 21.4 6.6 37.09 Mean 0.60 ± 0.14 33.2 ± 13 32.3 ± 6.17 33.2 ± 15.5 98.8 ± 34.8 1 Alhaji marorum 0.10 21.2 25 21.3 67.5 Herbs 2 Dicaytra roxburghina 0.08 17.02 19.9 18.02 54.9 3 Helitropuim eurapallum 0.04 8.51 9.9 10.5 28.9 4 Carathamus oxycantha 0.02 4.25 4.98 2.5 11.73 5 Amaranthus hybridus 0.05 10.6 9.9 10.8 31.3 6 Tribulus terristris 0.03 6.38 4.98 7.16 18.5 7 Cyprus rotundus 0.15 31.9 25 29.4 86.3 Mean 0.06 ± 0.01 14.2 ± 3.66 14.2 ± 3.35 14.2 ± 3.47 42.74 ± 10.4 SITEII (Mureed) 1 Acacia modesta 0.92 12.56 19.61 21.74 53.91 Trees 2 Ziziphus mauritiana 3.36 45.90 39.22 43.48 128.60 3 Capparis decidua 0.30 4.09 6.53 2.17 12.79 4 Acacia nilotica 2.74 37.43 34.64 32.61 104.8 Mean 1.83 ± 0.72 24.9 ± 1.089 25 ± 9 25 ± 8 62.5 ± 26 Shrubs 1 Ziziphus nummularia 0.1 29.41 30.79 42.5 102.7 2 Lantana camara 0.66 11.76 15.38 12 39.1 3 Prosopis cineraria 0.66 23.53 23.07 22.2 68.8 4 Grawia optiva 0.33 11.76 15.38 12 39.1 5 Dodonaea viscosa 0.33 23.53 15.38 12 50.9 Mean 0.56 ± 0.09 199.99 ± 3.4 20.00 ± 3.04 20.00 ± 5.9 60.13 ± 11.94 Herbs 1 Cynoglosum lancealat 0.05 21 21 19.4 61.4 2 Oenothera rorea 0.04 17.3 14.28 16.95 48.5 3 Amaranthus hybridus 0.04 17.3 14.28 15.25 46.8 4 Chenopodium alleum 0.05 21 28.57 21.46 71.0 5 Trianthema portulcaras 0.03 13.04 14.28 15.5 42.8 6 Avera javanica 0.02 8.69 7.12 11.29 27.1 Mean 0.03 ± 0.02 16.38 ± 1.77 16.58 ± 2.99 16.64 ± 1.42 49.6 ± 6.21

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Table 2. Burrow characteristics and Estimates of population density (/km2) of Indian pangolin (Manis crassicaudata) at seven selected study sites in District Chakwal during 2010–2011 Total number of burrows Area 2 Feeding Average Average average average Study sites (km ) Living burrows Population Burrows, depth, diameter, diameter depth searched Inctive, n active, n Density/h n inches inches (inches) (inches) Chumbi 22314.48 2 111560.010 surla Jubair Pur26128.3219.5620.010 Murreed 2 17 8 8 3 0 10.5 56 0.015 Bauhn 6 19 12 9 4 1 10 56 0.007 Chokora 2 18 8 8 2 0 11.5 54 0.010 Khokar 22012.59.52 312520.010 Zair Dohk Surla 6 29 14.5 9.5 3 0 9.0 56 0.005 Total 22 132 66.9 50.8 18 6 73.5 392 0.067 Mean ± SE 3.14 18.85 ± 2.63 11.0 ± 0.90 8.61 ± 0.26 2.57 ± 0.29 0.85 ± 0.40 10.5 ± 0.35 56.0 ± 1.15 0.010 ± 0.003 mum (29.4) and Tribulus terristris least (7.16) relative were much deeper and less in numbers than those of cover (Table 1). Whereas at Mureed site (siteII), feeding ones. Living burrows were further confirmed among the six herb species recorded Chenopodium for their use by the animal species as categorized either alleum had highest relative cover (21.46) and Avera inactive or active (Table 2). A living burrow was estab javanica (11.29) the lowest value (Table 1). lished as active if any indirect signs of the animal spe Although Indian pangolin is not a tree dweller cies were found around that burrow such as foot prints unlike to some African species but even then trees, on the soil around, scale prints or presence of faecal herbs, and shrubs form important components of its sample around. Similarly, feeding burrows were con habitat. It was especially noticeable that at study siteI firmed by the presence of dead body parts of ants and (Jubairpur) Indian pangolin was closely associated presence of colonies inside the burrows. with Zizyphus mauritiana, Acacia nilotica, Zizyphus Both feeding and living burrows were quantified for nummularia, Prosopis cineraria which indicates that their size, depth and activity (Table 2; Fig. 3). The these plant species were more preferred by Indian average depth of living burrows was 56.0 ± 1.15 inches pangolin for digging burrows around them. Similarly, (n = 24) whereas those of feeding burrows was, at study site–II (Mureed) Lantana camara was also 11.01 ± 0.90 inches (n = 132). The diameters of both among the preferred vegetation type. The tree species feeding and living burrows, on average, were 8.61 ± like Prosopis, Zizyphus and Acacia nilotica may be 0.26 and 10.5 ± 0.35, respectively. Both types of bur important for Indian pangolin from the point of view rows of Indian pangolin had characteristic circular of food provision because abundant termite mounds shape. and ’s colonies were observed on the soil below and Results of burrow characteristics viz. numbers of on the trunks of these tree species. Moreover, Zizyphus burrows, their average depths and diameters, recorded nummularia and Lantana camara may have an impor at seven sites were analysed statistically through stu tant role of providing the protection to the animal spe dent’s paired t–test using the software “Past”. The cies. Very limited published past literature about numbers of feeding burrows at seven selected sites were Indian pangolin does not reflect its habitat require significantly different from those of living permanent ments and such kind of association with certain vege burrows at the same sites (p < 0.001; t– 6.337). The tation types; therefore, this fact is hereby being average diameters of feeding burrows also differed sig reported for the first time. Richer et al. (1997) had nificantly from those of permanent living burrows reported that feeding sites of Indian pangolin may (p <0.01; t = –3.596). Similarly, average depths of include grasses, bare grounds, and bases of trees, feeding burrows were significantly different from those shrubs, roots, leaf litter, fallen logs and even elephant of living burrows (p < 0.001; t = –32.92). dung piles in its habitat. At seven selected sites of the district, average popu The burrows of the animal species were confirmed lation density of Indian pangolin was estimated to be on the basis of their diameter, depth and shape. Two 0.010 ± 0.003/ha (Table 2). Highest density estimates types of burrows were found; feeding burrows and liv were recorded at Mureed site (0.015/ha) while mini ing/permanent burrows. Living or permanent burrows mum (0.005/ha) at Dohk Surla. Reported sightings

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Rd m lu e Murred h J Talagang Rd Chakwal Jubair Pur

Khokar Zair dam

Kallar Kahar

Chumbi Surla Basharat Hills

Choa Sadan Shah

M2

10.36 mi

Study sites Occurance of lndain pangolin

Fig. 2. A satellite image of district Chakwal showing seven selected study sites, Red circles indicating occurrence of Indian pangolin (Manis crassicaudata), (taken and modified from Google Earth).

35 0.10 Living Burrow Feeding Burrow Population Density 0.09 30 3 0.08 25 3 0.07 5 5 0.06 20 2 3 0.05 15 29 0.04 23 10 20 0.03 17 19 18 3 0.015 0.02 5 0.010 0.010 0.010 0.010 6 0.007 0.005 0.02 0 0 Chumbi Surla Murreed Chokora Dohk Surla Jubair Pur Bauhn Khokar Zair

Fig. 3. Population density (per ha) of Indian pangolin (Manis crassicaudata) estimated at selected sites against numbers of feeding and living burrows in the study area.

(n = 5–7 ) and fecal counts (n = 5) were high is concerned, the authors could not find any studies est at Mureed site compared to all other sites (Table 3; depicting the population density of the species, not Fig. 3). only in Pakistan, but in South Asia as well. The species It is not easy to estimate population of Indian is rarely observed due to its secretive, solitary, and noc pangolin in its habitat because of its shy nature and turnal habits, and also not enough research studies nocturnal habit. As far as the past published literature exist on its population density or global population

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(CITES 2000). The Indian pangolin is thought to tional Islamic University , for her kind help occur in small numbers in Bangladesh, where this spe in developing the distribution map of the species in the cies was described as rare in 1986 (Khan 1985). In study area. India, the overall status of the species is not well known (Tikader 1983). This species is relatively uncommon in Pakistan (Roberts, 1997). It is of vari REFERENCES able abundance in Sri Lanka, but nowhere common Atkins, W.A., Pholidota (), in Grzimek’s Ani (Phillips, 1981). Overall, the species is thought to be in mal Life Encyclopedia, vol. 16. Grzimek, B., Kleiman, D.G., significant decline due to hunting for food and medi Geist, V., and McDade, M.C., Eds., Detroit: Thomson cines. The overall population trend is expected to be Gale, 2004. declining (IUCN 2011–12). In this context in the Begon, M., Investigating Animal Abundance, London: Asian region, the population density estimates of the Edward Arnold, 1979. species are pioneer to be reported, in this study, not Cottam, G. and Curtis, J.T., The use of distance measures only from Pakistan but also from India, Sri Lanka and in phytosociological sampling, Ecology, 1956, vol. 37, no. 3, Bangla Desh. pp. 451–460. Emlen, J.T., A method for describing and comparing avian MannWhitney Test” was applied using SPSS 17 to habitats, Ibis, 1956, vol. 98, no. 4, pp. 565–576. test if the vegetation and burrow abundance ranks were Emry, R.J., A North American Oligocene pangolin and statistically different at the two selected study sites. other additions to Pholidota, Bull. Am. Mus. Nat. Hist., The numbers of burrows were rated on an abundance 1970, vol. 142, pp. 459–510. rank scale as 0 (5 burrows and below) and 1 (6 burrows Hutton, A.F., Notes on the Indian pangolin (Manis crassi and above). The vegetation recorded from the two sites caudata), J. Bombay Nat. Hist. Soc.,1949, vol. 48, pp. 805– was categorized into two groups viz. A and B based on 806. burrow ranks. The test yielded a significant difference Nowak, R.M., Walker’s of the World, 6th ed., (p < 0.05) with group A having a high mean rank Baltimore, Md.: Johns Hopkins Univ. Press, 1999, (23.00) as compared to group B (mean rank = 10.50). pp. 642–643. The test confirmed that the animal species preferred to Qureshi, R., Waheed, A., Arshad, M., and Umbreen, T., dig burrows near certain vegetation types such as Zizi Medicoethnobotanical inventory of tehsil Chakwal, Paki phus mauritiana, Acacia nilotica, Zizyphus nummu stan, Pakistan J. Bot., 2009, vol. 41, no. 2, pp. 529–538. laria, Prosopis cineraria, Lantana camara and Acasia Richer, R.A., Coulson, I.M., and Heath, M.E., Foraging modesta. However, the medians of the vegetation den behaviour and ecology of the Cape pangolin (Manis tem sities of the two sites were not significantly different minckii) in northwestern Zimbabwe, Afr. J. Ecol., 1997, (p > 0.05). vol. 35, no. 4, pp. 361–369. The current study also revealed that Indian Roberts, T.J., Mammals of Pakistan, , Pakistan: pangolin was being illegally hunted and killed fre Oxford Univ. Press, 1997. quently in the study area for obtaining its scales. Southwood, T.R.E., Ecological Methods, with Particular Therefore, it is recommended to take immediate con Reference to the Study of Insect Populations, London: Meth servation efforts in the study area to save population of uen, 1966. this vital insectivorous unique animal species. Swart, J.M., Richardson, P.R.K., and Ferguson, J.W.H., Ecological factors affecting the feeding behaviour of pangolins (Manis temminckii), J. Zool. (London), 1999, ACKNOWLEDGMENT vol. 247, no. 3, pp. 281–292. Wu, S.B, Liu, N.F, Ma, G.Z, Xu, Z.R., and Chen, H., The authors are highly grateful to Higher Educa Studies on habitat selection by (Manis tion Commission (HEC) Islamabad, Pakistan for pro pentadactyla) in winter in Dawuling Natural Reserve, Acta viding financial support for this research work. We are Ecol. Sinica, vol. 23, no. 6, pp. 1079–1086. also grateful to Dr. Syeda Maria Ali, Assistant Profes Zoological Survey of India, ENVIS Newsl., 2002, vol. 9, sor, Department of Environmental Sciences, Interna pp. 1–2.

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