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Morphometric analysis and roosting ecology of bat species Pteropus Medius in Mansehra, Khyber Pakhtunkhwa, Pakistan

Análise morfométrica e ecologia de poleiro de espécies de morcegos Pteropus Medius em Mansehra, Khyber Pakhtunkhwa, Paquistão

Abstract

Morphometric measurement and roosting ecology of Pteropus medius were aimed to find out in Mansehra district of KP, Pakistan. Total 3149 numbers of bats were found in eight biological spots visited; Baffa Doraha, Darband, Dadar, Jallu, Hazara University, Garhi Habibullah Chattar Plain and Jabori, in total 299 numbers of different species of trees including; Morus alba, Pinus raxburghi, Eucalyptus camaldulensis, Morus nigra, Grevillea robusta, Brousonetia papyrifera, Platanus orientalis, Ailanthus altissima, Hevea brasiliensis and Populus nigra. Morphometric features were measured and found vary according to sex of the bats. The average wing span, wing`s length from tip of wing to neck, from thumb to tip of wing and the body`s length from head and claws were recorded to be 102.98 cm, 49.07cm, 28.7 cm and 22.78 cm respectively in males while 93.67 cm, 44.83cm, 24.78cm and 22.78 cm respectively in female bats. Mean circumference of the body including wings and without wing were measured as 22.78 cm and 17.29 cm in males and that of female were 20.07 cm and 16.9 cm. Average length of thumb 3.64 cm, ear`s length 3.1 cm, snout 5.62cm, eye length were 1.07 cm for both sexes and length between the feet in extended position were16.3 cm. Generally different measurement of males bodies were found to be greater than female such as mean body surface area, mass, volume and pressure were found to be 2691.79 cm2, 855.7gm,1236.4 ml and 295.77 dyne/cm3for male and 2576.46 cm2, 852.71gm,1207 ml and 290.2 dyne/cm3 respectively for female. While weight and density for both males and females bats were same with mean of 8.59 newton and 0.701 g/m3. Findings of current reports can add valued information in literature about bats, which can be used for species identification and conservation.

Keywords:
Pteropus medius; roosting trees; morphometric analysis; Pakistan

Resumo

A medição morfométrica e a ecologia de poleiro de Pteropus medius foram realizadas no distrito de Mansehra de KP, Paquistão. Foram encontrados 3.149 morcegos em 8 pontos biológicos visitados; Baffa Doraha, Darband, Dadar, Jallu, Universidade Hazara, Garhi Habibullah Chattar Plain e Jabori, no total 299 números de diferentes espécies de árvores, incluindo: Morus alba, Pinus raxburghi, Eucalyptus camaldulensis, Morus nigra, Grevillea robusta, Brousonetia papyrifera, Platanus orientalis, Ailanthus altissima, Hevea brasiliensis e Populus nigra. As características morfométricas foram medidas e variam de acordo com o sexo dos morcegos. A envergadura média da asa, o comprimento da asa da ponta da asa ao pescoço, do polegar à ponta da asa e o comprimento do corpo da cabeça e garras foram registrados em 102,98 cm, 49,07 cm, 28,7 cm e 22,78 cm, respectivamente, nos machos. Enquanto 93,67 cm, 44,83 cm, 24,78 cm e 22,78 cm respectivamente, nas fêmeas. As circunferências médias do corpo incluindo asas e sem asas foram medidas de 22,78 cm e 17,29 cm nos machos e as das fêmeas foram 20,07 cm e 16,9 cm. O comprimento médio do polegar 3,64 cm, comprimento da orelha 3,1 cm, focinho 5,62 cm, comprimento dos olhos 1,07 cm para ambos os sexos e comprimento entre os pés em posição estendida foi de 16,3 cm. Geralmente, as medidas diferentes dos corpos masculinos foram maiores que as femininas, como a área de superfície corporal média, massa, volume e pressão foram encontrados em 2691,79 cm2, 855,7 gm,1236,4 ml e 295,77 dines para masculino e 2576,46 cm2, 852,71 gm, 1207 ml e 290,2 dines respectivamente para fêmeas. Enquanto o peso e a densidade para machos e fêmeas de morcegos foram os mesmos com média de 8,59 N e 0,701 g/m3. Os achados de relatórios atuais podem agregar informações valiosas na literatura sobre morcegos, que podem ser utilizadas para identificação e conservação de espécies.

Palavras-chave:
Pteropus medius; árvores empoleiradas; análise morfométrica; Paquistão

1. Introduction

Vertebrate diversity is severely affected due to increased anthropogenic activities in aquatic and terrestrial habitats. Ecosystem changes result in changes to the habitats of species (Hassan et al., 2021aHASSAN, H., ALI, Q.M., AHMAD, N., MASOOD, Z., HOSSAIN, M.Y., GABOL, K., KHAN, W., HUSSAIN, M., ALI, A., ATTAULLAH, M. and KAMAL, M., 2021a. Assessment of growth characteristics, the survival rate and body composition of Asian Sea bass Lates calcarifer (Bloch, 1790) under different feeding rates in closed aquaculture system. Saudi Journal of Biological Sciences, vol. 28, no. 2, pp. 1324-1330. http://dx.doi.org/10.1016/j.sjbs.2020.11.056. PMid:33613062.
http://dx.doi.org/10.1016/j.sjbs.2020.11...
, bHASSAN, H.U., ALI, Q.M., KHAN, W., MASOOD, Z., ABDEL-AZIZ, M.F.A., SHAH, M.I.A., GABOL, K., WATTOO, J., MAHMOOD CHATTA, A., KAMAL, M., ZULFIQAR, T. and HOSSAIN, M.Y., 2021b. AEffect of feeding frequency as a rearing system on biological performance, survival, body chemical composition and economic efficiency of Asian seabass Lates calcarifer (Bloch, 1790) reared under controlled environmental condition. Saudi Journal of Biological Sciences, vol. 28, no. 12, pp. 7360-7366. http://dx.doi.org/10.1016/j.sjbs.2021.08.031. PMid:34867038.
http://dx.doi.org/10.1016/j.sjbs.2021.08...
). The biological diversity of each ecosystem depends on the ecological services delivered (Hassan et al., 2023HASSAN, H.U., MAHBOOB, S., MASOOD, Z., RIAZ, M.N., RIZWAN, S., AL-MISNE, F., ABDEL-AZIZ, M.F.A., AL-GHANIM, K.A., GABOL, K., CHATTA, A.M., KHAN, N.A., SAEED and WAQAR, M., 2023. Biodiversity of commercially important finfish species caught by mid-water and bottom trawls from two different coasts of Arabian Sea: threats and conservation strategies. Brazilian Journal of Biology = Revista Brasileira de Biologia, vol. 83, pp. e249211. http://dx.doi.org/10.1590/1519-6984.249211.
http://dx.doi.org/10.1590/1519-6984.2492...
). Chiropteran are different from all other mammals which have wings, make them able for flight freely, and are second major mammalian order after rodents, and are diverse enough almost 1,232 species of bats are known which contribute to one fourth of 5,487 total mammal and contribute 20% out of total wild animals. Pakistan's ecosystems contain a broad variety of life and wealthy natural habitats (Hassan et al., 2020HASSAN, H.U., ALI, Q.M., AHMAD, N., ATTAULLAH, M., CHATTA, A.M., FAROOQ, U. and ALI, A., 2020. Study of vertebrate diversity and associated threats in selected habitats of Sindh and Balochistan, Pakistan. International Journal of Biology and Biotechnology, vol. 17, pp. 163-175.). In Pakistan bats comprise about one fourth of the known mammalian species which comprise 50 species with 26 genera and 8 families (Roberts, 1997ROBERTS, T.J., 1997. The Mammals of Pakistan. New York: Oxford University Press.; Simmons, 2005SIMMONS, N.B., 2005. Chiroptera. In: K. D. ROSE and J. D. ARCHIBALD, eds. The rise of placental mammals. Baltimore: Johns Hopkins University Press, pp. 159-174.; Simmons, 2010SIMMONS, N.B., 2010. Personal communication. New York: American Museum of Natural History.; Schipper et al., 2008SCHIPPER, J., CHANSON, J.S., CHIOZZA, F., COX, N.A., HOFFMANN, M., KATARIYA, V., LAMOREUX, J., RODRIGUES, A.S., STUART, S.N., TEMPLE, H.J., BAILLIE, J., BOITANI, L., LACHER JUNIOR, T.E., MITTERMEIER, R.A., SMITH, A.T., ABSOLON, D., AGUIAR, J.M., AMORI, G., BAKKOUR, N., BALDI, R., BERRIDGE, R.J., BIELBY, J., BLACK, P.A., BLANC, J.J., BROOKS, T.M., BURTON, J.A., BUTYNSKI, T.M., CATULLO, G., CHAPMAN, R., COKELISS, Z., COLLEN, B., CONROY, J., COOKE, J.G., FONSECA, G.A., DEROCHER, A.E., DUBLIN, H.T., DUCKWORTH, J.W., EMMONS, L., EMSLIE, R.H., FESTA-BIANCHET, M., FOSTER, M., FOSTER, S., GARSHELIS, D.L., GATES, C., GIMENEZ-DIXON, M., GONZALEZ, S., GONZALEZ-MAYA, J.F., GOOD, T.C., HAMMERSON, G., HAMMOND, P.S., HAPPOLD, D., HAPPOLD, M., HARE, J., HARRIS, R.B., HAWKINS, C.E., HAYWOOD, M., HEANEY, L.R., HEDGES, S., HELGEN, K.M., HILTON-TAYLOR, C., HUSSAIN, S.A., ISHII, N., JEFFERSON, T.A., JENKINS, R.K., JOHNSTON, C.H., KEITH, M., KINGDON, J., KNOX, D.H., KOVACS, K.M., LANGHAMMER, P., LEUS, K., LEWISON, R., LICHTENSTEIN, G., LOWRY, L.F., MACAVOY, Z., MACE, G.M., MALLON, D.P., MASI, M., MCKNIGHT, M.W., MEDELLÍN, R.A., MEDICI, P., MILLS, G., MOEHLMAN, P.D., MOLUR, S., MORA, A., NOWELL, K., OATES, J.F., OLECH, W., OLIVER, W.R., OPREA, M., PATTERSON, B.D., PERRIN, W.F., POLIDORO, B.A., POLLOCK, C., POWEL, A., PROTAS, Y., RACEY, P., RAGLE, J., RAMANI, P., RATHBUN, G., REEVES, R.R., REILLY, S.B., REYNOLDS III, J.E., RONDININI, C., ROSELL-AMBAL, R.G., RULLI, M., RYLANDS, A.B., SAVINI, S., SCHANK, C.J., SECHREST, W., SELF-SULLIVAN, C., SHOEMAKER, A., SILLERO-ZUBIRI, C., SILVA, N., SMITH, D.E., SRINIVASULU, C., STEPHENSON, P.J., VAN STRIEN, N., TALUKDAR, B.K., TAYLOR, B.L., TIMMINS, R., TIRIRA, D.G., TOGNELLI, M.F., TSYTSULINA, K., VEIGA, L.M., VIÉ, J.C., WILLIAMSON, E.A., WYATT, S.A., XIE, Y. and YOUNG, B.E., 2008. The status of the world’s land and marine mammals: diversity, threat, and knowledge. Science, vol. 322, no. 5899, pp. 225-230. http://dx.doi.org/10.1126/science.1165115. PMid:18845749.
http://dx.doi.org/10.1126/science.116511...
; Kunz et al., 2011KUNZ, T.H., BRAUN DE TORREZ, E., BAUER, D., LOBOVA, T. and FLEMING, T.H., 2011. Ecosystem services provided by bats. Annals of the New York Academy of Sciences, vol. 1223, no. 1, pp. 1-38. http://dx.doi.org/10.1111/j.1749-6632.2011.06004.x. PMid:21449963.
http://dx.doi.org/10.1111/j.1749-6632.20...
). In Indian subcontinent 119 bats species have been reported (Bates and Harrison, 1997BATES, P.J.J. and HARRISON, D.L., 1997. Bats of the Indian subcontinent. Sevenoaks: Harrison Zoological Museum, 258 p.). Among which the contribution of bats from Pakistan are 56 species (Mahmood-ul-Hassan et al., 2009MAHMOOD-UL-HASSAN, M., JONES, M.G. and DIETZ, C., 2009. The bats of Pakistan, the least known creature. Muller: Verlag. 168 p.). Bats were adapted to access to a varity territories, having most climatic zones and earthbound land types, it's feeding on fruit, leaves, nectar, flowers, fish, blood, small mammals, and insects but the majority are feeding on insects (Schnitzler and Kalko, 2001SCHNITZLER, H.U. and KALKO, E.K., 2001. Echolocation by insect-eating bats: we define four distinct functional groups of bats and find differences in signal structure that correlate with the typical echolocation tasks faced by each group. Bioscience, vol. 51, no. 7, pp. 557-569. http://dx.doi.org/10.1641/0006-3568(2001)051[0557:EBIEB]2.0.CO;2.
http://dx.doi.org/10.1641/0006-3568(2001...
). Pteropus medius (Indian flying fox) have accommodated in sub order megachiroptera in the family Pteropodidae which live in colonial form in trees that keep them safe from various dangers (Richmond et al., 1998RICHMOND, J.Q., BANACK, S.A. and GRANT, G.S., 1998. Comparative analysis of wing morphology, flight behaviour, and habitat use in flying foxes (Genus: pteropus). Australian Journal of Zoology, vol. 46, no. 3, pp. 283-289. http://dx.doi.org/10.1071/ZO97059.
http://dx.doi.org/10.1071/ZO97059...
; Cheke and Dahl, 1981CHEKE, A.S. and DAHL, J.F., 1981. The status of bats on western Indian Ocean islands, with special reference to Pteropus. Mammalia, vol. 45, no. 2, pp. 205-238. http://dx.doi.org/10.1515/mamm.1981.45.2.205.
http://dx.doi.org/10.1515/mamm.1981.45.2...
; Rainey and Pierson, 1992RAINEY, W.E. and PIERSON, E.D., 1992. Distribution of Pacific island flying foxes. In: D.E. WILSON and G.L. GRAHAM, eds. Pacific Island flying foxes: proceedings of an international conservation conference. Washington, DC: US Department of the Interior, Fish and Wildlife Service, Biological Report, pp. 111-122.). These Indian fruit bat have been reported to be inhabitants of trees such as Acacia species, Ficus, Bauhinia, Tamarindus indica and Casurina Samanea saman species (Chakravarthy et al., 2009CHAKRAVARTHY, A.K., YESHWANTH, H.M., KUMAR, L.V. and KUMAR, N.P., 2009. Giant Indian fruit bat (Pteropus giganteus Brunnich) roost in Karnataka, south India: a case for preservation as a heritage site. Tiger Paper, vol. 36, pp. 25-30.). While in Pakistan these are reported in trees like Ficus bengalensis and Broussonetia papyifers (Roberts, 1977). The habitat preference depends on factors such as secure from predators, environmental stresses and resource availabilities (Kunz, 1982KUNZ, T.H., 1982. Ecology of bats. Boston: Springer. Roosting ecology of bats, pp. 1-55. http://dx.doi.org/10.1007/978-1-4613-3421-7_1.
http://dx.doi.org/10.1007/978-1-4613-342...
). They use special unique sense echolocations to locate their niche and preys etc. (Schnitzler et al., 2003SCHNITZLER, H.-U., MOSS, C.F. and DENZINGER, A., 2003. From spatial orientation to food acquisition in echolocating bats. Trends in Ecology & Evolution, vol. 18, no. 8, pp. 386-394. http://dx.doi.org/10.1016/S0169-5347(03)00185-X.
http://dx.doi.org/10.1016/S0169-5347(03)...
). Bats play important role in ecosystem such as regenerations of forest and maintain plants populations’ structure and distribution as well as in food chain (Heithaus et al., 1975HEITHAUS, E.R., FLEMING, T.H. and OPLER, P.A., 1975. Foraging patterns and resource utilization in seven species of bats in a seasonal tropical forest. Ecology, vol. 56, no. 4, pp. 841-854. http://dx.doi.org/10.2307/1936295.
http://dx.doi.org/10.2307/1936295...
; Fleming et al., 1998FLEMING, T.H., NELSON, A.A. and DALTON, V.M., 1998. Roosting behavior of the lesser long-nosed bat, Leptonycteris curasoae. Journal of Mammalogy, vol. 79, no. 1, pp. 147-155. http://dx.doi.org/10.2307/1382849.
http://dx.doi.org/10.2307/1382849...
; Estrada et al., 1993ESTRADA, A., COATES‐ESTRADA, R. and MERITT JUNIOR, D., 1993. Bat species richness and abundance in tropical rain forest fragments and in agricultural habitats at Los Tuxtlas, Mexico. Ecography, vol. 16, no. 4, pp. 309-318. http://dx.doi.org/10.1111/j.1600-0587.1993.tb00220.x.
http://dx.doi.org/10.1111/j.1600-0587.19...
).

Humans’ activities badly affect biodiversity at all level. Degradation of habitat mostly brought many bat species to the side of extinction. Monitoring of bats for long time is thus necessary to know the negative impact of human on the diversity of bats all over the world (Meyer et al., 2010MEYER, C.F.J., AGUIAR, L.M.S., AGUIRRE, L.F., BAUMGARTEN, J., CLARKE, F.M., COSSON, J., VILLEGAS, S.E., FAHR, J., FARIA, D., FUREY, N., HENRY, M., HODGKISON, R., JENKINS, R.K.B., JUNG, K.G., KINGSTON, T., KUNZ, T.H., GONZALEZ, M.C.M., MOYA, I., PONS, J., RACEY, P.A., REX, K., SAMPAIO, E.M., STONER, K.E., VOIGT, C.C., VON STADEN, D., WEISE, C.D. and KALKO, E.K.V., 2010. Long-term monitoring of tropical bats for anthropogenic impact assessment: gauging the statistical power to detect population change. Biological Conservation, vol. 143, no. 11, pp. 2797-2807. http://dx.doi.org/10.1016/j.biocon.2010.07.029.
http://dx.doi.org/10.1016/j.biocon.2010....
). Unluckily 8 species of bats have gone through extinction, and among which of bats which feed on fruits are at high risk (Clawson, 2002CLAWSON, R.L., 2002. Trends in population size and current status. In: A. KURTA and J. KENNEDY, eds. The Indiana bat: biology and management of an endangered species. Austin: Bat Conservation International, pp. 2-8.). As human population increased deforestation occur for agricultural and housing purposes have vanished roosting sites of these bats (Mickleburgh et al., 2002MICKLEBURGH, S.P., HUTSON, A.M. and RACEY, P.A., 2002. A review of the global conservation status of bats. Oryx, vol. 36, no. 1, pp. 18-34. http://dx.doi.org/10.1017/S0030605302000054.
http://dx.doi.org/10.1017/S0030605302000...
; Fujita and Tuttle, 1991FUJITA, M.S. and TUTTLE, M.D., 1991. Flying foxes (Chiroptera: Pteropodidae): threatened animals of key ecological and economic importance. Conservation Biology, vol. 5, no. 4, pp. 455-463. http://dx.doi.org/10.1111/j.1523-1739.1991.tb00352.x.
http://dx.doi.org/10.1111/j.1523-1739.19...
; Mildenstein et al., 2005MILDENSTEIN, T.L., STIER, S.C., NUEVO-DIEGO, C.E. and MILLS, L.S., 2005. Habitat selection of endangered and endemic large flying-foxes in Subic Bay, Philippines. Biological Conservation, vol. 126, no. 1, pp. 93-102. http://dx.doi.org/10.1016/j.biocon.2005.05.001.
http://dx.doi.org/10.1016/j.biocon.2005....
). In Pakistan less attention has been given to conservation of bars (Butt and Beg, 2001BUTT, A. and BEG, M.A., 2001. Description of two new species of spiders of the families Clubionidae and Oxyopidae from Pakistan. Pakistan Journal of Zoology, vol. 33, no. 1, pp. 35-38.). The correct identification of these species is key step to conserve them. In the world, scientists use many approaches and processes to identify different species of bats. Now advanced method are advised to differentiate species with same morphological characters on the basis of variations in their phylogeny (Russo et al., 2006RUSSO, I.R.M., CHIMIMBA, C.T. and BLOOMER, P., 2006. Mitochondrial DNA differentiation between two species of Aethomys (Rodentia: Muridae) from southern Africa. Journal of Mammalogy, vol. 87, no. 3, pp. 545-553. http://dx.doi.org/10.1644/05-MAMM-A-222R3.1.
http://dx.doi.org/10.1644/05-MAMM-A-222R...
), but theses equipment are of high price to be purchased in many developing countries. Therefore bat zoologists in most part of the world use classical morphological traits and behaviour of bats to identify them (Nagorsen and Brigham, 1993NAGORSEN, D.W. and BRIGHAM, R.M., 1993. The bats of British Columbia. Vancouver: UBC Press. 164 p.; Harris, 1974HARRIS, A.H., 1974. Myotis yumanensis in interior southwestern North America with comments on Myotis lucifugus. Journal of Mammalogy, vol. 55, no. 3, pp. 589-607. http://dx.doi.org/10.2307/1379548.
http://dx.doi.org/10.2307/1379548...
). Among which factors such as skull biometry are also used for identifications (Hill and Smith, 1984HILL, J. and SMITH, J., 1984. Bats: a natural history. Austin: University of Texas Press.; Jacobs et al., 2006JACOBS, D.S., EICK, G.N., SCHOEMAN, M.C. and MATTHEE, C.A., 2006. Insectivorous bat, Scotophilus dinganii. Journal of Mammalogy, vol. 87, no. 1, pp. 161-170. http://dx.doi.org/10.1644/04-MAMM-A-132R2.1.
http://dx.doi.org/10.1644/04-MAMM-A-132R...
). Identifications keys of chiropteran species are one of the authentic ways to recognize them (Daniel, 2009DANIEL, B.A., 2009. Bat taxonomy and echolocation workshop for researchers at M.K.U. Small Mammal Mail, vol. 1, no. 2, pp. 39-44.; Srinivasulu et al., 2010SRINIVASULU, C., RACEY, P.A. and MISTRY, S., 2010. A key to the bats (Mammalia: Chiroptera) of South Asia. Journal of Threatened Taxa, vol. 2, no. 7, pp. 1001-1076. http://dx.doi.org/10.11609/JoTT.o2352.1001-76.
http://dx.doi.org/10.11609/JoTT.o2352.10...
). Many reports on bats have been published across the globe such as Hutson et al. (2001)HUTSON, A.M., MICKLEBURGH, S.P. and RACEY, P.A., 2001. Microchiropteran bats: global status survey and conservation action plan. Gland: IUCN. IUCN/SSC Action Plans for the Conservation of Biological Diversity. http://dx.doi.org/10.2305/IUCN.CH.2001.SSC-AP.1.en.
http://dx.doi.org/10.2305/IUCN.CH.2001.S...
; Houston et al. (2004)HOUSTON, R.D., BOONMAN, A.M. and JONES, G., 2004. Do echolocation signal parameters restrict bats’ choice of prey? In: J. THOMAS, C. MOSS and M. VATER, eds. Echolocation in bats and dolphins. Chicago: Chicago University Press, pp. 339-345.; Russo et al. (2006)RUSSO, I.R.M., CHIMIMBA, C.T. and BLOOMER, P., 2006. Mitochondrial DNA differentiation between two species of Aethomys (Rodentia: Muridae) from southern Africa. Journal of Mammalogy, vol. 87, no. 3, pp. 545-553. http://dx.doi.org/10.1644/05-MAMM-A-222R3.1.
http://dx.doi.org/10.1644/05-MAMM-A-222R...
; Jacobs et al. (2006)JACOBS, D.S., EICK, G.N., SCHOEMAN, M.C. and MATTHEE, C.A., 2006. Insectivorous bat, Scotophilus dinganii. Journal of Mammalogy, vol. 87, no. 1, pp. 161-170. http://dx.doi.org/10.1644/04-MAMM-A-132R2.1.
http://dx.doi.org/10.1644/04-MAMM-A-132R...
; Weller et al. (2007)WELLER, T.J., SCOTT, S.A., RODHOUSE, T.J., ORMSBEE, P.C. and ZINCK, J.M., 2007. Field identification of the cryptic vespertilionid bats, Myotis lucifugus and M. yumanensis. Acta Chiropterologica, vol. 9, no. 1, pp. 133-147. http://dx.doi.org/10.3161/1733-5329(2007)9[133:FIOTCV]2.0.CO;2.
http://dx.doi.org/10.3161/1733-5329(2007...
; Pereswiet-Soltan (2007)PERESWIET-SOLTAN, A., 2007. Relation between climate and bat fauna in Europe. Travaux du Muséum d’Histoire Naturelle, vol. 50, pp. 505-515.; Kelm et al. (2008)KELM, D.H., WIESNER, K.R. and VON HELVERSEN, O., 2008. Effects of artificial roosts for frugivorous bats on seed dispersal in a Neotropical forest pasture mosaic. Conservation Biology, vol. 22, no. 3, pp. 733-741. http://dx.doi.org/10.1111/j.1523-1739.2008.00925.x. PMid:18445078.
http://dx.doi.org/10.1111/j.1523-1739.20...
; Kalka et al. (2008)KALKA, M.B., SMITH, A.R. and KALKO, E.K., 2008. Bats limit arthropods and herbivory in a tropical forest. Science, vol. 320, no. 5872, p. 71. http://dx.doi.org/10.1126/science.1153352. PMid:18388286.
http://dx.doi.org/10.1126/science.115335...
; Williams-Guillen et al. (2008)WILLIAMS-GUILLÉN, K., PERFECTO, I. and VANDERMEER, J., 2008. Bats limit insects in a neotropical agroforestry system. Science, vol. 320, no. 5872, p. 70. http://dx.doi.org/10.1126/science.1152944. PMid:18388285.
http://dx.doi.org/10.1126/science.115294...
; Whitaker and Karataş (2009)WHITAKER, J.O. and KARATAŞ, A., 2009. Food and feeding habits of some bats from Turkey. Acta Chiropterologica, vol. 11, no. 2, pp. 393-403. http://dx.doi.org/10.3161/150811009X485611.
http://dx.doi.org/10.3161/150811009X4856...
; Srinivasulu et al. (2010)SRINIVASULU, C., RACEY, P.A. and MISTRY, S., 2010. A key to the bats (Mammalia: Chiroptera) of South Asia. Journal of Threatened Taxa, vol. 2, no. 7, pp. 1001-1076. http://dx.doi.org/10.11609/JoTT.o2352.1001-76.
http://dx.doi.org/10.11609/JoTT.o2352.10...
; Ghazali and Dzeverin (2013)GHAZALI, M. and DZEVERIN, I., 2013. Correlations between hardness of food and craniodental traits in nine Myotis species (Chiroptera, Vespertilionidae). Vestnik Zoologii, vol. 47, no. 1, pp. 67-76. http://dx.doi.org/10.2478/vzoo-2013-0006.
http://dx.doi.org/10.2478/vzoo-2013-0006...
; Rummel et al. (2019)RUMMEL, A.D., SWARTZ, S.M. and MARSH, R.L., 2019. Warm bodies, cool wings: regional heterothermy in flying bats. Biology Letters, vol. 15, no. 9, p. 20190530. http://dx.doi.org/10.1098/rsbl.2019.0530. PMid:31506035.
http://dx.doi.org/10.1098/rsbl.2019.0530...
; Anderson and Ruxton (2020)ANDERSON, S.C. and RUXTON, G.D., 2020. The evolution of flight in bats: a novel hypothesis. Mammal Review, vol. 50, no. 4, pp. 426-439. http://dx.doi.org/10.1111/mam.12211.
http://dx.doi.org/10.1111/mam.12211...
; MacCraken et al. (2021)MACCRAKEN, G.F., LEE, Y.F., GILLAM, E.H., FRICK, W. and KRAUEL, J. 2021. Bats flying at high altitudes. In: B.K. LIM, M.B. FENTON, R.M. BRIGHAM, S. MISTRY, A. KURTA, E.H. GILLAM, A. RUSSELL and J. ORTEGA, eds. 50 years of bat research. Cham: Springer, pp. 189-205. http://dx.doi.org/10.1007/978-3-030-54727-1_12.
http://dx.doi.org/10.1007/978-3-030-5472...
. But, no proper consideration has been offered towards bats and few reports are available on this regards from the northwestern part of Pakistan which is the habitat of many numbers of species of animals. Current study can be value addition to present literature on bats as current site of study have divers species of Bats which need exploration.

2. Material and Method

2.1. Study area

Current study was carried out in Mansehra (34.3313°N, 73.1980°E) district of PK (Pakhtunkhwa), Pakistan. Where Eight (n=8) biological spots were visited to check different sites that where could be find communities of bats.

2.2. Data collection

Net and slingshots were used to capture bats samples (Pteropus medius) from eight selected sites. All the safety steps were followed and transported to parasitology laboratory, Department of Zoology, Hazara University, Khyber Pakhtunkhwa, Pakistan for further morphometric analysis.

2.3. Morphometric analysis

The bats samples were anaesthetized with the help of chloroform and killed in vacuum chamber. Bats were fitted on white sheets with help of paper pins and the body parts such as width, and length as well as circumference was measured with scale. While body mass were calculated by digital scales. To get volume of each specimen of bats graduated cylinder were used and other parameter such as pressure, weight and density were evaluated through chemical formulae;

Pressure p = w/A, where (w) are the weight of bats and (A) area.

Density D = m/V, (m) are the mass of bats and (V) is volume

Weight W = mg, (m) are mass and g gravitational acceleration

2.4. Roosting site analysis

Different roosting sites and trees species were noted in each biological site and direct roost calculation method were used for Pteropus medius colonies calculation (Rodríguez-Herrera et al., 2008RODRÍGUEZ-HERRERA, B., MEDELLÍN, R.A. and GAMBA-RIOS, M., 2008. Roosting requirements of white tent-making bat Ectophylla alba (Chiroptera: phyllostomidae). Acta Chiropterologica, vol. 10, no. 1, pp. 89-95. http://dx.doi.org/10.3161/150811008X331126.
http://dx.doi.org/10.3161/150811008X3311...
).

2.5. Statistical analysis

Descriptive statistics, ANOVA and Pearson correlation were applied to measure mean variances and correlation, previous verification of normal distribution and variance homogeneity (Zar, 1999ZAR, J.H., 1999. Biostatistical analysis. Upper Saddle River: Prentice Hall Inc. 661 p.) by using SPSS 18, and ORIGIN PRO 9.0 for graphing.

3. Results

3.1. Morphometric profile

Morphometric measurement of the current study showed that generally size of different body part of male bats is larger than that of female bats. The average measurements in males bats were recorded to be wing span (102.98 cm), wing`s length from tip of wing to neck (49.07cm), from thumb to tip of wing (28.7 cm) and the body`s length from head and claws (22.78 cm). While 93.67cm, 44.83cm, 24.78cm and 22.78cm respectively in female bats. Mean circumference of the male body including wings were 22.78 cm and without wing were measured as 17.29 cm. While these measurement in female bats were 20.07 cm and 16.9 cm respectively. In the same way mean body surface area, mass, volume and pressure in male bats were found to be 2691.79 cm2, 855.7gm, 1236.4 ml and 295.77 dyne/cm3respectively. While these measurement in female bats were measured as body surface area 2576.46 cm2, mass 852.71gm, volume 1207 ml and pressure 290.2 dyne/cm3. However some measurements were same in both sexes and found exactly equal in length such as average lengths of thumb 3.64 cm, snout 5.62cm, ear`s length 3.1 cm, length between the feet in extended position 16.3cm while eye length were found to be 1.07 cm. Weight and density for both males and females bats were also same with mean of 8.59 newton and 0.701 g/m3 respectively (Tables 1-2).

Table 1
Mean of different morphometric analysis for both sexes.
Table 2
Mean of mass, weight and other parameter of both male and female bats.

3.2. Roosting trees

Total 299 roosting trees were counted containing bats colonies at all sites, related to different families including; Proteaceae, Salicaceae, Platanaceae, Myrtaceae, Simaroubaceae, Pinaceae, Euphorbiaceae and Moraceae. The species were; Platanus orientalis, Hevea brasiliensis, Pinus raxburghi, Populus nigra, Ailanthus altissima, Morus alba, Brousonetia papyrifera, Grevillea robusta, Morus nigra, Eucalyptus camaldulensis. Different sites had different numbers and different types of trees. Total numbers and types of trees at each biological spot were; Baffa Doraha n=73 (Platanus orientalis n=6, Populus nigra n=47, Eucalyptus camaldulensis n=7, Grevillea robusta n=13) and in 2nd site Garhi Habibullah n=45 (Pinus raxburghi n=11, Populus nigra n=31, Ailanthus altissima n=3). At 3rd site Darband the tree numbers and types were n=23 trees (Grevillea robusta n=6, Hevea brasiliensis n=4, Pinus raxburghi n=13). While at 4th site Chattar plain counted trees were n=41 trees (Ailanthus altissima n=2, Morus alba n=6, Platanus orientalis n=17, Morus nigra n=4, Brousonetia papyrifera n=3, Eucalyptus camaldulensis n=9,). And at 5th site Dadar n=34 trees (Grevillea robusta n=7, Eucalyptus camaldulensis n=12, Pinus raxburghii n=15). 6th site Jabori n=33 (Pinus raxburghi n=16, Populus nigra n=11, Morus alba n=6). And 7th Jallu numbers of trees were n=30 (Hevea brasiliensis n=21, Melia azedarac n=9). While at 8th biological site Hazara University trees counts were n=20 (Eucalyptus camaldulensis n=13, Pinus raxburghii n=7) (Table 3).

Table 3
Number and types of different roosting trees at each site.

3.3. Bats colonies

Mean count of bat colonies were counted to be 118.22 ± 73.50 with maximum count at Baffa Doraha with mean 277 ± 94.08 and minimum count of 58 ± 52.52 at Chattar plain. Over all descending pattern of means of bats colonies were Baffa Doraha (277 ± 94.08) > Ghari Habibullah (171 ± 86.94) > Dadar (117.33 ± 71.39) > Darband (94.67± 38.3) > Jabori (88.33 ± 62.17) > Jallu (75 ± 39.59) > Hazara University (64.5 ± 38.89) > Chattar plain (58 ± 52.52) (Figure 1).

Figure 1
Mean of bats at different biological site.

3.4. Statistical results

There were no statistically significant difference among mean of bats colonies at all biological site as the result of one way anova showed that P > 0.05 (P=0.833). From this result we may predict that bats have no sites preference according to current data. However these bats colonies were dependent on trees numbers and were strong positive correlated with numbers of trees present at each site (r = 0.930, p =0.000).Which means that numbers of trees have direct impacts on bats colonies. In other words high numbers of trees in biological spots would have high numbers of colonies according to correlation result of current study. Furthermore the result of correspondence analysis showed that bats prefer to roost on Populus nigra as maximum colonies were found on tree species Populus nigra (Tables 4-5).

Table 4
Non-significant differences among the means of bats at each site.
Table 5
Correlation between numbers of trees and bat colonies at all sites.

4. Discussion

Identification of bats specimen and different biometrical features were measured through externally morphological analysis (Jacobs et al., 2006JACOBS, D.S., EICK, G.N., SCHOEMAN, M.C. and MATTHEE, C.A., 2006. Insectivorous bat, Scotophilus dinganii. Journal of Mammalogy, vol. 87, no. 1, pp. 161-170. http://dx.doi.org/10.1644/04-MAMM-A-132R2.1.
http://dx.doi.org/10.1644/04-MAMM-A-132R...
; Hill and Smith, 1985HILL, J.E. and SMITH, J.D., 1985. Bats: a natural history. London: British Museum.). The average wing span of male bats were found to be 102.98 cm and 93.67 cm in female in current study as compared to previously published reports such as Simmons (2005)SIMMONS, N.B., 2005. Chiroptera. In: K. D. ROSE and J. D. ARCHIBALD, eds. The rise of placental mammals. Baltimore: Johns Hopkins University Press, pp. 159-174. where the wingspan was 884±18.17 mm of the killed P. medius. Wing span have been reported in range of 112.58 ±1.90 cm (Khan et al., 2021KHAN, W., NISA, N.N., KHAN, A.R., RAHBAR, B., MEHMOOD, S.A., AHMED, S., KAMAL, M., SHAH, M., RASOOL, A., PAHANWAR, W.A., ULLAH, I. and KHAN, S., 2021. Roosting ecology and morphometric analysis of Pteropus medius (Indian flying fox) in Lower Dir, district, Pakistan. Brazilian Journal of Biology = Revista Brasileira de Biologia, vol. 81, no. 1, pp. 77-82. http://dx.doi.org/10.1590/1519-6984.221935. PMid:32401851.
http://dx.doi.org/10.1590/1519-6984.2219...
). Thumbs have been reported for adhering to trees as similar opinion was assumed by (Bennett, 1993BENNETT, M.B., 1993. Structural modifications involved in the fore‐and hind limb grip of some flying foxes (Chiroptera: pteropodidae). Journal of Zoology, vol. 229, no. 2, pp. 237-248. http://dx.doi.org/10.1111/j.1469-7998.1993.tb02633.x.
http://dx.doi.org/10.1111/j.1469-7998.19...
). Furthermore, other measurements of the current study such as length of snout 5.62 cm, ear were 3.1 cm, length amid the feet 16.3 cm in stretched position and length of eye were 1.07 cm. The possible reason behind the difference among current morphometric measurements with other published reports may be due to body size, age and sex of the bats. As many published reports have showed, generally male bat of species P. medius are larger in size as compared to female bats (Khan et al., 2021KHAN, W., NISA, N.N., KHAN, A.R., RAHBAR, B., MEHMOOD, S.A., AHMED, S., KAMAL, M., SHAH, M., RASOOL, A., PAHANWAR, W.A., ULLAH, I. and KHAN, S., 2021. Roosting ecology and morphometric analysis of Pteropus medius (Indian flying fox) in Lower Dir, district, Pakistan. Brazilian Journal of Biology = Revista Brasileira de Biologia, vol. 81, no. 1, pp. 77-82. http://dx.doi.org/10.1590/1519-6984.221935. PMid:32401851.
http://dx.doi.org/10.1590/1519-6984.2219...
; Marimuthu et al., 1998MARIMUTHU, G., RAJAN, K.E., KOILRAJ, A.J., ISAAC, S.S. and BALASINGH, J., 1998. Observations on the foraging behavior of a tent roosting megachiropteran bat Cynopterus sphinx. Biotropica, vol. 30, no. 2, pp. 321-324. http://dx.doi.org/10.1111/j.1744-7429.1998.tb00066.x.
http://dx.doi.org/10.1111/j.1744-7429.19...
; Thatcher, 2004THATCHER, O., 2004 [viewed 19 October 2004]. Fruit and nectar bat biology [online]. Lubee Bat Conservacy. Available from: http://www.lubee.org/about-biology.aspx
http://www.lubee.org/about-biology.aspx...
). However, Surface areas of bats in present study were 295.77 cm2 for both sexes. Many reports have been showed that Surface areas of bats may be varied according to sex, as body surface areas were reported by Kumar et al. (2016)KUMAR, S., STECHER, G. and TAMURA, K., 2016. MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Molecular Biology and Evolution, vol. 33, no. 7, pp. 1870-1874. http://dx.doi.org/10.1093/molbev/msw054. PMid:27004904.
http://dx.doi.org/10.1093/molbev/msw054...
to be 2691.79 cm2 male and that 2576.46 cm2 for female. In current study average mass of bats were 869.6 gm, weight 8.59 newton and density 0.701 g/m3 in both sexes. Which were in similarity range with other published reports such as published study of Khan et al. (2021)KHAN, W., NISA, N.N., KHAN, A.R., RAHBAR, B., MEHMOOD, S.A., AHMED, S., KAMAL, M., SHAH, M., RASOOL, A., PAHANWAR, W.A., ULLAH, I. and KHAN, S., 2021. Roosting ecology and morphometric analysis of Pteropus medius (Indian flying fox) in Lower Dir, district, Pakistan. Brazilian Journal of Biology = Revista Brasileira de Biologia, vol. 81, no. 1, pp. 77-82. http://dx.doi.org/10.1590/1519-6984.221935. PMid:32401851.
http://dx.doi.org/10.1590/1519-6984.2219...
have reported the mass of male bats 855.7 gm and average mass of female bats 852.71 gm, Similarly Roberts (1997)ROBERTS, T.J., 1997. The Mammals of Pakistan. New York: Oxford University Press. reported body mass of bat 600 to 1600 gm and reported that females were usually smaller than males. On the other side Rahman et al. (2015)RAHMAN, F.U., PERVEEN, F., RAUF, T., SALIM, M., ALI, Z. and KHATTAK, M.N.K., 2015. Mormophometric characters and distribution of bat (mammalia: chiroptera) fauna in northwestern Pakistan. The Journal of Animal & Plant Sciences, vol. 25, no. 3, suppl. 2, pp. 454-460. have reported larger value of average mass of bats 1121.9±38.9 gm. This difference with current report may be due to variances among different factors of bats for instance age, sex and habitat of different biological spot. In addition present study showed that the numbers of trees in biological spots have direct positive impacts on bats colonies as these roosting trees are shelters and keep them safe from predators and environmental stress. Same reports have been reported by different researchers such as Rainey and Pierson (1992)RAINEY, W.E. and PIERSON, E.D., 1992. Distribution of Pacific island flying foxes. In: D.E. WILSON and G.L. GRAHAM, eds. Pacific Island flying foxes: proceedings of an international conservation conference. Washington, DC: US Department of the Interior, Fish and Wildlife Service, Biological Report, pp. 111-122., Richmond et al. (1998)RICHMOND, J.Q., BANACK, S.A. and GRANT, G.S., 1998. Comparative analysis of wing morphology, flight behaviour, and habitat use in flying foxes (Genus: pteropus). Australian Journal of Zoology, vol. 46, no. 3, pp. 283-289. http://dx.doi.org/10.1071/ZO97059.
http://dx.doi.org/10.1071/ZO97059...
.

5. Conclusion

Current study showed that different biological spot sites have different counts of bats colonies which were dependent on trees numbers at each site. Furthermore as their measurement have showed the male bats were larger in size than female. Studies like this should be conducted to accurately identify each and every species of bats and campaign, seminars and program should be arranged regarding bats to conserve them.

Acknowledgements

This work was financially supported by the project MECESUP UCT 0804, and express the gratitude to M.I., and S.M.A., for their valuable comments for improves the manuscript.

References

  • ANDERSON, S.C. and RUXTON, G.D., 2020. The evolution of flight in bats: a novel hypothesis. Mammal Review, vol. 50, no. 4, pp. 426-439. http://dx.doi.org/10.1111/mam.12211
    » http://dx.doi.org/10.1111/mam.12211
  • BATES, P.J.J. and HARRISON, D.L., 1997. Bats of the Indian subcontinent Sevenoaks: Harrison Zoological Museum, 258 p.
  • BENNETT, M.B., 1993. Structural modifications involved in the fore‐and hind limb grip of some flying foxes (Chiroptera: pteropodidae). Journal of Zoology, vol. 229, no. 2, pp. 237-248. http://dx.doi.org/10.1111/j.1469-7998.1993.tb02633.x
    » http://dx.doi.org/10.1111/j.1469-7998.1993.tb02633.x
  • BUTT, A. and BEG, M.A., 2001. Description of two new species of spiders of the families Clubionidae and Oxyopidae from Pakistan. Pakistan Journal of Zoology, vol. 33, no. 1, pp. 35-38.
  • CHAKRAVARTHY, A.K., YESHWANTH, H.M., KUMAR, L.V. and KUMAR, N.P., 2009. Giant Indian fruit bat (Pteropus giganteus Brunnich) roost in Karnataka, south India: a case for preservation as a heritage site. Tiger Paper, vol. 36, pp. 25-30.
  • CHEKE, A.S. and DAHL, J.F., 1981. The status of bats on western Indian Ocean islands, with special reference to Pteropus. Mammalia, vol. 45, no. 2, pp. 205-238. http://dx.doi.org/10.1515/mamm.1981.45.2.205
    » http://dx.doi.org/10.1515/mamm.1981.45.2.205
  • CLAWSON, R.L., 2002. Trends in population size and current status. In: A. KURTA and J. KENNEDY, eds. The Indiana bat: biology and management of an endangered species Austin: Bat Conservation International, pp. 2-8.
  • DANIEL, B.A., 2009. Bat taxonomy and echolocation workshop for researchers at M.K.U. Small Mammal Mail, vol. 1, no. 2, pp. 39-44.
  • ESTRADA, A., COATES‐ESTRADA, R. and MERITT JUNIOR, D., 1993. Bat species richness and abundance in tropical rain forest fragments and in agricultural habitats at Los Tuxtlas, Mexico. Ecography, vol. 16, no. 4, pp. 309-318. http://dx.doi.org/10.1111/j.1600-0587.1993.tb00220.x
    » http://dx.doi.org/10.1111/j.1600-0587.1993.tb00220.x
  • FLEMING, T.H., NELSON, A.A. and DALTON, V.M., 1998. Roosting behavior of the lesser long-nosed bat, Leptonycteris curasoae. Journal of Mammalogy, vol. 79, no. 1, pp. 147-155. http://dx.doi.org/10.2307/1382849
    » http://dx.doi.org/10.2307/1382849
  • FUJITA, M.S. and TUTTLE, M.D., 1991. Flying foxes (Chiroptera: Pteropodidae): threatened animals of key ecological and economic importance. Conservation Biology, vol. 5, no. 4, pp. 455-463. http://dx.doi.org/10.1111/j.1523-1739.1991.tb00352.x
    » http://dx.doi.org/10.1111/j.1523-1739.1991.tb00352.x
  • GHAZALI, M. and DZEVERIN, I., 2013. Correlations between hardness of food and craniodental traits in nine Myotis species (Chiroptera, Vespertilionidae). Vestnik Zoologii, vol. 47, no. 1, pp. 67-76. http://dx.doi.org/10.2478/vzoo-2013-0006
    » http://dx.doi.org/10.2478/vzoo-2013-0006
  • HARRIS, A.H., 1974. Myotis yumanensis in interior southwestern North America with comments on Myotis lucifugus. Journal of Mammalogy, vol. 55, no. 3, pp. 589-607. http://dx.doi.org/10.2307/1379548
    » http://dx.doi.org/10.2307/1379548
  • HASSAN, H.U., ALI, Q.M., AHMAD, N., ATTAULLAH, M., CHATTA, A.M., FAROOQ, U. and ALI, A., 2020. Study of vertebrate diversity and associated threats in selected habitats of Sindh and Balochistan, Pakistan. International Journal of Biology and Biotechnology, vol. 17, pp. 163-175.
  • HASSAN, H., ALI, Q.M., AHMAD, N., MASOOD, Z., HOSSAIN, M.Y., GABOL, K., KHAN, W., HUSSAIN, M., ALI, A., ATTAULLAH, M. and KAMAL, M., 2021a. Assessment of growth characteristics, the survival rate and body composition of Asian Sea bass Lates calcarifer (Bloch, 1790) under different feeding rates in closed aquaculture system. Saudi Journal of Biological Sciences, vol. 28, no. 2, pp. 1324-1330. http://dx.doi.org/10.1016/j.sjbs.2020.11.056 PMid:33613062.
    » http://dx.doi.org/10.1016/j.sjbs.2020.11.056
  • HASSAN, H.U., ALI, Q.M., KHAN, W., MASOOD, Z., ABDEL-AZIZ, M.F.A., SHAH, M.I.A., GABOL, K., WATTOO, J., MAHMOOD CHATTA, A., KAMAL, M., ZULFIQAR, T. and HOSSAIN, M.Y., 2021b. AEffect of feeding frequency as a rearing system on biological performance, survival, body chemical composition and economic efficiency of Asian seabass Lates calcarifer (Bloch, 1790) reared under controlled environmental condition. Saudi Journal of Biological Sciences, vol. 28, no. 12, pp. 7360-7366. http://dx.doi.org/10.1016/j.sjbs.2021.08.031 PMid:34867038.
    » http://dx.doi.org/10.1016/j.sjbs.2021.08.031
  • HASSAN, H.U., MAHBOOB, S., MASOOD, Z., RIAZ, M.N., RIZWAN, S., AL-MISNE, F., ABDEL-AZIZ, M.F.A., AL-GHANIM, K.A., GABOL, K., CHATTA, A.M., KHAN, N.A., SAEED and WAQAR, M., 2023. Biodiversity of commercially important finfish species caught by mid-water and bottom trawls from two different coasts of Arabian Sea: threats and conservation strategies. Brazilian Journal of Biology = Revista Brasileira de Biologia, vol. 83, pp. e249211. http://dx.doi.org/10.1590/1519-6984.249211
    » http://dx.doi.org/10.1590/1519-6984.249211
  • HEITHAUS, E.R., FLEMING, T.H. and OPLER, P.A., 1975. Foraging patterns and resource utilization in seven species of bats in a seasonal tropical forest. Ecology, vol. 56, no. 4, pp. 841-854. http://dx.doi.org/10.2307/1936295
    » http://dx.doi.org/10.2307/1936295
  • HILL, J. and SMITH, J., 1984. Bats: a natural history Austin: University of Texas Press.
  • HILL, J.E. and SMITH, J.D., 1985. Bats: a natural history London: British Museum.
  • HOUSTON, R.D., BOONMAN, A.M. and JONES, G., 2004. Do echolocation signal parameters restrict bats’ choice of prey? In: J. THOMAS, C. MOSS and M. VATER, eds. Echolocation in bats and dolphins Chicago: Chicago University Press, pp. 339-345.
  • HUTSON, A.M., MICKLEBURGH, S.P. and RACEY, P.A., 2001. Microchiropteran bats: global status survey and conservation action plan Gland: IUCN. IUCN/SSC Action Plans for the Conservation of Biological Diversity. http://dx.doi.org/10.2305/IUCN.CH.2001.SSC-AP.1.en
    » http://dx.doi.org/10.2305/IUCN.CH.2001.SSC-AP.1.en
  • JACOBS, D.S., EICK, G.N., SCHOEMAN, M.C. and MATTHEE, C.A., 2006. Insectivorous bat, Scotophilus dinganii Journal of Mammalogy, vol. 87, no. 1, pp. 161-170. http://dx.doi.org/10.1644/04-MAMM-A-132R2.1
    » http://dx.doi.org/10.1644/04-MAMM-A-132R2.1
  • KALKA, M.B., SMITH, A.R. and KALKO, E.K., 2008. Bats limit arthropods and herbivory in a tropical forest. Science, vol. 320, no. 5872, p. 71. http://dx.doi.org/10.1126/science.1153352 PMid:18388286.
    » http://dx.doi.org/10.1126/science.1153352
  • KELM, D.H., WIESNER, K.R. and VON HELVERSEN, O., 2008. Effects of artificial roosts for frugivorous bats on seed dispersal in a Neotropical forest pasture mosaic. Conservation Biology, vol. 22, no. 3, pp. 733-741. http://dx.doi.org/10.1111/j.1523-1739.2008.00925.x PMid:18445078.
    » http://dx.doi.org/10.1111/j.1523-1739.2008.00925.x
  • KHAN, W., NISA, N.N., KHAN, A.R., RAHBAR, B., MEHMOOD, S.A., AHMED, S., KAMAL, M., SHAH, M., RASOOL, A., PAHANWAR, W.A., ULLAH, I. and KHAN, S., 2021. Roosting ecology and morphometric analysis of Pteropus medius (Indian flying fox) in Lower Dir, district, Pakistan. Brazilian Journal of Biology = Revista Brasileira de Biologia, vol. 81, no. 1, pp. 77-82. http://dx.doi.org/10.1590/1519-6984.221935 PMid:32401851.
    » http://dx.doi.org/10.1590/1519-6984.221935
  • KUMAR, S., STECHER, G. and TAMURA, K., 2016. MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Molecular Biology and Evolution, vol. 33, no. 7, pp. 1870-1874. http://dx.doi.org/10.1093/molbev/msw054 PMid:27004904.
    » http://dx.doi.org/10.1093/molbev/msw054
  • KUNZ, T.H., 1982. Ecology of bats Boston: Springer. Roosting ecology of bats, pp. 1-55. http://dx.doi.org/10.1007/978-1-4613-3421-7_1
    » http://dx.doi.org/10.1007/978-1-4613-3421-7_1
  • KUNZ, T.H., BRAUN DE TORREZ, E., BAUER, D., LOBOVA, T. and FLEMING, T.H., 2011. Ecosystem services provided by bats. Annals of the New York Academy of Sciences, vol. 1223, no. 1, pp. 1-38. http://dx.doi.org/10.1111/j.1749-6632.2011.06004.x PMid:21449963.
    » http://dx.doi.org/10.1111/j.1749-6632.2011.06004.x
  • MACCRAKEN, G.F., LEE, Y.F., GILLAM, E.H., FRICK, W. and KRAUEL, J. 2021. Bats flying at high altitudes. In: B.K. LIM, M.B. FENTON, R.M. BRIGHAM, S. MISTRY, A. KURTA, E.H. GILLAM, A. RUSSELL and J. ORTEGA, eds. 50 years of bat research Cham: Springer, pp. 189-205. http://dx.doi.org/10.1007/978-3-030-54727-1_12
    » http://dx.doi.org/10.1007/978-3-030-54727-1_12
  • MAHMOOD-UL-HASSAN, M., JONES, M.G. and DIETZ, C., 2009. The bats of Pakistan, the least known creature Muller: Verlag. 168 p.
  • MARIMUTHU, G., RAJAN, K.E., KOILRAJ, A.J., ISAAC, S.S. and BALASINGH, J., 1998. Observations on the foraging behavior of a tent roosting megachiropteran bat Cynopterus sphinx. Biotropica, vol. 30, no. 2, pp. 321-324. http://dx.doi.org/10.1111/j.1744-7429.1998.tb00066.x
    » http://dx.doi.org/10.1111/j.1744-7429.1998.tb00066.x
  • MEYER, C.F.J., AGUIAR, L.M.S., AGUIRRE, L.F., BAUMGARTEN, J., CLARKE, F.M., COSSON, J., VILLEGAS, S.E., FAHR, J., FARIA, D., FUREY, N., HENRY, M., HODGKISON, R., JENKINS, R.K.B., JUNG, K.G., KINGSTON, T., KUNZ, T.H., GONZALEZ, M.C.M., MOYA, I., PONS, J., RACEY, P.A., REX, K., SAMPAIO, E.M., STONER, K.E., VOIGT, C.C., VON STADEN, D., WEISE, C.D. and KALKO, E.K.V., 2010. Long-term monitoring of tropical bats for anthropogenic impact assessment: gauging the statistical power to detect population change. Biological Conservation, vol. 143, no. 11, pp. 2797-2807. http://dx.doi.org/10.1016/j.biocon.2010.07.029
    » http://dx.doi.org/10.1016/j.biocon.2010.07.029
  • MICKLEBURGH, S.P., HUTSON, A.M. and RACEY, P.A., 2002. A review of the global conservation status of bats. Oryx, vol. 36, no. 1, pp. 18-34. http://dx.doi.org/10.1017/S0030605302000054
    » http://dx.doi.org/10.1017/S0030605302000054
  • MILDENSTEIN, T.L., STIER, S.C., NUEVO-DIEGO, C.E. and MILLS, L.S., 2005. Habitat selection of endangered and endemic large flying-foxes in Subic Bay, Philippines. Biological Conservation, vol. 126, no. 1, pp. 93-102. http://dx.doi.org/10.1016/j.biocon.2005.05.001
    » http://dx.doi.org/10.1016/j.biocon.2005.05.001
  • NAGORSEN, D.W. and BRIGHAM, R.M., 1993. The bats of British Columbia Vancouver: UBC Press. 164 p.
  • PERESWIET-SOLTAN, A., 2007. Relation between climate and bat fauna in Europe. Travaux du Muséum d’Histoire Naturelle, vol. 50, pp. 505-515.
  • RAHMAN, F.U., PERVEEN, F., RAUF, T., SALIM, M., ALI, Z. and KHATTAK, M.N.K., 2015. Mormophometric characters and distribution of bat (mammalia: chiroptera) fauna in northwestern Pakistan. The Journal of Animal & Plant Sciences, vol. 25, no. 3, suppl. 2, pp. 454-460.
  • RAINEY, W.E. and PIERSON, E.D., 1992. Distribution of Pacific island flying foxes. In: D.E. WILSON and G.L. GRAHAM, eds. Pacific Island flying foxes: proceedings of an international conservation conference Washington, DC: US Department of the Interior, Fish and Wildlife Service, Biological Report, pp. 111-122.
  • RICHMOND, J.Q., BANACK, S.A. and GRANT, G.S., 1998. Comparative analysis of wing morphology, flight behaviour, and habitat use in flying foxes (Genus: pteropus). Australian Journal of Zoology, vol. 46, no. 3, pp. 283-289. http://dx.doi.org/10.1071/ZO97059
    » http://dx.doi.org/10.1071/ZO97059
  • ROBERTS, T.J., 1997. The Mammals of Pakistan New York: Oxford University Press.
  • RODRÍGUEZ-HERRERA, B., MEDELLÍN, R.A. and GAMBA-RIOS, M., 2008. Roosting requirements of white tent-making bat Ectophylla alba (Chiroptera: phyllostomidae). Acta Chiropterologica, vol. 10, no. 1, pp. 89-95. http://dx.doi.org/10.3161/150811008X331126
    » http://dx.doi.org/10.3161/150811008X331126
  • RUMMEL, A.D., SWARTZ, S.M. and MARSH, R.L., 2019. Warm bodies, cool wings: regional heterothermy in flying bats. Biology Letters, vol. 15, no. 9, p. 20190530. http://dx.doi.org/10.1098/rsbl.2019.0530 PMid:31506035.
    » http://dx.doi.org/10.1098/rsbl.2019.0530
  • RUSSO, I.R.M., CHIMIMBA, C.T. and BLOOMER, P., 2006. Mitochondrial DNA differentiation between two species of Aethomys (Rodentia: Muridae) from southern Africa. Journal of Mammalogy, vol. 87, no. 3, pp. 545-553. http://dx.doi.org/10.1644/05-MAMM-A-222R3.1
    » http://dx.doi.org/10.1644/05-MAMM-A-222R3.1
  • SCHIPPER, J., CHANSON, J.S., CHIOZZA, F., COX, N.A., HOFFMANN, M., KATARIYA, V., LAMOREUX, J., RODRIGUES, A.S., STUART, S.N., TEMPLE, H.J., BAILLIE, J., BOITANI, L., LACHER JUNIOR, T.E., MITTERMEIER, R.A., SMITH, A.T., ABSOLON, D., AGUIAR, J.M., AMORI, G., BAKKOUR, N., BALDI, R., BERRIDGE, R.J., BIELBY, J., BLACK, P.A., BLANC, J.J., BROOKS, T.M., BURTON, J.A., BUTYNSKI, T.M., CATULLO, G., CHAPMAN, R., COKELISS, Z., COLLEN, B., CONROY, J., COOKE, J.G., FONSECA, G.A., DEROCHER, A.E., DUBLIN, H.T., DUCKWORTH, J.W., EMMONS, L., EMSLIE, R.H., FESTA-BIANCHET, M., FOSTER, M., FOSTER, S., GARSHELIS, D.L., GATES, C., GIMENEZ-DIXON, M., GONZALEZ, S., GONZALEZ-MAYA, J.F., GOOD, T.C., HAMMERSON, G., HAMMOND, P.S., HAPPOLD, D., HAPPOLD, M., HARE, J., HARRIS, R.B., HAWKINS, C.E., HAYWOOD, M., HEANEY, L.R., HEDGES, S., HELGEN, K.M., HILTON-TAYLOR, C., HUSSAIN, S.A., ISHII, N., JEFFERSON, T.A., JENKINS, R.K., JOHNSTON, C.H., KEITH, M., KINGDON, J., KNOX, D.H., KOVACS, K.M., LANGHAMMER, P., LEUS, K., LEWISON, R., LICHTENSTEIN, G., LOWRY, L.F., MACAVOY, Z., MACE, G.M., MALLON, D.P., MASI, M., MCKNIGHT, M.W., MEDELLÍN, R.A., MEDICI, P., MILLS, G., MOEHLMAN, P.D., MOLUR, S., MORA, A., NOWELL, K., OATES, J.F., OLECH, W., OLIVER, W.R., OPREA, M., PATTERSON, B.D., PERRIN, W.F., POLIDORO, B.A., POLLOCK, C., POWEL, A., PROTAS, Y., RACEY, P., RAGLE, J., RAMANI, P., RATHBUN, G., REEVES, R.R., REILLY, S.B., REYNOLDS III, J.E., RONDININI, C., ROSELL-AMBAL, R.G., RULLI, M., RYLANDS, A.B., SAVINI, S., SCHANK, C.J., SECHREST, W., SELF-SULLIVAN, C., SHOEMAKER, A., SILLERO-ZUBIRI, C., SILVA, N., SMITH, D.E., SRINIVASULU, C., STEPHENSON, P.J., VAN STRIEN, N., TALUKDAR, B.K., TAYLOR, B.L., TIMMINS, R., TIRIRA, D.G., TOGNELLI, M.F., TSYTSULINA, K., VEIGA, L.M., VIÉ, J.C., WILLIAMSON, E.A., WYATT, S.A., XIE, Y. and YOUNG, B.E., 2008. The status of the world’s land and marine mammals: diversity, threat, and knowledge. Science, vol. 322, no. 5899, pp. 225-230. http://dx.doi.org/10.1126/science.1165115 PMid:18845749.
    » http://dx.doi.org/10.1126/science.1165115
  • SCHNITZLER, H.U. and KALKO, E.K., 2001. Echolocation by insect-eating bats: we define four distinct functional groups of bats and find differences in signal structure that correlate with the typical echolocation tasks faced by each group. Bioscience, vol. 51, no. 7, pp. 557-569. http://dx.doi.org/10.1641/0006-3568(2001)051[0557:EBIEB]2.0.CO;2
    » http://dx.doi.org/10.1641/0006-3568(2001)051[0557:EBIEB]2.0.CO;2
  • SCHNITZLER, H.-U., MOSS, C.F. and DENZINGER, A., 2003. From spatial orientation to food acquisition in echolocating bats. Trends in Ecology & Evolution, vol. 18, no. 8, pp. 386-394. http://dx.doi.org/10.1016/S0169-5347(03)00185-X
    » http://dx.doi.org/10.1016/S0169-5347(03)00185-X
  • SIMMONS, N.B., 2005. Chiroptera. In: K. D. ROSE and J. D. ARCHIBALD, eds. The rise of placental mammals Baltimore: Johns Hopkins University Press, pp. 159-174.
  • SIMMONS, N.B., 2010. Personal communication. New York: American Museum of Natural History.
  • SRINIVASULU, C., RACEY, P.A. and MISTRY, S., 2010. A key to the bats (Mammalia: Chiroptera) of South Asia. Journal of Threatened Taxa, vol. 2, no. 7, pp. 1001-1076. http://dx.doi.org/10.11609/JoTT.o2352.1001-76
    » http://dx.doi.org/10.11609/JoTT.o2352.1001-76
  • THATCHER, O., 2004 [viewed 19 October 2004]. Fruit and nectar bat biology [online]. Lubee Bat Conservacy. Available from: http://www.lubee.org/about-biology.aspx
    » http://www.lubee.org/about-biology.aspx
  • WELLER, T.J., SCOTT, S.A., RODHOUSE, T.J., ORMSBEE, P.C. and ZINCK, J.M., 2007. Field identification of the cryptic vespertilionid bats, Myotis lucifugus and M. yumanensis. Acta Chiropterologica, vol. 9, no. 1, pp. 133-147. http://dx.doi.org/10.3161/1733-5329(2007)9[133:FIOTCV]2.0.CO;2
    » http://dx.doi.org/10.3161/1733-5329(2007)9[133:FIOTCV]2.0.CO;2
  • WHITAKER, J.O. and KARATAŞ, A., 2009. Food and feeding habits of some bats from Turkey. Acta Chiropterologica, vol. 11, no. 2, pp. 393-403. http://dx.doi.org/10.3161/150811009X485611
    » http://dx.doi.org/10.3161/150811009X485611
  • WILLIAMS-GUILLÉN, K., PERFECTO, I. and VANDERMEER, J., 2008. Bats limit insects in a neotropical agroforestry system. Science, vol. 320, no. 5872, p. 70. http://dx.doi.org/10.1126/science.1152944 PMid:18388285.
    » http://dx.doi.org/10.1126/science.1152944
  • ZAR, J.H., 1999. Biostatistical analysis Upper Saddle River: Prentice Hall Inc. 661 p.

Publication Dates

  • Publication in this collection
    17 July 2023
  • Date of issue
    2023

History

  • Received
    18 Dec 2021
  • Accepted
    18 Mar 2022
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