A review of the bacular morphology of some Indian bats (Mammalia: Chiroptera)

Main Article Content

Bhargavi Srinivasulu
https://orcid.org/0000-0002-9035-3058
Harpreet Kaur
https://orcid.org/0000-0001-7928-7830
Tariq Ahmed Shah
https://orcid.org/0000-0001-6151-4214
Gundena Devender
https://orcid.org/0000-0002-2204-3787
Gopi Asad
https://orcid.org/0000-0001-5600-2054
Sreehari Raman
https://orcid.org/0000-0001-9812-1166
Chelmala Srinivasulu
https://orcid.org/0000-0003-4331-8580

Abstract

Bacular studies play a significant role in the case of bats and other mammals since it is considered an important taxon-specific character, thus helping in species discrimination. Structure of the baculum (os penis) also aids in examining and understanding cryptic diversity in bats. The baculum has been used in taxonomic studies of bats but such studies for Indian bats are few and far between. It was felt necessary to put together a comprehensive document depicting the bacular morphology of bats in India so as to be helpful for future bat studies. The penises of the bats were excised, treated with KOH, and then dyed with alizarin red to extract the bacula. The extracted bacula were measured using an oculometer, photographed, and preserved in glycerol. Of the total of 47 species of bats (belonging to nine families) collected and studied during the past decade, we present the bacular morphology of 44 species from peninsular India, Andaman Islands, and Jammu and Kashmir. Bacular morphology of eight taxa, namely, Eonycteris spelaea, Rhinolophus pusillus, R. lepidus monticola, R. cognatus, Hipposideros cf. grandis, Myotis peytoni, M. horsfieldii dryas, and M. longipes are presented here for the first time from India.

Article Details

Section
Communications
Author Biographies

Bhargavi Srinivasulu, Natural History Museum and Wildlife Biology & Taxonomy Lab, Department of Zoology, University College of Science, Osmania University, Hyderabad, Telangana State 500007, India.

UGC-Post Doctoral Fellow (W)

Harpreet Kaur, Natural History Museum and Wildlife Biology & Taxonomy Lab, Department of Zoology, University College of Science, Osmania University, Hyderabad, Telangana State 500007, India.

Post Doctoral Fellow

Tariq Ahmed Shah, Natural History Museum and Wildlife Biology & Taxonomy Lab, Department of Zoology, University College of Science, Osmania University, Hyderabad, Telangana State 500007, India.

Senior Research Fellow

Gundena Devender, Natural History Museum and Wildlife Biology & Taxonomy Lab, Department of Zoology, University College of Science, Osmania University, Hyderabad, Telangana State 500007, India.

Research Scholar

Gopi Asad, Natural History Museum and Wildlife Biology & Taxonomy Lab, Department of Zoology, University College of Science, Osmania University, Hyderabad, Telangana State 500007, India.

Project Assistant

Sreehari Raman, Center for Integrative Conservation, Xishuangbanna Tropical Botanical Garden, Chinese Academy of Sciences, Menglun, Mengla, Yunnan Province, 666303, PR China.

Research Fellow

Chelmala Srinivasulu, Natural History Museum and Wildlife Biology & Taxonomy Lab, Department of Zoology, University College of Science, Osmania University, Hyderabad, Telangana State 500007, India.

Assistant Professor

Department of Zoology

References

Agrawal, V.C. & Y.P. Sinha (1973). Studies on the bacula of some oriental bats. Anatomischer Anzeiger 133: 180–192.

Aksenova, T.G. & P.K. Smirnov (1986). Structural features of Lagomorpha genitals. pp. 5–6. In: 4rth All Union Theriological Society Meeting Report. All Union Theriological Society, Moscow, USSR.

Albayrak, I. & N. Aşan (2001). The structure of baculum in Myotis myotis and Myotis blythi (Chiroptera: Vespertilionidae) from Turkey. Turkish Journal of Zoology 25: 229–233.

Bates, P. J. J. & D.L. Harrison (1997). Bats of the Indian Subcontinent. Harrison Zoological Museum, Sevenoaks, Kent, United Kingdom. 258pp.

Bates, P.J.J., F. Ratrimomanarivo, D.L. Harrison & S.M. Goodman (2006). A review of pipistrelles and serotines (Chiroptera: Vespertilionidae) from Madagascar, including the description of a new species of Pipistrellus. Acta Chiropterologica 8(2): 299–324. https://doi.org/10.3161/1733-5329(2006)8[299:Adoans]2.0.CO;2

Bates, P.J.J., O. Tun, M.M. Aung, A. Lu, M.R. Lum & M.M. Sein (2015). A review of Hipposideros lankadiva Kelaart, 1850 (Chiroptera: Hipposideridae) with a description of a new subspecies from Myanmar. Tropical Natural History 15(2): 191–204. https://li01.tci-thaijo.org/index.php/tnh/article/view/103082

Benda, P., A. Kiefer, V. Hanák, V. & M. Veith (2004). Systematic status of African populations of long-eared bats, genus Plecotus (Mammalia: Chiroptera). Folia Zoologica 53 (Monograph, 1): 1–47.

Benda, P., M.M. Al-Jumaily, A. Reiter & A.K. Nasher (2011). Noteworthy records of bats from Yemen with description of a new species from Socotra. Hystrix the Italian Journal of Mammalogy 22(1): 23–56. https://doi.org/10.4404/hystrix-22.1-4473

Bhatnagar, K.P. (1967). Bacula of some Indian Megachiroptera. Journal of Mammalogy 48(3): 494–497. https://doi.org/10.2307/1377802 DOI: https://doi.org/10.2307/1377802

Brindle M. & C. Opie (2016). Postcopulatory sexual selection influences baculum evolution in primates and carnivores. Proceedings of the Royal Society B 283: 20161736. https://doi.org/10.1098/rspb.2016.1736 DOI: https://doi.org/10.1098/rspb.2016.1736

Brown, R.E. (1967). Bacula of some New World molossid bats. Mammalia 31(4): 645–667. https://doi.org/10.1515/mamm.1967.31.4.645 DOI: https://doi.org/10.1515/mamm.1967.31.4.645

Brown, R.E., H.H. Genoways & J.K. Jones Jr. (1971). Bacula of some Neotropical bats. Mammalia 35(3): 456–464. https://doi.org/10.1515/mamm.1971.35.3.456 DOI: https://doi.org/10.1515/mamm.1971.35.3.456

Burt, W.H. (1960). Bacula of North American mammals. Miscellaneous Publications of Museum of Zoology, University of Michigan 113:1–75. DOI: https://doi.org/10.3998/mpub.9690254

Chaine, J. (1925). L’os pénien: étude descriptive et comparative. Actes de la Société Linnéenne de Bordeaux 78: 1–195.

Corbet, G.B. (1964). The grey long-eared bat Plecotus austriacus in England and the Channel Islands. Proceedings of the Zoological Society of London 143(3): 511–515. https://doi.org/10.1111/j.1469-7998.1964.tb03875.x DOI: https://doi.org/10.1111/j.1469-7998.1964.tb03875.x

Davis, D.D. (1947). The bacula of some fruit bats (Pteropus). Fieldiana, Chicago Natural History Museum 31(16): 125–131. DOI: https://doi.org/10.5962/bhl.title.3050

Didier, R. (1949). Etude systématique de l’os pénien des mammifèrs: famille des félidés. Mammalia 13(1): 17–37. https://doi.org/10.1515/mamm.1949.13.1.17 DOI: https://doi.org/10.1515/mamm.1949.13.1.17

Didier, R. (1964). Etude systématique de l’os pénien des mammifèrs. Mammalia 29: 331–342. https://doi.org/10.1515/mamm.1965.29.3.331 DOI: https://doi.org/10.1515/mamm.1965.29.3.331

Dixson, A.F. (1995). Baculum length and copulatory behaviour in carnivores and pinnipeds (Grand Order Ferae). Journal of Zoology 235(1): 67–76. https://doi.org/10.1111/j.1469-7998.1995.tb05128.x DOI: https://doi.org/10.1111/j.1469-7998.1995.tb05128.x

Douangboubpha, B., S. Bumrungsri, P. Soisook, C. Satasook, N.M. Thomas & P.J.J. Bates (2010). A taxonomic review of the Hipposideros bicolor species complex and H. pomona (Chiroptera: Hipposideridae) in Thailand. Acta Chiropterologica 12(2): 415–438. https://doi.org/10.3161/150811010X537990 DOI: https://doi.org/10.3161/150811010X537990

Eadie, W.R. (1947). Homologies of the male accessory reproductive glands in Sorex and Blarina. The Anatomical Record 98(3): 347–359. https://doi.org/10.1002/ar.1090980305 DOI: https://doi.org/10.1002/ar.1090980305

Erbajeva, M.A., J.I. Mead, N.V. Alexeeva, C. Angelone & S.L. Swift (2011). Taxonomic diversity of late Cenozoic Asian and North American ochotonids (an overview). Paleontological Electronica 14(3) 42A: 1–9.

Goodman, S.M., C.F. Rakotondramanana, B. Ramasindrazana, A. Monadjem, M.C. Schoeman, P.J. Taylor, K. Naughton & B. Appleton (2015). An integrative approach to characterize Malagasy bats of the subfamily Vespertilioninae Gray, 1821, with the description of a new species of Hypsugo. Journal of the Linnean Society 173(4): 988–1018. https://doi.org/10.1111/zoj.12223 DOI: https://doi.org/10.1111/zoj.12223

Hanák, V. & J. Gaisler (1969). Notes on the taxonomy and ecology of Myotis longipes (Dobson, 1873). Zoologicke Listy 18(3): 195–206.

Hamilton, W.J. Jr. (1946). A study of the baculum in some North American Microtinae. Journal of Mammalogy 27(4): 378–387. https://doi.org/10.2307/1375346 DOI: https://doi.org/10.2307/1375346

Hamilton, W.J. Jr. (1949). The bacula of some North American vespertilionid bats. Journal of Mammalogy 30(2): 97–102. https://doi.org/10.2307/1375254 DOI: https://doi.org/10.2307/1375254

Heller, K.G. & M. Volleth (1984). Taxonomic position of ‘Pipistrellus societatis’ Hill, 1972 and the karyological characteristics of the genus Eptesicus (Chiroptera: Vespertilionidae). Zeitschrift für zoologische Systematik und Evolutionsforschung 22(1): 65–77. https://doi.org/10.1111/j.1439-0469.1984.tb00563.x DOI: https://doi.org/10.1111/j.1439-0469.1984.tb00563.x

Herdina, A.N. (2014). The bat baculum: Histomorphological methods and micro CT-based 3D models to distinguish cryptic species of Pipistrellus and Plecotus and to test functional hypotheses using post-mortem specimens. Ph.D. Thesis, University of Vienna, Austria. 185pp.

Hill, J.E. (1976). Bats referred to the genus Hesperotenus Peters, 1869 (Chiroptera: Vespertilionidae) with the description of a new subgenus. Bulletin of the British Museum of Natural History (Zoology) 32: 1–28.

Hill, J.E. & D.L. Harrison (1987). The baculum in the Vespertilioninae (Chiroptera: Vespertilionidae) with a systematic review, a synopsis of Pipistrellus and Eptesicus, and the description of a new genus and subgenus. Bulletin of the British Museum of natural History (Zoology) 52: 225–305.

Hutson, A.M., S. Rossiter, G. Csorba & C. Burgin (2019). Family Rhinolophidae (Horseshoe Bats), pp. 260–332. In: Wilson, D.E. & R.A. Mittemeier (eds.). Handbook of the Mammals of the World: Bats. Lynx Edicions, Spain, 1008pp.

Kaur, H., C. Srinivasulu, B. Srinivasulu, T.A. Shah, G. Devender & A. Srinivasulu (2014). Taxonomic notes and distribution extension of Durga Das’s leaf-nosed bat Hipposideros durgadasi Khajuria, 1970 (Chiroptera: Hipposideridae) from south India. Biodiversity Data Journal 2: e4127. https://doi.org/10.3897/BDJ.2.e4127 DOI: https://doi.org/10.3897/BDJ.2.e4127

Kaur, H., C. Srinivasulu, T.A. Shah, G. Devender & B. Srinivasulu (2017). Updates on the distribution of the Cantor’s Leaf-nosed Bat, Hipposideros galeritus Cantor, 1846 (Chiroptera, Hipposideridae): new records from peninsular India. Check List 13(6): 909–912. https://doi.org/10.15560/13.6.909 DOI: https://doi.org/10.15560/13.6.909

Khajuria, H. (1979). Studies on the bat (Chiroptera. Mammalia) of M.P., India. Pt. I. (Families Pteropodidae, Rhinopomatidae and Emballonuridae). Records of the Zoological Survey of India, Occasional Paper No. 13. Zoological Survey of India, Calcutta, 59 pp.

Khajuria, H. (1980). Taxonomical and ecological studies on the bats of Jabalpur district, Madhya Pradesh, India. Part 2. (Families Megadermatidae, Rhinolopbidae and Vespertilionidae). Records of the Zoological Survey of India, Occasional Paper No. 19. Zoological Survey of India, Calcutta, 69pp.

Khajuria, H. (1982). External genitalia and bacula of some central Indian Microchiroptera. Säugetierkundliche Mitteilungen 30: 287–295.

Kitchener, D.J. & Maharadatunkamsi (1991). Description of a new species of Cynopterus (Chiroptera: Pteropodidae) from Nusa Tenggara, Indonesia. Records of the Western Australian Museum 15(2): 307–363.

Kitchener, D.J., N. Caputi & B. Jones (1986). Revision of Australo-Papuan Pipistrellus and Falsistrellus (Microchiroptera: Vespertilionidae). Records of the Western Australian Museum 12: 435–495.

Kruskop, S.V. (2015). Dull and bright: cryptic diversity within the Hipposideros larvatus group in Indochina (Chiroptera: Hipposideridae). Lynx n.s. (Praha) 46: 29–42.

Kruskop, S.V. & A.V. Borisenko (2013). A new species of south-east Asian Myotis (Chiroptera: Vespertilionidae), with comments on Vietnamese ‘whiskered bats’. Acta Chiropterologica 15(2): 293–305. https://doi.org/10.3161/150811013X678937 DOI: https://doi.org/10.3161/150811013X678937

Kruskop, S.V. & L.A. Lavrenchenko (2000). A new species of long-eared bat (Plecotus; Vespertilionidae, Mammalia) from Ethiopia. Myotis 38: 5–17.

Krutzsch, P.H. (1959). Variation in the os penis of tropical fruit bats. Journal of Mammalogy 40: 387–392. https://doi.org/10.2307/1376563 DOI: https://doi.org/10.2307/1376563

Krutzsch, P.H. (1962). Additional data on the os penis of Megachiroptera. Journal of Mammalogy 43: 34–42. https://doi.org/10.2307/1376878 DOI: https://doi.org/10.2307/1376878

Krutzsch, P.H. (2005). Reproductive anatomy and cyclicity of the bat Eonycteris spelaea Dobson (Chiroptera: Pteropodidae) in West Malaysia. Acta Chiropterologica 7(1): 51–64. http://doi.org/10.3161/1733-5329(2005)7[51:RAACOT]2.0.CO;2

Krutzsch, P.H. & T.A. Vaughan (1955). Additional data on the bacula of North American bats. Journal of Mammalogy 36: 96–100. https://doi.org/10.2307/1375727 DOI: https://doi.org/10.2307/1375727

Lanza, B. (1959). Chiroptera, pp. 187–473. In: Toschi, A. & B. Lanza Fauna d’Italia. Vol. IV. Mammalia (Generatilià, Insectivora, Chiroptera). Calderini, Bologna. VIII+485pp.

Lanza, B. (1960). Su due specie criptiche di Orecchione: Plecotus auritus (L) e P. wardi Thomas (Mamm: Chiroptera). Monitore Zoologico Italiano 68: 7–23.

Lanza, B. (1963). Sui baculum e sui genitali esterni maschili di Pteropus (Mamm. Megachiroptera). Monitore Zoologico Italiano 70-71 (1962–1963): 507–542, 6 figs.

Lanza, B. (1970). The baculum of Pteropus and its significance for the phylogenesis of the genus (Mammalia, Megachiroptera). Monitore Zoologico Italiano. Supplemento 3: 37–68. https://doi.org/10.1080/03749444.1970.10736760 DOI: https://doi.org/10.1080/03749444.1970.10736760

Larivière, S. & S.H. Ferguson (2002). On the evolution of the mammalian baculum: vaginal friction, prolonged intromission or induced ovulation? Mammal Review 32(4): 283–294. https://doi.org/10.1046/j.1365-2907.2002.00112.x DOI: https://doi.org/10.1046/j.1365-2907.2002.00112.x

Martin, R.D. (2007). The evolution of human reproduction: A primatological perspective. American Journal of Physical Anthropology 134 (S45 Yearbook of Physical Anthropology) 50: 59–84. https://doi.org/10.1002/ajpa.20734 DOI: https://doi.org/10.1002/ajpa.20734

Patterson, B.D. & C.S. Thaeler (1982). The mammalian baculum: hypothesis on the nature of bacular variability. Journal of Mammalogy 63(1): 1–15. https://doi.org/10.2307/1380665 DOI: https://doi.org/10.2307/1380665

Perrin, W.F., B. Wursig & J.G.M. Thewissen (eds). (2009). Encyclopaedia of Marine Mammals, 2nd edn. Academic Press, London, UK, 1352pp.

Rakotondramanana, C.F. & S.M. Goodman (2017). A review of the bacular morphology of Malagasy bats. Acta Chiropterologica 19(1): 51–70. https://doi.org/10.3161/15081109ACC2017.19.1.004 DOI: https://doi.org/10.3161/15081109ACC2017.19.1.004

Romer, A.S. & C.S. Parsons (1986). The Vertebrate Body. 5th edition. W.B. Saunders, Philadelphia, USA. 679 pp.

Schultz, N.G., M. Lough-Stevens, E. Abreu, T. Orr & M.D. Dean (2016). The baculum was gained and lost multiple times during mammalian evolution. Integrative and Comparative Biology 56(4): 644–656. https://doi.org/10.1093/icb/icw034 DOI: https://doi.org/10.1093/icb/icw034

Sikes, R.S. (2016). Guidelines of the American Society of Mammalogists for the use of wild mammals in research and education. Journal of Mammalogy 97(3): 663–688. https://doi.org/10.1093/jmammal/gyw078 DOI: https://doi.org/10.1093/jmammal/gyw078

Sinha, Y.P. (1976). Bacula of Rajasthan bats. Mammalia 40: 97–103. https://doi.org/10.1515/mamm.1976.40.1.97 DOI: https://doi.org/10.1515/mamm.1976.40.1.97

Sinha, Y.P. (1983). Notes on bacula of some Indian bats. Geobios New Reports 2(2): 134–136.

Soota, T.D. & Y. Chaturvedi (1980). New locality record of Pipistrellus camortae Miller from Car Nicobar and its systematic status. Records of the Zoological Survey of India 77: 83–87.

Srinivasulu, B., C. Srinivasulu, H. Kaur, T.A. Shah, G. Devender & A. Srinivasulu (2014). The reassessment of the threatened status of the Indian endemic Kolar Leaf-nosed Bat Hipposideros hypophyllus Kock and Bhat, 1994 (Mammalia: Chiroptera: Hipposideridae). Journal of Threatened Taxa 6(12): 6493–6501. https://doi.org/10.11609/JoTT.o4117.6493-501 DOI: https://doi.org/10.11609/JoTT.o4117.6493-501

Srinivasulu, B., A. Srinivasulu, C. Srinivasulu, T. Dar, A. Gopi & G. Jones (2016). First record of the Diadem Leaf-Nosed Bat Hipposideros diadema (E. Geoffroy, 1813) (Chiroptera: Hipposideridae) from the Andaman Islands, India with the possible occurrence of a hitherto unreported subspecies. Journal of Threatened Taxa 8(11): 9316–9321. https://doi.org/10.11609/jott.2862.8.11.9316-9321 DOI: https://doi.org/10.11609/jott.2862.8.11.9316-9321

Srinivasulu, B. & C. Srinivasulu (2018). In plain sight: bacular and noseleaf morphology supports distinct specific status of Roundleaf Bats Hipposideros pomona Andersen, 1918 and Hipposideros gentilis Andersen, 1918 (Chiroptera: Hipposideridae). Journal of Threatened Taxa 10(8): 12018–12026. https://doi.org/10.11609/jott.4111.10.8.12018-12026 DOI: https://doi.org/10.11609/jott.4111.10.8.12018-12026

Srinivasulu, C. (2018). South Asian Mammals: An Updated Checklist and their Scientific Names. CRC Press Taylor and Francis Group, Florida, USA. i-xvii+355pp. DOI: https://doi.org/10.1201/9780429466199

Srinivasulu, C., A. Srinivasulu & B. Srinivasulu (2020). Checklist of the bats of South Asia (v1.1). https://threatenedtaxa.org/index.php/JoTT/checklists/bats/southasia [Date of publication: 13 April 2020].

Srinivasulu, C., A. Srinivasulu, B. Srinivasulu & G. Jones (2018). A new subspecies of the Malayan Bamboo Bat (Chiroptera: Vespertilionidae: Tylonycteris malayana eremtaga) from the Andaman Islands, India. Journal of Threatened Taxa 10(1): 11210–11217. https://doi.org/10.11609/jott.3906.10.1.11210-11217 DOI: https://doi.org/10.11609/jott.3906.10.1.11210-11217

Srinivasulu, C., A. Srinivasulu, B. Srinivasulu & G. Jones (2019). Integrated approaches to identifying cryptic bat species in areas of high endemism: The case of Rhinolophus andamanensis in the Andaman Islands. PLoS ONE 14(10): e0213562; https://doi.org/10.1371/journal.pone.0213562 DOI: https://doi.org/10.1371/journal.pone.0213562

Srinivasulu, C., B. Srinivasulu, H. Kaur, T.A. Shah & G. Devender (2015). New records of Rhinolophus beddomei Andersen, 1905 (Chiroptera: Rhinolophidae) from central peninsular region of India, including echolocation call characteristics. Mammalia 79(3): 369–373. https://doi.org/10.1515/mammalia-2013-0180 DOI: https://doi.org/10.1515/mammalia-2013-0180

Srinivasulu, C., P.A. Racey & S. Mistry (2010). A key to the bats (Mammalia: Chiroptera) of South Asia. Journal of Threatened Taxa 2(7): 1001–1076. https://doi.org/10.11609/JoTT.o2352.1001-76 DOI: https://doi.org/10.11609/JoTT.o2352.1001-76

Strelkov, P.P. (1989). New data on the structure of baculum of Palaearctic bats. 1. The genera Myotis, Plecotus, and Barbastella. In: Hanak, V., I. Horacek and J. Gaisler (eds.). European bat research 1987. Proceedings of the Fourth European Bat Research Symposium, Prague, Czechoslovakia. August 18-23, 1987. Charles University Press, Prague, vol. i-xxiii, pp. 87–94.

Thomas, O. (1915). The penis bone, or “baculum” as a guide to the classification of certain squirrels. Annals and Magazine of Natural History 8(15): 383–387.

Topál, Gy. (1958). Morphological studies on the os penis of bats in the Carpathian Basin. Annales Historico-Naturales Musei Nationalis Hungarici 50 (series nova 9): 331–342.

Topál, Gy. (1975). Bacula of some Old World Leaf-nosed bats (Rhinolophidae and Hipposideridae, Chiroptera: Mammalia). Vertebrata Hungarica 16: 21–54.

Wassif, K. & G. Madkour (1972). The structure of os penis in Egyptian bats (Microchiroptera). Bulletin of the Zoological Society of Egypt 24: 45–51.

Wassif, K., G. Madkour & D. Soliman (1984). Fauna and flora of Egypt. 1. On a collection of bats from Egypt. Cairo Academy of Scientific Research and Technology Natural History Museum of Egypt, Cairo, 36 pp +vi plts.

Weimann, B., M.A. Edwards & C.N. Jass (2014). Identification of the baculum in American pika (Ochotona princeps: Lagomorpha) from southwestern Alberta, Canada. Journal of Mammalogy 95(2): 284–289. https://doi.org/10.1644/13-MAMM-A-165 DOI: https://doi.org/10.1644/13-MAMM-A-165

Williams-Ashman, H.G. (1990). Enigmatic features of penile development and functions. Perspectives in Biology and Medicine 33(3): 335–374. https://doi.org/10.1353/pbm.1990.0008 DOI: https://doi.org/10.1353/pbm.1990.0008

Zubaid, A. & G.W.H. Davison (1987). A comparative study of the baculum in Peninsular Malaysian hipposiderines. Mammalia 51(1): 139–144. https://doi.org/10.1515/mamm.1987.51.1.139 DOI: https://doi.org/10.1515/mamm.1987.51.1.139

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