Geometric Morphometrics Analysis of Inter-Population Wing Shape Variations in Bats
Article Sidebar
Main Article Content
Abstract
Background: The cryptic diversity of bat fauna in Pakistan demands to incorporate an efficient and reliable approach for morphological species identification. The traditional taxonomic approaches are effective in exploring variations of characters but have proved to be less efficient in quantifying the interspecific and intraspecific differences. Geometric morphometric method has recently act as an efficient tool to analyze the overall changes in shape and size of biological features. The present study is therefore conducted to exploit the use of geometric morphometric methods along with traditional morphological measurements to examine the size and shape differences among four geographically isolated population groups of insectivorous bat species (Pipistrellus coromandra).
Methods: Specimens were collected from different locations of Punjab, Pakistan. Twelve well-defined landmarks to quantify the variation in right wing of bats were analyzed using geometric morphometric tools and wing measurements of 5 selected parameters were also taken using traditional morphological measurements.
Results: The results of external measurements for wing overlapped for most part among the different studied population groups. Fur colour photographs displayed in the inter-population had shown visible change from dark brown to light brown giving an indication of more morphological differences. Regarding the geometric morphometric results, wing-shape differences were found to dominate in inter-population as compared to intra-population for bats species (Pipistrellus coromandra) which clearly reflects the effects of habitat factors on different populations phenotypically. The wireframe for the first two PCs indicated an overall shape change trend with the displacement of landmark points representing the expansion along the upper wing margins in PC1 compared to PC2.
Conclusion: The current study has successfully explored the power of geometric morphometric in reflecting the variations in wing shape among different populations of bats species (Pipistrellus coromandra).
Article Details
This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.
References
Adams, D. C., Rohlf, F. J., & Slice, D. E. (2004). Geometric morphometrics: Ten years of progress following the ‘revolution’. Italian Journal of Zoology, 71(1), 5–16. https://doi.org/10.1080/11250000409356545 DOI: https://doi.org/10.1080/11250000409356545
Adams, D. C., Rohlf, F. J., & Slice, D. E. (2013). A field comes of age: Geometric morphometrics in the 21st century. Hystrix: The Italian Journal of Mammalogy, 24(1), 7–14. https://doi.org/10.4404/hystrix-24.1-6283
Adams, R. A. (1996). Size-specific resource use in juvenile little brown bats, Myotis lucifugus (Chiroptera: Vespertilionidae): Is there an ontogenetic shift?. Canadian Journal of Zoology, 74(7), 1204-1210. https://doi.org/10.1139/z96-133 DOI: https://doi.org/10.1139/z96-133
Aldridge, H. (1986). Manoeuvrability and ecological segregation in the little brown (Myotis lucifugus) and Yuma (M. yumanensis) bats (Chiroptera: Vespertilionidae). Canadian Journal of Zoology, 64(9), 1878–1882. https://doi.org/10.1139/z86-280 DOI: https://doi.org/10.1139/z86-280
Aldridge, H. D. J. N., & Rautenbach, I. L. (1987). Morphology, echolocation, and resource partitioning in insectivorous bats. Journal of Animal Ecology, 56(3), 763–778. https://doi.org/10.2307/4947 DOI: https://doi.org/10.2307/4947
Baracchi, D., Dapporto, L., & Turillazzi, S. (2011). Relevance of wing morphology in distinguishing and classifying genera and species of Stenogastrinae wasps. Contributions to Zoology, 80(3), 191–199. https://doi.org/10.1163/18759866-08003003 DOI: https://doi.org/10.1163/18759866-08003003
Barão, K. R., Gonçalves, G. L., Mielke, O. H. H., Kronforst, M. R., & Moreira, G. R. P. (2014). Species boundaries in Philaethria butterflies: an integrative taxonomic analysis based on genitalia ultrastructure, wing geometric morphometrics, DNA sequences, and amplified fragment length polymorphisms. Zoological Journal of Linnean Society, 170, 690–709. https://doi.org/10.1111/zoj.12118 DOI: https://doi.org/10.1111/zoj.12118
Bates, P., & Harrison, D. (1998). Bats of the Indian subcontinent. Biodiversity and Conservation, 7(10), 1383–1386. https://doi.org/10.1023/A:1017113501563 DOI: https://doi.org/10.1023/A:1017113501563
Birch, J. M. (1997). Comparing wing shape of bats: the merits of principal-components analysis and relative-warp analysis. Journal of Mammalogy, 78(4), 1187–1198. https://doi.org/10.2307/1383062 DOI: https://doi.org/10.2307/1383062
Blood, B. R., & McFarlane D. A. (1988). A new method of calculating the wing area of bats. Mammalia 52(4), 600–603. https://scholarship.claremont.edu/wmkeckscience/82/ DOI: https://doi.org/10.1515/mamm-1988-0419
Bookstein, F. L. (1991). Morphometric tools for landmark data. Geometry and Biology. Cambridge University Press. DOI: https://doi.org/10.1017/CBO9780511573064
Brunet-Rossinni, A. K., & Wilkinson, G. S. (2009). Methods for age estimation and the study of senescence in bats. 315–325. https://science.umd.edu/faculty/wilkinson/Brunet-Rossini_ch15.pdf
Cordeiro-Estrela, P., Baylac, M., Denys, C., & Polop, J. (2008). Combining geometric morphometrics and pattern recognition to identify interspecific patterns of skull variation: case study in sympatric Argentinian species of the genus Calomys (Rodentia: Cricetidae: Sigmodontinae). Biological Journal of the Linnean Society, 94(2), 365–378. https://doi.org/10.1111/j.1095-8312.2008.00982.x DOI: https://doi.org/10.1111/j.1095-8312.2008.00982.x
de Camargo, N. F., & de Oliveira, H. F. (2012). Sexual dimorphism in Sturnira lilium (Chiroptera, Phyllostomidae): can pregnancy and pup carrying be responsible for differences in wing shape?. Plos One, 7(11), e49734. https://doi.org/10.1371/journal.pone.0049734 DOI: https://doi.org/10.1371/journal.pone.0049734
Dietz, C., Dietz, I., & Siemers, B. M. (2006). Wing measurement variations in the five European horseshoe bat species (Chiroptera: Rhinolophidae). Journal of Mammalogy, 87(6), 1241–1251. https://www.jstor.org/stable/4126902 DOI: https://doi.org/10.1644/05-MAMM-A-299R2.1
dos Reis, S. F., Duarte, L. C., Monteiro, L. R., & Von Zuben, F. J. (2002). Geographic variation in cranial morphology in Thrichomys apereoides (Rodentia: Echimyidae). II. Geographic units, morphological discontinuities, and sampling gaps. Journal of Mammalogy, 83(2), 345–353. https://doi.org/10.1644/1545-1542(2002)083<0345:GVICMI>2.0.CO;2 DOI: https://doi.org/10.1644/1545-1542(2002)083<0345:GVICMI>2.0.CO;2
Fenton, M. B. (1990). The foraging behaviour and ecology of animal-eating bats. Canadian Journal of Zoology. 68(3), 411-422. https://doi.org/10.1139/z90-061 DOI: https://doi.org/10.1139/z90-061
Findley, J. S., & Black, H. (1983). Morphological and dietary structuring of a Zambian insectivorous bat community. Ecology, 64(4), 625–630. https://doi.org/10.2307/1937180 DOI: https://doi.org/10.2307/1937180
Francuski, L. J., Vujić, A., Kovačević, A., Ludoški, J., & Milankov, V. (2009). Identification of the species of the Cheilosia variabilis group (Diptera, Syrphidae) from the Balkan Peninsula using wing geometric morphometrics, with the revision of status of C. melanopa redi Vujić, 1996. Contributions to Zoology, 78(3), 129–140. https://doi.org/10.1163/18759866-07803004 DOI: https://doi.org/10.1163/18759866-07803004
Hamidullah, Javid, A., Rasheed, S., Zeb, J., Ullah, A., Khan, M. I. & Attaullah. (2018). First record of Myotis formosus Hodgson's bat (Hodgson, 1835) from Bajaur Agency, Pakistan. The Journal of Animal & Plant Sciences, 28(4), 1199–1203 http://www.thejaps.org.pk/docs/v-28-04/33.pdf
Hedrick, B. P., & Dumont, E. R. (2018). Putting the leaf-nosed bats in context: a geometric morphometric analysis of three of the largest families of bats. Journal of Mammalogy, 99(5), 1042–1054. https://doi.org/10.1093/jmammal/gyy101 DOI: https://doi.org/10.1093/jmammal/gyy101
Herdina, A. N., Hulva, P., Horáček, I., Benda, P., Mayer, C., Hilgers, H., & Metscher, B. D. (2014). MicroCT imaging reveals morphometric baculum differences for discriminating the cryptic species Pipistrellus pipistrellus and P. pygmaeus. Acta Chiropterologica, 16(1), 157–168. https://doi.org/10.3161/150 811014X683372 DOI: https://doi.org/10.3161/150811014X683372
Javid, A., Mahmood-ul-Hassan, M., Afzal, M., Nadeem, M. S., Hussain, S. M. (2012). Recent record of least Pipistrelle (Pipistrellus tenuis)(Vespertilionidae: Chiroptera) from Islamabad. The Journal of Animal & Plant Sciences, 22(4), 1042–1047. http://www.thejaps.org.pk/docs/V-22-4/37.pdf
Javid, A., Mahmood-ul-Hassan, M., Hussain, S. M., & Iqbal, K. (2014). Recent record of the Asiatic lesser yellow house bat (Scotophilus kuhlii) from Punjab, Pakistan. Mammalia 78(1), 133–137. https://doi.org/10.1515/mammalia-2013-0012 DOI: https://doi.org/10.1515/mammalia-2013-0012
Kalcounis, M. C., & Brigham, R. M. J. (1995). Intraspecific variation in wing loading affects habitat use by little brown bats (Myotis lucifugus). Canadian Journal of Zoology, 73, 89-95. https://libres.uncg.edu/ir/uncg/f/M_Kalcounis-Ruppell_Intraspecific_1995.pdf DOI: https://doi.org/10.1139/z95-011
Klingenberg C. P. (2011). MorphoJ: an integrated software package for geometric morphometrics. Molecular Ecology Resources, 11(2), 353–357. https://doi.org/10.1111/j.1755-0998.2010.02924.x DOI: https://doi.org/10.1111/j.1755-0998.2010.02924.x
Mahmood-ul-Hassan, M., & Salim, M. (2014). Two new bat species (Chiroptera: Mammalia) for Pakistan: Miniopterus fuliginosus and Myotis formosus. Mammalia, 79, 125–129. https://doi.org/10.1515/mammalia-2013-0160 DOI: https://doi.org/10.1515/mammalia-2013-0160
McPeek, M. A. (1990). Behavioral differences between Enallagma species (Odonata) influencing differential vulnerability to predators. Ecology,71(5), 1714–1726. https://doi.org/10.2307/1937580 DOI: https://doi.org/10.2307/1937580
Meyer, C. F. J., Aguiar, L. M. S., Aguirre, L. F., Baumgarten, J., Clarke, F. M., Cosson, J. F., Villegas S. E., Fahr, J., Faria, D, Furey, N., Henry, M., Hodgkison, R., Jenkins, R., Jung, K., Kingston T., Kunz, T., Mac G. S., María C., Moya, M., …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, 143(11), 2797–2807. https://doi.org/10.1016/j.biocon.2010.07.029 DOI: https://doi.org/10.1016/j.biocon.2010.07.029
Michaux, B. (1989). Morphological variation of species through time. Biological Journal of the Linnean Society 38(3), 239–255. https://doi.org/10.1111/j.1095-8312.1989.tb01577.x DOI: https://doi.org/10.1111/j.1095-8312.1989.tb01577.x
Nedeljković, Z., Ačanski, J., Vujić, A., Obreht, D., Ðan, M., Ståhls, G. and Radenković, S. (2013), Taxonomy of Chrysotoxum festivum Linnaeus, 1758 (Diptera: Syrphidae)–an integrative approach. Zoological Journal of Linnean Society, 169(1), 84–102. https://doi.org/10.1111/zoj.12052 DOI: https://doi.org/10.1111/zoj.12052
Neto, J. M., Gordinho, L., Belda, E. J., Marín, M., Monrós, J. S., Fearon, P., & Crates, R. (2013). Phenotypic divergence among West European populations of reed bunting Emberiza schoeniclus: the effects of migratory and foraging behaviours. Plos One, 8(5), e63248. https://doi.org/10.1371/journal.pone. 0063248 DOI: https://doi.org/10.1371/journal.pone.0063248
Nogueira, M. R., Peracchi, A. L., & Monteiro, L. R. (2009). Morphological correlates of bite force and diet in the skull and mandible of phyllostomid bats. Functional Ecology, 23(4), 715–723. https://doi.org/10.1111/j.1365-2435.2009.01549.x DOI: https://doi.org/10.1111/j.1365-2435.2009.01549.x
Norberg, U. M. (1981). Flight, morphology and the ecological niche in some birds and bats. In: Day, M. H. (Ed.): Vertebrate Locomotion, Symposia Zoological Society London. Academic Press.
Ospina-Garcés, S. M., De Luna, E., Herrera, M. L. G., & Flores-Martínez, J. J. (2016). Cranial shape and diet variation in Myotis species (Chiroptera: Vespertilionidae): testing the relationship between form and function. Acta Chiropterologica, 18(1), 163–180. https://doi.org/10.3161/15081109ACC2016.18.1.007 DOI: https://doi.org/10.3161/15081109ACC2016.18.1.007
Paunović, M., & Stamenković, S. J. M. (1998). A revision of the distribution and status of Rhinolophus euryale Blasius, 1853 and Rhinolophus blasii Peters, 1866 (Rhinolophidae) in Yugoslavia, based on the discrimination properties of distinctive morphological characters. Myotis, 36, 7–23. https://eurekamag.com/research/037/701/037701220.php
Pepinelli, M., Spironello, M., & Currie, D. C. (2013). Geometric morphometrics as a tool for interpreting evolutionary transitions in the black fly wing (Diptera: Simuliidae). Zoological Journal of the Linnean Society,169(2), 377–388. https://doi.org/10.1111/zoj.12065 DOI: https://doi.org/10.1111/zoj.12065
Perveen, F., & Faiz-ur-Rehman, (2015). Characteristics of the first record of bat (Mammalia: Chiroptera) fauna from Peshawar and adjacent areas, Khyber Pakhtunkhwa, Pakistan. Global Journal of Animal Scientific Reseaerch, 3(1), 148–160. http://archives.gjasr.com/index.php/GJASR/article/view/135/370
Richards, L. R., Taylor, P. J., Schoeman, M. C., Goodman, S. M., Daele, P. A. A. G. V., & Lamb, J. M. (2012). Cranial size and shape variation in Afrotropical Otomops (Mammalia: Chiroptera: Molossidae): testing species limits using a morphometric approach. Biological Journal of the Linnean Society, 106(4), 910–925. https://doi.org/10.1111/j.1095-8312.2012.01899.x DOI: https://doi.org/10.1111/j.1095-8312.2012.01899.x
Riedel, A., Sagata, K., Suhardjono, Y. R., Tänzler, R., & Balke, M. (2013). Integrative taxonomy on the fast track-towards more sustainability in biodiversity research. Frontiers in Zoology, 10, 15. https://doi.org/10.1186/1742-9994-10-15 DOI: https://doi.org/10.1186/1742-9994-10-15
Roberts, T. J. (1997). The mammals of Pakistan (Revised Ed.) Oxford University Press.
Rohlf, F. (2010a). tpsDig, Digitize Landmarks and Outlines, (Version 2.16). Department of Ecology and Evolution. State University of New York, Stony Brook.
Rohlf, J. (2010b). tpsUtil. (Version 1.46), Department of Ecology and Evolution. State University of New York, Stony Brook.
Salim, M., Javid, A., Hussain, A., Faiz-ur-Rahman, & Hamidullah, (2016). First provincial record of desert yellow bat Scotoecus pallidus (Dobson, 1876) from Khyber Pakhtunkhwa, Pakistan. Punjab University Journal of Zoology, 31(2), 171–175. https://researcherslinks.com/current-issues/First-provincial-record/26/1/1913
Schmieder, D. A., Benítez, H. A., Borissov, I. M., & Fruciano, C. (2015). Bat species comparisons based on external morphology: A test of traditional versus geometric morphometric approaches. Plos One, 10(5), e0127043. https://doi.org/10.1371/journal.pone.0127043 DOI: https://doi.org/10.1371/journal.pone.0127043
Sevcik, M. (2003). Does wing morphology reflect different foraging strategies in sibling bat species Plecotus auritus and P. austriacus? Folia Zoologica, 52(2), 121–126. https://www.ivb.cz/wp-content/uploads/52_121-126.pdf
Von Busse, R., Hedenström, A., Winter, Y., & Johansson, L. C. (2012). Kinematics and wing shape across flight speed in the bat, Leptonycteris yerbabuenae. Biology Open 1(12), 1226–1238. https://doi.org/10.1242/bio.20122964 DOI: https://doi.org/10.1242/bio.20122964
Zelditch, M. L., Swiderski, D. L., & Sheets, H. D. (2012). Geometric morphometrics for Biologists: A primer. Academic Press. https://doi.org/10.1016/C2010-0-66209-2