PL EN


Preferencje help
Widoczny [Schowaj] Abstrakt
Liczba wyników
2014 | 16 | 1 |

Tytuł artykułu

MicroCT imaging reveals morphometric baculum differences for discriminating the cryptic species Pipistrellus pipistrellus and P. pygmaeus

Warianty tytułu

Języki publikacji

EN

Abstrakty

EN
With the recent and continuing discovery of further cryptic bat species, it is essential to find morphological species discriminating characters. Pipistrellus pipistrellus (common pipistrelle) and Pipistrellus pygmaeus (soprano pipistrelle) have been recognized as separate species since 1997, but no reliable morphological species discriminating trait has yet been found. The most commonly used morphological species discrimination traits are ‘wing vein’ pattern and shape and color of the penis, but these have not been validated on sets of genetically identified specimens. The baculum (os penis) has long been used successfully in species discrimination in bats and other mammals. In this study, we tested the reliability of the established traits and demonstrated how to reliably separate the common pipistrelle and the soprano pipistrelle by simple baculum measurements. The bacula of museum specimens of these two species and of Pipistrellus hanaki were imaged with high-resolution microCT. Several measurements were taken on the size-calibrated volume images, and their value for species discrimination was tested by discriminant analysis with leave-one-out cross validation. We showed that P. pipistrellus and P. pygmaeus specimens can be discriminated by measuring the projected length, height, and width of the baculum (n = 48; all but one classified correctly). Geometric morphometrics was used to analyze and locate variations in baculum shape. Principal component analysis of baculum variation was not sufficient to separate these species. Most of the interspecific variation in baculum shape can be found in the proximal third (the base) of the baculum, and most individual variation can be observed in lateral view, especially in the dorsoventral curve. Quantitative details of morphology are becoming more important to distinguish cryptic species and understand their phylogeographic distributions. The simple baculum measurements can be used to classify single specimens and could be taken without microCT, on a resected baculum.

Słowa kluczowe

Wydawca

-

Rocznik

Tom

16

Numer

1

Opis fizyczny

p.157-168,fig.,ref.

Twórcy

autor
  • Department of Theoretical Biology, Faculty of Life Sciences, University of Vienna, Althanstrasse 14, A-1090 Vienna, Austria
autor
  • Department of Zoology, Faculty of Science, Charles University, Vinicna 7, CZ-128 44 Praha 2, Czech Republic
  • Life Science Research Centre, Faculty of Science, University of Ostrava, Chittussiho 10, CZ-710 00 Ostrava, Czech Republic
autor
  • Department of Zoology, Faculty of Science, Charles University, Vinicna 7, CZ-128 44 Praha 2, Czech Republic
autor
  • Department of Zoology, Faculty of Science, Charles University, Vinicna 7, CZ-128 44 Praha 2, Czech Republic
  • Department of Zoology, National Museum (Natural History), Vaclavske Namesti 68, CZ-115 79 Praha 1, Czech Republic
autor
  • Department of Theoretical Biology, Faculty of Life Sciences, University of Vienna, Althanstrasse 14, A-1090 Vienna, Austria
autor
  • Department of Integrative Zoology, Faculty of Life Sciences, University of Vienna, Althanstrasse 14, A-1090 Vienna, Austria
  • Department of Theoretical Biology, Faculty of Life Sciences, University of Vienna, Althanstrasse 14, A-1090 Vienna, Austria

Bibliografia

  • 1. D. V. Abramochkin , G. S. Sukhova , and L. V. Rozenshtraukh . 2006. Effect of acetylcholine on the action potential in bat atrium and ventricle. Doklady Biological Sciences, 407: 121–122. Google Scholar
  • 2. D. C. Adams , F. J. Rohlf , and D. E. Slice . 2004. Geometric morphometrics: ten years of progress following the ‘revolution’. Italian Journal of Zoology, 71: 5–16. Google Scholar
  • 3. G. Arnqvist 1998. Comparative evidence for the evolution of genitalia by sexual selection. Nature, 393: 784–786. Google Scholar
  • 4. N. Açan-Bayedmir , and I. Albayrak . 2006. A study on the breeding biology of some bat species in Turkey (Mammalia: Chiroptera). Turkish Journal of Zoology, 30: 103–110. Google Scholar
  • 5. G. Azzali , M. L. Arcari , B. Spaggiari , and G. Romita . 2003. Ultrastructural aspects of the follicular cells of the pars tuberalis in bats related to the seasonal cycle. The Anatomical Record, 273A: 763–771. Google Scholar
  • 6. H. Baagøe 1977. Age determination in bats. Videnskabelige Meddelelser Dansk Naturhistorisk Forening, 140: 53–92. Google Scholar
  • 7. A. J. Baker , C. H. Daugherty , R. Colbourne , and J. L. McLennan . 1995. Flightless brown kiwis of New Zealand possess extremely subdivided population structure and cryptic species like small mammals. Proceedings of the National Academy of Sciences of the United States of America, 92: 8254–8258. Google Scholar
  • 8. K. E. Barlow , and G. Jones . 1999. Roosts, echolocation calls and wing morphology of two phonic types of Pipistrellus pipistrellus. Zeitschrift für Säugetierkunde, 64: 257–268. Google Scholar
  • 9. K. E. Barlow , G. Jones , and E. M. Barratt . 1997. Can skull morphology be used to predict ecological relationships between bat species? A test using two cryptic species of pipistrelle. Proceedings of the Royal Society, 264B: 1695–1700. Google Scholar
  • 10. E. M. Barratt , M. W. Bruford , T. M. Burland , P. A. Racey , and R. K. Wayne . 1995. Characterization of mitochondrial DNA variability within the microchiropterean genus Pipistrellus: approaches and applications. Symposia of the Zoological Society of London, 67: 377–386. Google Scholar
  • 11. E. M. Barratt , R. Deaville , T. M. Burland , M. W. Bruford , G. Jones , P. A. Racey , and R. K. Wayne . 1997. DNA answers the call of pipistrelle bat species. Nature, 387: 138–139. Google Scholar
  • 12. T. Bartonička 2008. Cimex pipistrelli (Heteroptera, Cimicidae) and the dispersal propensity of bats: an experimental study. Parasitology Research, 104: 163–168. Google Scholar
  • 13. T. Bartonička , A. Bielik , and Z. Řehák . 2008. Roost switching and activity patterns in the soprano pipistrelle, Pipistrellus pygmaeus, during lactation. Annales Zoologici Fennici, 45: 503–512. Google Scholar
  • 14. T. Bartonička , P. Kañuch , B. Bímová , and J. Bryja . 2010. Olfactory discrimination between two cryptic species of bats Pipistrellus pipistrellus and P. pygmaeus. Folia Zoologica, 59: 175–182. Google Scholar
  • 15. N. I. Becker , J. A. Encarnação , M. Tschapka , and E. K. V. Kalko . 2013. Energetics and life-history of bats in comparison to small mammals. Ecological Research, 28: 249–258. Google Scholar
  • 16. P. Benda , and P. Vallo . 2012. New look on the geographical variation in Rhinolophus clivosus with description of a new horseshoe bat species from Cyrenaica, Libya. Vespertilio, 16: 69–96. Google Scholar
  • 17. P. Benda , P. Hulva , M. Andreas , and M. Uhrin . 2003. Notes on the distribution of Pipistrellus pipistrellus complex in the Eastern Mediterranean: first records of P. pipistrellus for Syria and of P. pygmaeus for Turkey. Vespertilio, 7: 87–95. Google Scholar
  • 18. P. Benda , P. Hulva , and J. Gaisler . 2004. Systematic status of African populations of Pipistrellus pipistrellus complex (Chiroptera: Vespertilionidae), with a description of a new species from Cyrenaica, Libya. Acta Chiropterologica, 6: 193–217. Google Scholar
  • 19. P Benda , V. Hanák , I. Horáček , P. Hulva , R. Lučan , and M. Ruedi . 2007. Bats (Mammalia: Chiroptera) of the eastern Mediterranean. Part 5. Bat fauna of Cyprus: review of records with confirmation of six species new for the island and description of a new subspecies. Acta Societatis Zoologicae Bohemicae, 71: 71–130. Google Scholar
  • 20. A. Bielik 2007. Letová aktivita netopierov z reprodukčnej kolónie Pipistrellus pygmaeus v laktačnom a postlaktačnom období s využitím telemetrie a detektoringu. M.Sci. Thesis, Masarykova Univerzita, Brno, 61 pp. Google Scholar
  • 21. W. Bogdanowicz 2009. Analysis of bat morphology. Pp. 409– 435, in Ecological and behavioral methods for the study of bats, 2nd edition ( T. H. Kunz and S. Parsons , eds.). Johns Hopkins University Press, Baltimore, 901 pp. Google Scholar
  • 22. F. Bookstein 1997. Landmark methods for forms without landmarks: morphometrics of group differences in outline shape. Medical Image Analysis, 1: 225–243. Google Scholar
  • 23. R. E. Brown 1967. Bacula of some New World molossid bats. Mammalia, 31: 645–667. Google Scholar
  • 24. E. M. Bruna , R. N. Fisher , and T. J. Case . 1996. Morphological and genetic evolution appear decoupled in Pacific skinks (Squamata: Scincidae: Emoia). Proceedings of the Royal Society, 263B: 681-688. Google Scholar
  • 25. J. Bryja , P. Kaňuch , A. Fornůsková , T. Bartonička , and Z. Řehák . 2009. Low population genetic structuring of two cryptic bat species suggests their migratory behaviour in continental Europe. Biological Journal of the Linnean Society, 96: 103–114. Google Scholar
  • 26. I. Danielsson , and C. Askenmo . 1999. Male genital traits and mating interval affect male fertilisation success in the water strider Gerris lacustris. Behavioral Ecology and Sociobiology, 46: 149–156. Google Scholar
  • 27. I. Davidson-Watts , S. Walls , and G. Jones . 2006. Differential habitat selection by Pipistrellus pipistrellus and Pipistrellus pygmaeus identifies distinct conservation needs for cryptic species of echolocating bats. Biological Conservation, 133: 118–127. Google Scholar
  • 28. S. Derouiche , M. Deville , M. L. Taylor , H. Akbar , J. Guillot , L. E. Carreto-Binaghi , M. Pottier , E. M. Aliouat , C. M. Aliouat-Denis , E. Dei-Cas , et al. 2009. Pneumocystis diversity as a phylogeographic tool. Memórias do Instituto Oswaldo Cruz, 104: 112–117. Google Scholar
  • 29. C. Dietz , and O. von Helversen . 2004. Illustrated identification key to the bats of Europe. Version 1.0 — electronic publication, 72 pp. Available at http://www.fledermaus-dietz.de/publications/publications.html. Google Scholar
  • 30. C. Dietz , O. von Helversen , and D. Nill . 2007. Handbuch der Fledermäuse Europas und Nordwestafrikas. Franckh-Kosmos Verlags GmbH, Stuttgart, 400 pp. Google Scholar
  • 31. W. G. Eberhard 1985. Sexual selection and animal genitalia. Harvard University Press Cambridge, MA, x + 244 pp. Google Scholar
  • 32. A. Evin , I. Horáček , and P. Hulva . 2011. Phenotypic diversification and island evolution of pipistrelle bats (Pipistrellus pipistrellus group) in the Mediterranean region inferred from geometric morphometrics and molecular phylogenetics. Journal of Biogeography, 38: 2091–2105. Google Scholar
  • 33. Ø. Hammer 2012. PAST PAleontological STatistics Version 2.17. Reference manual. Natural History Museum, University of Oslo, Oslo, 229 pp. Google Scholar
  • 34. ø. Hammer , D. A. T. Harper , and P. D. Ryan . 2001. PAST: Paleontological statistics software package for education and data analysis. Palaeontologia Electronica, 4: 1–9. http:// palaeo-electronica.org/2001_1/past/issue1_01.htm. Google Scholar
  • 35. U. Häussler , A. Nagel , M. Braun , and A. Arnold . 2000. External characters discriminating sibling species of european pipistrells, Pipistrellus pipistrellus (Schreber, 1774) and P. pygmaeus (Leach, 1825). Myotis, 37: 27–40. Google Scholar
  • 36. J. L. Hill , and D. L. Harrison . 1987. The baculum in the Vespertilioninae (Chiroptera: Vespertilionidae) with a systematic review, a synopsis of Pipistrellus and Eptesicus, and the descriptions of a new genus and subgenus. Bulletin of the British Museum (Natural History) Zoology, 52: 225–305. Google Scholar
  • 37. I. Horáček , and V. Hanák . 1985. Generic status of Pipistrellus savii and comments on classification of the genus Pipistrellus (Chiroptera, Vespertilionidae). Myotis, 23–24: 9–16. Google Scholar
  • 38. D. J. Hosken , and P. Stockley . 2004. Sexual selection and genital evolution. Trends in Ecology and Evolution, 19: 87–93. Google Scholar
  • 39. C. M. House , and L. W. Simmons . 2002. Genital morphology and fertilization success in the dung beetle Onthophagus taurus: an example of sexually selected male genitalia. Proceedings of the Royal Society, 270B: 447–455. Google Scholar
  • 40. P. Hulva , I. Horáček , P. P. Strelkov , and P. Benda . 2004a. Molecular architecture of Pipistrellus pipistrellus/Pipistrellus pygmaeus complex (Chiroptera: Vespertilionidae): further cryptic species and Mediterranean origin of the divergence. Molecular Phylogenetics and Evolution, 32: 1023–1035. Google Scholar
  • 41. I. Hulva , I. Horáček , P. P. Strelkov , and P. Benda . 2004b. Phylogeography of Pipistrellus pipistrellus/P. pygmaeus complex (Chiroptera: Vespertilionidae). Bat Research News, 45: 120. Google Scholar
  • 42. P. Hulva , P. Benda , V. Hanák , A. Evin , and I. Horáček . 2007. New mitochondrial lineages within the Pipistrellus pipistrellus complex from Mediterranean Europe. Folia Zoologica, 56: 378–388. Google Scholar
  • 43. P. Hulva , A. Fornůsková , A. Chudárková , A. Evin , B. Allegrini , P. Benda , and J. Bryja . 2010. Mechanisms of radiation in a bat group from the genus Pipistrellus inferred by phylogeography, demography and population genetics. Molecular Ecology, 19: 5417–5431. Google Scholar
  • 44. C. Ibáñez , J. L. García-Mudarra , M. Ruedi , B. Stadelmann , and J. Juste . 2006. The Iberian contribution to cryptic diversity in European bats. Acta Chiropterologica, 8: 277–297. Google Scholar
  • 45. K. Isaksen , and M. Landsgard . 2007. The soprano pipistrelle Pipistrellus pygmaeus confirmed as a wintering species in Norway. Fauna (Oslo), 60: 212–225. Google Scholar
  • 46. G. Jones , and K. E. Barlow . 2001. Cryptic species of echolocating bats. Pp. 345–349, in Echolocation in bats and dolphins ( J. A. Thomas , C. F. Moss , and M. Vater , eds.). University of Chicago Press, Chicago, xxvii + 604 pp. Google Scholar
  • 47. G. Jones , and S. M. van Parijs . 1993. Bimodal echolocation in pipistrelle bats: are cryptic species present? Proceedings of the Royal Society, 251B: 119–125. Google Scholar
  • 48. P. Kaňuch , P. Hájková , Z. Řehák , and J. Bryja . 2007. A rapid PCR-based test for species identification of two cryptic bats Pipistrellus pipistrellus and P. pygmaeus and its application on museum and dropping samples. Acta Chiropterologica, 9: 277–282. Google Scholar
  • 49. P Kañuch , A. Fornůsková , T. Bartonička , J. Bryja , and Z. Řehák . 2010. Do two cryptic pipistrelle bat species differ in their autumn and winter roosting strategies within the range of sympatry. Folia Zoologica, 59: 102–107. Google Scholar
  • 50. J. Kusch , and A. Schmitz . 2013. Environmental factors affecting the differential use of foraging habitat by three sympatric species of Pipistrellus. Acta Chiropterologica, 15: 57–67. Google Scholar
  • 51. C. A. Long , and T. Frank . 1968. Morphometric variaton and function in the baculum, with comments on correlation of parts. Journal of Mammalogy, 49: 32–43. Google Scholar
  • 52. S. Lüpold , A. G. McElligott , and D. J. Hosken . 2004. Bat genitalia: allometry, variation and good genes. Biological Journal of the Linnean Society, 83: 497-507. Google Scholar
  • 53. M. Ø. Madsen 2013. Phenotypic divergence of the three-spined stickleback (Gasterosteus aculeatus) — relating body shape and habitat. M.Sci. Thesis, Universität Wien, Vienna, 71 pp. Google Scholar
  • 54. F. Mayer , and O. von Helversen . 2001a. Cryptic diversity in European bats. Proceedings of the Royal Society, 268B: 1825–1832. Google Scholar
  • 55. F. Mayer , and O. von Helversen . 2001b. Sympatric distribution of two cryptic bat species across Europe. Biological Journal of the Linnean Society, 74: 365–374. Google Scholar
  • 56. F. Mayer , C. Dietz , and A. Kiefer . 2007. Molecular species identification boosts bat diversity. Frontiers in Zoology, 4: 5. Google Scholar
  • 57. E. Mayr 1942. Systematics and the origin of species. Columbia University Press, New York, xxxv + 334 pp. Google Scholar
  • 58. B. D. Metscher 2011. X-ray microtomographic imaging of intact vertebrate embiyos. Cold Spring Harbor Protocols, 2011: 1462-1471. Google Scholar
  • 59. P. Mitteröcker , and F. Bookstein . 2011. Linear discrimination, ordination, and the visualization of selection gradients in modern morphometrics. Evolutionary Biology, 38: 100–114. Google Scholar
  • 60. P Mitteröcker , and P. Gunz . 2009. Advances in geometric morphometrics. Evolutionary Biology, 36: 235–247. Google Scholar
  • 61. I. Pavlinić , N. Tvrtković and D. Holcer . 2008. Morphological identification of the soprano pipistrelle (Pipistrellus pygmaeus Leach, 1825) in Croatia. Hystrix — Italian Journal of Mammalogy (N.S.), 19: 47–53. Google Scholar
  • 62. K. J. Petrželková , N. C. Downs , J. Zukal , and P. A. Racey . 2009. A comparison between emergence and return activity in pipistrelle bats Pipistrellus pipistrellus and P. pygmaeus. Acta Chiropterologica, 8: 381–390. Google Scholar
  • 63. P. A. Racey , E. M. Barratt , T. M. Burland , R. Deaville , D. Gotelli , G. Jones , and S. B. Piertney . 2007. Microsatellite DNA polymorphism confirms reproductive isolation and reveals differences in population genetic structure of cryptic pipistrelle bat species. Biological Journal of the Linnean Society, 90: 539–550. Google Scholar
  • 64. Z. Řehák , T. Bartonička , and A. Bielik . 2004. Distributional status of Pipistrellus pipistrellus (Schreber, 1774) and P. pygmaeus (Leach, 1825) in the Czech Republic: results of mapping. Bat Research News, 45: 145. Google Scholar
  • 65. S. Renaud , P. Alibert , and J.-C. Auffray . 2009. Mandible shape in hybrid mice. Naturwissenschaften, 96: 1043–1050. Google Scholar
  • 66. F. Rohlf , and D. Slice . 1990. Extensions of the Procrustes method for the optimal superimposition of landmarks. Systematic Biology, 39: 40–59. Google Scholar
  • 67. J. M. Russ , G. Jones , and P. A. Racey . 2005. Responses of soprano pipistrelles, Pipistrellus pygmaeus, to their experimentally modified distress calls. Animal Behaviour, 70: 397–404. Google Scholar
  • 68. I. Salicini , C. Ibáñez , and J. Juste . 2013. Deep differentiation between and within Mediterranean glacial refugia in a flying mammal, the Myotis nattereri bat complex. Journal of Biogeography, 40: 1182–1193. Google Scholar
  • 69. T. Sattler 2003. Ecological factors affecting the distribution of the sibling species Pipistrellus pygmaeus and Pipistrellus pipistrellus in Switzerland. M.Sci. Thesis, Universität Bern, Bern, 78 pp. Google Scholar
  • 70. T. Sendor , I. Roedenbeck , S. Hampl , M. Ferreri , and M. Simon . 2002. Revision of morphological identification of pipistrelle bat phonic types (Pipistrellus pipistrellus Schreber, 1774). Myotis, 40: 11–17. Google Scholar
  • 71. P. G. Smith , and P. A. Racey . 2009. Selection of timber mortises in a church roof by Pipistrellus sp. at 52 degrees N. Acta Chiropterologica, 11: 205–207. Google Scholar
  • 72. F. Spitzenberger , P. P. Strelkov , H. Winkler , and E. Haring . 2006. A preliminary revision of the genus Plecotus (Chiroptera, Vespertilionidae) based on genetic and morphological results. Zoologica Scripta, 35: 187–230. Google Scholar
  • 73. A. Sztencel-Jabłonka , and W. Bogdanowicz . 2012. Population genetics study of common (Pipistrellus pipistrellus) and soprano (Pipistrellus pygmaeus) pipistrelle bats from central Europe suggests interspecific hybridization. Canadian Journal of Zoology, 90: 1251–1260. Google Scholar
  • 74. A. Sztencel-Jabłonka , G. Jones , and W. Bogdanowicz . 2009. Skull morphology of two cryptic bat species: Pipistrellus pipistrellus and P. pygmaeus — a 3D geometric morphometrics approach with landmark reconstruction. Acta Chiropterologica, 11: 113–126. Google Scholar
  • 75. O. von Helversen , and M. Holderied . 2003. Zur Unterscheidung von Zwergfledermaus (Pipistrellus pipistrellus) und Mückenfledermaus (Pipistrellus mediterraneus/pygmaeus) im Feld. Nyctalus (N.F.), 8: 420–426. Google Scholar
  • 76. O. von Helversen , K. G. Heller , F. Mayer , A. Nemeth , M. Volleth , and P. Gombkötö . 2001. Cryptic mammalian species: a new species of whiskered bat (Myotis alcathoe n. sp.) in Europe. Naturwissenschaften, 88: 217–223. Google Scholar
  • 77. D. A. Waters , and J. G. Wong . 2007. The allocation of energy to echolocation pulses produced by soprano pipistrelles (Pipistrellus pygmaeus) during the wingbeat cycle. The Journal of the Acoustical Society of America, 121: 2990–3000. Google Scholar
  • 78. G. W. Weber , K. Schäfer , H. Prossinger , P. Gunz , P. Mitteröcker , and H. Seidler . 2001. Virtual anthropology: the digital evolution in anthropological sciences. Journal of Physiological Anthropology and Applied Human Science, 20:69-80. Google Scholar
  • 79. T. Ziegler , A. Feiler , and U. Zöphel . 2001. New data on the genital morphology of the midge bat Pipistrellus pygmaeus (Leach, 1825) from Germany (Mammalia: Chiroptera: Vespertilionidae). Zoologische Abhandlungen (Dresden), 51: 435–444. Google Scholar
  • 80. U. Zöphel , T. Ziegler , A. Feiler , and S. Pocha . 2002. First records of the midge bat, Pipistrellus pygmaeus (Leach, 1825), for Saxony (Mammalia: Chiroptera: Vespertilionidae). Faunistische Abhandlungen Staatliches Museum für Tierkunde Dresden, 22: 411–422. Google Scholar

Uwagi

Rekord w opracowaniu

Typ dokumentu

Bibliografia

Identyfikatory

Identyfikator YADDA

bwmeta1.element.agro-b611b4f2-7ba5-4a5f-b1d5-7a199c637056
JavaScript jest wyłączony w Twojej przeglądarce internetowej. Włącz go, a następnie odśwież stronę, aby móc w pełni z niej korzystać.