Echolocation call analysis and presence-only modelling as conservation monitoring tools for rhinolophoid bats in Thailand

• Autorzy: Hughes A.C. , Satasook C. , Bates P. J. J. , Soisook P. , Sritongchuay T. , Jones G. , Bumrungsri S.
• Języki publikacji: EN

Abstrakty

EN

Bats are an important component of biodiversity in Southeast Asia, and are key indicators of habitat quality. Acoustic analysis of echolocation calls not only allows the identification of bat species that are difficult to capture, but also allows for rapid and standardised ways to survey and monitor bats over large areas. However keys based on call parameters must also account for geographic variation in call parameters, and consider any effects of morphology and sex on call frequency. Presence-only modelling can predict likely geographic locations of specific taxa, and can used to refine decision making so that species unlikely to occur in a specific region can be omitted from more localised acoustic libraries. Here we develop an acoustic library for the echolocation calls of rhinolophoid bats in Thailand, and use presence-only modelling (Maxent) to explore how species with similar calls in a library developed at the national level can sometimes be largely allopatric, and hence identifiable, once geographic range is predicted. Presence-only modelling can also be used to explore whether species with similar calls adjust call frequency in likely areas of sympatry. We analysed calls from fourteen species of rhinolophid and twelve hipposiderid species from Thailand. Calls from a further three rhinolophid and one hipposiderid species are also described but not analysed statistically because of small sample sizes. Even without considering geographic variation, 69% of rhinolophid (14 species with a minimum of five individuals/ species) and 91% of hipposiderid calls (12 species) could be classified successfully to species using two call parameters (frequency of most energy (FMAXE) and duration) in a discriminant function analysis. Most of the discrimination was achieved because species often utilised different frequency bands. Morphology can also affect call frequency both across and within species. In both rhinolophids and hipposiderid families there was a negative relationship between FMAXE and forearm length. Within species, FMAXE was negatively related to forearm length in Rhinolophus microglobosus, R. pusillus and R. thomasi, and positively related to forearm length in R. affinis and R. pearsonii. Male R. pusillus called at higher frequencies than females, although there was no sexual size dimorphism in forearm length. Call frequency was negatively related to relative humidity in R. pusillus, suggesting that bats called at lower frequencies in humid environments to counter increases in atmospheric attenuation. Presence-only modelling was used to show that some species with similar call frequencies (e.g., R. lepidus and R. microglobosus; R. yunanensis and R. trifoliatus are predicted to occur largely in allopatry, and so could be identified reliably in particular parts of the country. Presenceonly modeling can assist in predicting areas of overlap between species with similar call frequencies. Other species (e.g., R. malayanus, R. coelophyllus) overlap in frequency when data from all of Thailand are combined, but seem to avoid call overlap when syntopic. Hence acoustic identification can be improved by taking into account local distribution patterns and patterns of species coexistence. The creation of call libraries at a local scale would have extensive potential as a resource to monitor changes in species distributions through time.

• Wydawca: -
• Czasopismo: Acta Chiropterologica
• Rocznik: 2010
• Tom: 12
• Numer: 2
• Opis fizyczny: p.311-327,ref.

Twórcy

autor

Hughes A.C.

• School of Biological Sciences, University of Bristol, Woodland Road, Bristol, BS8 1UG, United Kingdom

autor

Satasook C.

• Princess Maha Chakri Sirindhorn Natural History Museum, Faculty of Science, Prince of Songkla University, 15 Karnjanavanit Road, Hat Yai, Songkhla 90112, Thailand

autor

Bates P. J. J.

• Harrison Institute, Centre for Systematics and Biodiversity Research, Bowerwood House, 15 St Botolph's Road, Sevenoaks, Kent, TN13 3AQ, United Kingdom

autor

Soisook P.

• Princess Maha Chakri Sirindhorn Natural History Museum, Faculty of Science, Prince of Songkla University, 15 Karnjanavanit Road, Hat Yai, Songkhla 90112, Thailand

autor

Sritongchuay T.

• Princess Maha Chakri Sirindhorn Natural History Museum, Faculty of Science, Prince of Songkla University, 15 Karnjanavanit Road, Hat Yai, Songkhla 90112, Thailand

autor

Jones G.

• School of Biological Sciences, University of Bristol, Woodland Road, Bristol, BS8 1UG, United Kingdom

autor

Bumrungsri S.

• Princess Maha Chakri Sirindhorn Natural History Museum, Faculty of Science, Prince of Songkla University, 15 Karnjanavanit Road, Hat Yai, Songkhla 90112, Thailand

Bibliografia

• 1. F. Achard , H. D. Eva , H. J. Stibig , P. Mayaux , J. Gallego , T. Richards , and J. P. Malingreau . 2002. Determination of deforestation rates of the world's humid tropical forests. Science, 297: 999–1002. Google Scholar
• 2. K. N. Armstrong , and R. B. Coles . 2007. Echolocation call frequency differences between geographic isolates of Rhinonicteris aurantia (Chiroptera: Hipposideridae): implications of nasal chamber size. Journal of Mammalogy, 88: 94–104. Google Scholar
• 3. W. Bogdanowicz 1990. Geographic variation and taxonomy of Daubenton's bat, Myotis daubentoni, in Europe. Journal of Mammalogy, 71: 205–218. Google Scholar
• 4. S. Bumrungsri , D. L. Harrison , C. Satasook , A. Prajukjitr , S. Thong-Aree , and P. J. J. Bates . 2006. A review of bat research in Thailand with eight new species records for the country. Acta Chiropterologica, 8: 325–359. Google Scholar
• 5. M. Cardillo , G. M. Mace , J. L. Gittleman , and A. Purvis . 2006. Latent extinction risk and the future battlegrounds of mammal conservation. Proceedings of the National Academy of Sciences of the USA, 103: 4157–61. Google Scholar
• 6. S.-F. Chen , G. Jones , and S. J. Rossiter . 2009. Determinants of echolocation call frequency variation in the Formosan lesser horseshoe bat (Rhinolophus monoceros). Proceedings of the Royal Society of London, 276B: 3901–3909. Google Scholar
• 7. S. J. B. Cooper , P. R. Day , T. B. Reardon , and M. Schulz . 2001. Assessment of species boundaries in Australian Myotis (Chiroptera: Vespertilionidae) using mitochondrial DNA. Journal of Mammalogy, 82: 328–338. Google Scholar
• 8. B. Douangboubpha , S. Bumrungsri , P. Soisook , S. W. Murray , S.B. Puechmaille , C. Satasook , S. S. H. Bu , D. L. Harrison , and P. J. J. Bates . 2010. A taxonomic review of Hipposideros halophyllus, with additional information on H. ater and H. cineraceus (Chiroptera: Hipposideridae) from Thailand and Myanmar. Acta Chiropterologica, 12: 29–50. Google Scholar
• 9. C. M. Francis 2008. Mammals of Thailand and South-East Asia. Asia Books, Bangkok, Thailand, 392 pp. Google Scholar
• 10. N. M. Furey , I. J. MacKie , and P. A Racey . 2009. The role of ultrasonic detectors in improving inventory and monitoring surveys in Vietnamese karst bat assemblages. Current Zoology, 55:327–341. Google Scholar
• 11. M. R. Gannon , and M. R. Willig . 1998. Long-term monitoring protocol for bats: lessons from the Luquillo Experimental Forest of Puerto Rico. Pp. 271–291, in Forest biodiversity in North, Central and South America, and the Caribbean. Research and Monitoring ( F. Dallmeir and J. A. Comiskey , eds.). Man and the Biosphere Series, 21. UNESCO and The Parthenon Publishing Group, Paris. Google Scholar
• 12. A. Guillén , J. Juste , and C. Ibáñez . 2000. Variation in the frequency of the echolocation calls of Hipposideros ruber in the Gulf of Guinea: an exploration of the adaptive meaning of the constant frequency value in rhinolophoid CF bats. Journal of Evolutionary Biology, 13: 70–80. Google Scholar
• 13. T. J. J. Hanebuth , K. Stattegger , and A. Bojanowski . 2009. Termination of the Last Glacial Maximum sea-level lowstand: the Sunda-Shelf data revisited. Global and Planetary Change, 66: 76–84. Google Scholar
• 14. K.-G. Heller , and O. Von Helversen . 1989. Resource partitioning of sonar frequency bands in rhinolophoid bats. Oecologia, 80: 178–186. Google Scholar
• 15. A. H. Hirzel , J. Hausser , D. Chessel , and N. Perrin . 2002. Ecological-niche factor analysis: how to compute habitat suitability maps without absence data. Ecology, 83: 2027–2036. Google Scholar
• 16. S. Hiryu , K. Katsura , L.-K. Lin , H. Riquimaroux , and Y. Watanabe . 2005. Doppler-shift compensation in the Taiwanese leaf-nosed bat (Hipposideros terasensis) recorded with a telemetry microphone system during flight. Journal of the Acoustic Society of America, 118: 3927–3933. Google Scholar
• 17. R. D. Houston , A. M. Boonman , and G. Jones . 2003. Do echolocation signal parameters restrict bats' choice of prey? Pp. 339–345, in Echolocation in bats and dolphins ( J. A. Thomas , C. F. Moss , and M. Vater , eds.). University of Chicago Press, Chicago, Illinois, 631 pp. Google Scholar
• 18. A. M. Hutson , S. P. Mickleburgh , and P. A. Racey (comp.). 2001. Microchiropteran bats: global status survey and conservation action plan. IUCN/SSC Chiroptera Specialist Group, IUCN, Gland, Switzerland, x + 258 pp. Google Scholar
• 19. D. S. Jacobs , R. M. R. Barclay , and M. H. Walker . 2007. The allometry of echolocation call frequencies of insectivorous bats: why do some species deviate from the pattern? Oecologia, 152: 583–594. Google Scholar
• 20. G. Jones 1995. Variation in bat echolocation: implications for resource partitioning and communication. Le Rhinolophe, 11: 53–59. Google Scholar
• 21. G. Jones 1999. Scaling of echolocation call parameters in bats. Journal of Experimental Biology, 202: 3359–3367. Google Scholar
• 22. G. Jones , and K. E. Barlow . 2004. 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, Illinois, 631 pp. Google Scholar
• 23. G. Jones , and T. Kokurewicz . 1994. Sex and age variation in echolocation calls and flight morphology of Daubenton's bats Myotis daubentonii. Mammalia, 58: 41–50. Google Scholar
• 24. G. Jones , and J. M. V. Rayner . 1991. Flight performance, foraging tactics and echolocation in the trawling insectivorous bat Myotis adversus (Chiroptera: Vespertilionidae). Journal of Zoology (London), 225: 393–412. Google Scholar
• 25. G. Jones , M. Morton , P. M. Hughes , and R. M. Budden . 1993. Echolocation, flight morphology and foraging strategies of some West African hipposiderid bats. Journal of Zoology (London), 230: 385–400. Google Scholar
• 26. G. Jones , D. S. Jacobs , T. H. Kunz , M. R. Willig , and P. A. Racey . 2009. Carpe noctem: the importance of bats as bioindicators. Endangered Species Research, 8: 93–115. Google Scholar
• 27. T. Kingston 2010. Research priorities for bat conservation in Southeast Asia: a consensus approach. Biodiversity and Conservation, 19: 471–484. Google Scholar
• 28. T. Kingston , G. Jones , A. Zubaid , and T. H. Kunz . 2000. Resource partitioning in rhinolophoid bats revisited. Oecologia, 124: 332–342. Google Scholar
• 29. T. Kingston , M. Lara , G. Jones , A. Zubaid , T. H. Kunz , and C. J. Schneider . 2001. Acoustic divergence in two cryptic Hipposideros species: a role for social selection? Proceedings of the Royal Society of London, 268B: 1381–1386. Google Scholar
• 30. T. Kingston , B. L. Lim , and A. Zubaid . 2006. Bats of Krau wildlife reserve. University Kebangsaan Malaysia, Bangalore, 145 pp. Google Scholar
• 31. J. M. Lamb , T. M. C. Ralph , S. M. Goodman , W. Bogdanowicz , J. Fahr , M. Gajewska , P. J. J. Bates , J. Eger , P. Benda , and P. J. Taylor . 2008. Phylogeography and predicted distribution of African-Arabian and Malagasy populations of giant mastiff bats, Otomops spp. (Chiroptera: Molossidae). Acta Chiropterologica, 10: 21–40. Google Scholar
• 32. B. D. Lawrence , and J. A. Simmons . 1982. Measurements of atmospheric attenuation at ultrasonic frequencies and the significance for echolocation by bats. Journal of the Acoustic Society of America, 71: 585–590. Google Scholar
• 33. G. Li , G. Jones , S. J. Rossiter , S.-F. Chen , S. Parsons , and S. Zhang . 2006. Phylogenetics of small horseshoe bats from east Asia based on mitochondrial DNA sequence variation. Journal of Mammalogy, 87: 1234–1240. Google Scholar
• 34. J. MacKinnon 1997. Protected areas system review of the Indo-Malayan realm. The Asian Bureau for Conservation Ltd., Canterbury, 198 pp. Google Scholar
• 35. G. M. C. MacSwiney , F. Clarke , and P. A. Racey . 2008. What you see is not what you get: the role of ultrasonic detectors in maximising inventory completeness in Neotropical forests. Journal of Applied Ecology, 45: 1364–1371. Google Scholar
• 36. B. Marwick 2009. Biogeography of Middle Pleistocene hominins in mainland Southeast Asia: a review of current evidence. Quaternary International, 202: 51–58. Google Scholar
• 37. P. Mayaux , P. Holmgren , F. Achard , H. Eva , H. J. Stibig , and A. Branthomme . 2005. Tropical forest cover change in the 1990s and options for future monitoring. Philosophical Transactions of the Royal Society of London. 360B: 373–384. Google Scholar
• 38. S. Mickleburgh , K. Waylen , and P. A. Racey . 2009. Bats as bushmeat — a global review. Oryx, 43: 217–234. Google Scholar
• 39. N. Myers , R. A. Mittermeier , C. G. Mittermeier , G. A. B. Da Fonseca , and J. Kent . 2000. Biodiversity hotspots for conservation priorities. Nature, 403: 853–858. Google Scholar
• 40. S. Parsons , and G. Jones . 2000. Acoustic identification of twelve species of echolocating bat by discriminant function analysis and artificial neural networks. Journal of Experimental Biology, 203: 2641–2656. Google Scholar
• 41. S. Pawar , M. S. Koo , C. Kelley , M. Firoz Ahmed , S. Chaudhuri , and S. Sarkar . 2007. Conservation assessment and prioritization of areas in Northeast India: priorities for amphibians and reptiles. Biological Conservation, 136: 346–361. Google Scholar
• 42. S. J. Phillips , R. P. Anderson , and R. E. Schapire . 2006. Maximum entropy modeling of species geographic distributions. Ecological Modelling, 190: 231–259. Google Scholar
• 43. S. Proches 2005. The world's biogeographical regions: cluster analyses based on bat distributions. Journal of Biogeography, 32: 607–614. Google Scholar
• 44. J. D. Pye 1979. Why ultrasound? Endeavour (N.S), 3: 57–62. Google Scholar
• 45. J. D. Pye 1993. Is fidelity futile? The ‘true’ signal is illusory, especially with ultrasound. Bioacoustics, 4: 271–286. Google Scholar
• 46. H. Rebelo , and G. Jones . 2010. Ground validation of presenceonly modelling with rare species: a case study on barbastelles Barbastella barbastellus (Chiroptera: Vespertilionidae). Journal of Applied Ecology, 47: 410–420. Google Scholar
• 47. H. Rebelo , P. Tarroso , and G. Jones . 2010. Predicted impact of climate change on European bats in relation to their biogeographic patterns. Global Change Biology, 16: 561–576. Google Scholar
• 48. M. F. Robinson 1996. A relationship between echolocation calls and noseleaf widths in bats of the genera Rhinolophus and Hipposideros. Journal of Zoology (London), 239: 389–393. Google Scholar
• 49. D. Russo , and G. Jones . 2000. The two cryptic species of Pipistrellus pipistrellus (Chiroptera: Vespertilionidae) occur in Italy: evidence from echolocation and social calls. Mammalia, 64: 187–197. Google Scholar
• 50. D. Russo , and G. Jones . 2002. Identification of twenty-two bat species (Mammalia: Chiroptera) from Italy by analysis of time-expanded recordings of echolocation calls. Journal of Zoology (London), 58: 98–103. Google Scholar
• 51. D. Russo , M. Mucedda , M. Bello , S. Biscardi , E. Pidinchedda , and G. Jones . 2007. Divergent echolocation call frequencies in insular rhinolophids (Chiroptera): a case of character displacement? Journal of Biogeography, 34: 2129–2138. Google Scholar
• 52. K. Safi , and B. M. Siemers . 2010. Implications of sensory ecology for species coexistence: biased perception links predator diversity to prey size distribution. Evolutionary Ecology, DOI 10.1007/s10682-009-9326-0. Google Scholar
• 53. G. Schuller , and G. Pollak . 1979. Disproportionate frequency representation in the inferior colliculus of Doppler-compensating greater horseshoe bats — evidence for an acoustic fovea. Journal of Comparative Physiology, 132: 47–54. Google Scholar
• 54. C. Sérgio , R. Figueira , D. Draper , R. Menezes , and A. J. Sousa . 2007. Modelling bryophyte distribution based on ecological information for extent of occurrence assessment. Biological Conservation, 135: 341–351. Google Scholar
• 55. B. M. Siemers , K. Beedholm , C. Dietz , I. Dietz , and T. Ivanova . 2005. Is species identity, sex, age or individual quality conveyed by echolocation call frequency in European horseshoe bats? Acta Chiropterologica, 7: 259–274. Google Scholar
• 56. N. S. Sodhi , L. P. Koh , B. W. Brook , and P. K. Ng . 2004. Southeast Asian biodiversity: an impending disaster. Trends in Ecology and Evolution, 19: 654–60. Google Scholar
• 57. N. S Sodhi , T. M. Brooks , L. P. Koh , G. Acciaioli , M. Erb , A. K.-J. Tan A , L. M. Curran , P. Brosius , T. M. Lee , J. M. Patlis , M. Gumal , and R. J. Lee . 2006. Biodiversity and human livelihood crises in the Malay Archipelago. Conservation Biology, 20: 1811–1813. Google Scholar
• 58. S. Bumrungsri Soisook. P. , C. Satasook , Vu Dinh Thong , Si Si Hla Bu , D. L. Harrison , and P.J. J. Bates . 2008. A taxonomic review of Rhinolophus stheno and R. malayanus (Chiroptera: Rhinolophidae) from continental Southeast Asia: an evaluation of echolocation call frequency in discriminating between cryptic species. Acta Chiropterologica, 10: 221–242. Google Scholar
• 59. P. Soisook , P. Niyomwan , M. Srikrachang , T. Srithongchuay , and P. J. J. Bates . 2010. Discovery of Rhinolophus beddomei (Chiroptera: Rhinolophidae) from Thailand with a brief comparison to other related taxa. Tropical Natural History, 10: 67–79. Google Scholar
• 60. S. Stoffberg , D. S. Jacobs , I. J. MacKie , and C. A. Matthee . 2010. Molecular phylogenetics and historical biogeography of Rhinolophus bats. Molecular Phylogenetics and Evolution, 54: 1–9. Google Scholar
• 61. K.-P. Sun , J. Feng , Z.-Z. Zhang , L.-J. Xu , and Y. Liu . 2009. Cryptic diversity in Chinese rhinolophids and hipposiderids (Chiroptera: Rhinolophidae and Hipposideridae). Mammalia, 73: 135–141. Google Scholar
• 62. K-P. Sun , J. Feng , T-L. Jiang , J. Ma , Z-Z. Zhang , and L-R. Jin . 2008a. A new cryptic species of Rhinolophus macrotis (Chiroptera: Rhinolophidae) from Jiangxi Province, China. Acta Chiropterologica, 10: 101–110. Google Scholar
• 63. K-P. Sun , J. Feng , L-G. Jin , Y. Liu , and Y-L. Jiang . 2008b. Identification of sympatric bat species by the echolocation calls. Frontiers of Biology in China, 2: 227–231. Google Scholar
• 64. A. Suyanto , and M. J. Struebig . 2007. Bats of the Sangkulirang limestone karst formations, East Kalimantan — a priority region for Bornean bat conservation. Acta Chiropterologica, 9: 67–95. Google Scholar
• 65. A. Thabah , D. S. J. Rossiter , T. Kingston , S. Zhang , S. Parsons , K. Mya My , A. Zubaid , and G. Jones . 2006. Genetic divergence and echolocation call frequency in cryptic species of Hipposideros larvatus sensu lato (Chiroptera: Hipposideridae) from the Indo-Malayan region. Biological Journal of the Linnean Society, 88: 119–130. Google Scholar
• 66. M. Trappe , and H.-U. Schnitzler . 1982. Doppler shift compensation in insect-catching horseshoe bats. Naturwissen-schaften, 69: 193–194. Google Scholar
• 67. N. Ulanovsky , B. Fenton M. , A. Tsoar , and C. Korine . 2004. Dynamics of jamming avoidance in echolocating bats. Proceedings of the Royal Society of London, 271B: 1467–1475. Google Scholar
• 68. N. Vaughan , G. Jones , and S. Harris . 1997. Identification of British bat species by multivariate analysis of echolocation call parameters. Bioacoustics, 7: 189–207. Google Scholar
• 69. X. M. Wang , X. J. Sun , P. X. Wang , and K. Stattegger . 2009. Vegetation on the Sunda shelf, South China Sea, during the last glacial maximum. Palaeogeography, Palaeoclimatology, Palaeoecology, 278: 88–97. Google Scholar
• 70. R. D. Warren , and M. S. Witter . 2002. Monitoring trends in bat populations through roost surveys: methods and data from Rhinolophus hipposideros. Biological Conservation, 105: 255–261. Google Scholar
• 71. D. S. Woodruff , and L. M. Turner . 2009. The Indochinese-Sundaic Zoogeographic transition: a description and analysis of terrestrial mammal species distributions. Journal of Biogeography, 36: 803–821. Google Scholar
• 72. Y. Wu , M. Harada , and M. Motokowa . 2009. Taxonomy of Rhinolophus yunanensis Dobson, 1872 (Chiroptera: Rhinolophidae) with a description of a new species from Thailand. Acta Chiropterologica, 11: 237–246. Google Scholar
• 73. H. Yoshino , S. Matsumura , K. Kinjo , H. Tamura , H. Ota , and M. Izawa . 2006. Geographical variation in echolocation call and body size of the Okinawan least horseshoe bat, Rhinolophus pumilus (Mammalia: Rhinolophidae), on Okinawa-jima island, Ryukyu archipelago, Japan. Zoological Science, 23: 661–667. Google Scholar
• 74. H. H. Zhao , S. Y. Zhang , M. X. Zuo , and J. Zhou . 2003. Correlations between call frequency and ear length in bats belonging to the families Rhinolophidae and Hipposideridae. Journal of Zoology (London), 259: 189—195. Google Scholar

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