Divergent echolocation call frequencies in insular rhinolophids (Chiroptera): a case of character displacement
Because rhinolophids have been hypothesized to use echolocation call frequency to recognize conspecifics, sympatric species calling at similar frequencies should be subject to acoustic character displacement, i.e. a drift in frequency values to minimize the risk of misidentification of conspecifics....
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Published in | Journal of biogeography Vol. 34; no. 12; pp. 2129 - 2138 |
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Main Authors | , , , , , |
Format | Journal Article |
Language | English |
Published |
Oxford, UK
Oxford, UK : Blackwell Publishing Ltd
01.12.2007
Blackwell Publishing Ltd Blackwell Publishing Blackwell |
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Abstract | Because rhinolophids have been hypothesized to use echolocation call frequency to recognize conspecifics, sympatric species calling at similar frequencies should be subject to acoustic character displacement, i.e. a drift in frequency values to minimize the risk of misidentification of conspecifics. However, it has been proposed that insufficient geographical separation between populations in sympatry and allopatry may counter the establishment of frequency differences by character displacement. Here we tested the hypothesis that insular populations should exhibit acoustic divergence, and this should be revealed by comparing call frequencies with those observed in mainland, allopatric populations of conspecifics. We also tested whether the evolutionary pressure towards acoustic divergence should be especially strong at sites where rhinolophid species emitting similar call frequencies roost together in order to minimize interspecific frequency overlap. Sardinia and southern Italy (Campania, Lazio, Abruzzo). Time-expanded echolocation calls and body size were recorded from Sardinian populations of Rhinolophus mehelyi Matschie, Rhinolophus hipposideros (Bechstein) and Rhinolophus euryale Blasius. Both call frequencies and forearm length of insular R. hipposideros and R. euryale were compared with those of populations from mainland areas of Italy where R. mehelyi is absent, to explore the hypothesis that the presence of the latter species (which calls at frequency values intermediate between the other two) may determine acoustic divergence in the other species. For Sardinian R. mehelyi and R. euryale, we also carried out intraspecific comparisons of call frequencies between bats from monospecific colonies and those from mixed colonies. As hypothesized, Sardinian R. hipposideros and R. euryale called at frequencies higher and lower, respectively, than in the peninsula. In this way, overlap with R. mehelyi is avoided. Body size showed no difference between insular and peninsular populations, i.e. frequency differences are not a by-product of difference in body size determined by insularity. Frequency values in Sardinian R. euryale from monospecific colonies did not differ from those of bats roosting together with R. mehelyi. However, R. mehelyi showed frequency values significantly higher when associated with R. euryale, possibly to minimize the risk of species misrecognition. At least under geographical isolation, character displacement may be a causal mechanism for shifts in call frequency of sympatric rhinolophids. Species recognition and facilitation of intraspecific communication (with possible implications for mate recognition) constitute the best candidate factors for the phenomenon we observed. |
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AbstractList | Aims Because rhinolophids have been hypothesized to use echolocation call frequency to recognize conspecifics, sympatric species calling at similar frequencies should be subject to acoustic character displacement, i.e. a drift in frequency values to minimize the risk of misidentification of conspecifics. However, it has been proposed that insufficient geographical separation between populations in sympatry and allopatry may counter the establishment of frequency differences by character displacement. Here we tested the hypothesis that insular populations should exhibit acoustic divergence, and this should be revealed by comparing call frequencies with those observed in mainland, allopatric populations of conspecifics. We also tested whether the evolutionary pressure towards acoustic divergence should be especially strong at sites where rhinolophid species emitting similar call frequencies roost together in order to minimize interspecific frequency overlap. Location Sardinia and southern Italy (Campania, Lazio, Abruzzo). Methods Time-expanded echolocation calls and body size were recorded from Sardinian populations of Rhinolophus mehelyi Matschie, Rhinolophus hipposideros (Bechstein) and Rhinolophus euryale Blasius. Both call frequencies and forearm length of insular R. hipposideros and R. euryale were compared with those of populations from mainland areas of Italy where R. mehelyi is absent, to explore the hypothesis that the presence of the latter species (which calls at frequency values intermediate between the other two) may determine acoustic divergence in the other species. For Sardinian R. mehelyi and R. euryale, we also carried out intraspecific comparisons of call frequencies between bats from monospecific colonies and those from mixed colonies. Results As hypothesized, Sardinian R. hipposideros and R. euryale called at frequencies higher and lower, respectively, than in the peninsula. In this way, overlap with R. mehelyi is avoided. Body size showed no difference between insular and peninsular populations, i.e. frequency differences are not a byproduct of difference in body size determined by insularity. Frequency values in Sardinian R. euryale from monospecific colonies did not differ from those of bats roosting together with R. mehelyi. However, R. mehelyi showed frequency values significantly higher when associated with R. euryale, possibly to minimize the risk of species misrecognition. Main conclusions At least under geographical isolation, character displacement may be a causal mechanism for shifts in call frequency of sympatric rhinolophids. Species recognition and facilitation of intraspecific communication (with possible implications for mate recognition) constitute the best candidate factors for the phenomenon we observed. Because rhinolophids have been hypothesized to use echolocation call frequency to recognize conspecifics, sympatric species calling at similar frequencies should be subject to acoustic character displacement, i.e. a drift in frequency values to minimize the risk of misidentification of conspecifics. However, it has been proposed that insufficient geographical separation between populations in sympatry and allopatry may counter the establishment of frequency differences by character displacement. Here we tested the hypothesis that insular populations should exhibit acoustic divergence, and this should be revealed by comparing call frequencies with those observed in mainland, allopatric populations of conspecifics. We also tested whether the evolutionary pressure towards acoustic divergence should be especially strong at sites where rhinolophid species emitting similar call frequencies roost together in order to minimize interspecific frequency overlap. Sardinia and southern Italy (Campania, Lazio, Abruzzo). Time-expanded echolocation calls and body size were recorded from Sardinian populations of Rhinolophus mehelyi Matschie, Rhinolophus hipposideros (Bechstein) and Rhinolophus euryale Blasius. Both call frequencies and forearm length of insular R. hipposideros and R. euryale were compared with those of populations from mainland areas of Italy where R. mehelyi is absent, to explore the hypothesis that the presence of the latter species (which calls at frequency values intermediate between the other two) may determine acoustic divergence in the other species. For Sardinian R. mehelyi and R. euryale, we also carried out intraspecific comparisons of call frequencies between bats from monospecific colonies and those from mixed colonies. As hypothesized, Sardinian R. hipposideros and R. euryale called at frequencies higher and lower, respectively, than in the peninsula. In this way, overlap with R. mehelyi is avoided. Body size showed no difference between insular and peninsular populations, i.e. frequency differences are not a by-product of difference in body size determined by insularity. Frequency values in Sardinian R. euryale from monospecific colonies did not differ from those of bats roosting together with R. mehelyi. However, R. mehelyi showed frequency values significantly higher when associated with R. euryale, possibly to minimize the risk of species misrecognition. At least under geographical isolation, character displacement may be a causal mechanism for shifts in call frequency of sympatric rhinolophids. Species recognition and facilitation of intraspecific communication (with possible implications for mate recognition) constitute the best candidate factors for the phenomenon we observed. Aims Because rhinolophids have been hypothesized to use echolocation call frequency to recognize conspecifics, sympatric species calling at similar frequencies should be subject to acoustic character displacement, i.e. a drift in frequency values to minimize the risk of misidentification of conspecifics. However, it has been proposed that insufficient geographical separation between populations in sympatry and allopatry may counter the establishment of frequency differences by character displacement. Here we tested the hypothesis that insular populations should exhibit acoustic divergence, and this should be revealed by comparing call frequencies with those observed in mainland, allopatric populations of conspecifics. We also tested whether the evolutionary pressure towards acoustic divergence should be especially strong at sites where rhinolophid species emitting similar call frequencies roost together in order to minimize interspecific frequency overlap. Location Sardinia and southern Italy (Campania, Lazio, Abruzzo). Methods Time‐expanded echolocation calls and body size were recorded from Sardinian populations of Rhinolophus mehelyi Matschie, Rhinolophus hipposideros (Bechstein) and Rhinolophus euryale Blasius. Both call frequencies and forearm length of insular R. hipposideros and R. euryale were compared with those of populations from mainland areas of Italy where R. mehelyi is absent, to explore the hypothesis that the presence of the latter species (which calls at frequency values intermediate between the other two) may determine acoustic divergence in the other species. For Sardinian R. mehelyi and R. euryale, we also carried out intraspecific comparisons of call frequencies between bats from monospecific colonies and those from mixed colonies. Results As hypothesized, Sardinian R. hipposideros and R. euryale called at frequencies higher and lower, respectively, than in the peninsula. In this way, overlap with R. mehelyi is avoided. Body size showed no difference between insular and peninsular populations, i.e. frequency differences are not a by‐product of difference in body size determined by insularity. Frequency values in Sardinian R. euryale from monospecific colonies did not differ from those of bats roosting together with R. mehelyi. However, R. mehelyi showed frequency values significantly higher when associated with R. euryale, possibly to minimize the risk of species misrecognition. Main conclusions At least under geographical isolation, character displacement may be a causal mechanism for shifts in call frequency of sympatric rhinolophids. Species recognition and facilitation of intraspecific communication (with possible implications for mate recognition) constitute the best candidate factors for the phenomenon we observed. Aims Because rhinolophids have been hypothesized to use echolocation call frequency to recognize conspecifics, sympatric species calling at similar frequencies should be subject to acoustic character displacement, i.e. a drift in frequency values to minimize the risk of misidentification of conspecifics. However, it has been proposed that insufficient geographical separation between populations in sympatry and allopatry may counter the establishment of frequency differences by character displacement. Here we tested the hypothesis that insular populations should exhibit acoustic divergence, and this should be revealed by comparing call frequencies with those observed in mainland, allopatric populations of conspecifics. We also tested whether the evolutionary pressure towards acoustic divergence should be especially strong at sites where rhinolophid species emitting similar call frequencies roost together in order to minimize interspecific frequency overlap. Location Sardinia and southern Italy (Campania, Lazio, Abruzzo). Methods Time‐expanded echolocation calls and body size were recorded from Sardinian populations of Rhinolophus mehelyi Matschie, Rhinolophus hipposideros (Bechstein) and Rhinolophus euryale Blasius. Both call frequencies and forearm length of insular R. hipposideros and R. euryale were compared with those of populations from mainland areas of Italy where R. mehelyi is absent, to explore the hypothesis that the presence of the latter species (which calls at frequency values intermediate between the other two) may determine acoustic divergence in the other species. For Sardinian R. mehelyi and R. euryale , we also carried out intraspecific comparisons of call frequencies between bats from monospecific colonies and those from mixed colonies. Results As hypothesized, Sardinian R. hipposideros and R. euryale called at frequencies higher and lower, respectively, than in the peninsula. In this way, overlap with R. mehelyi is avoided. Body size showed no difference between insular and peninsular populations, i.e. frequency differences are not a by‐product of difference in body size determined by insularity. Frequency values in Sardinian R. euryale from monospecific colonies did not differ from those of bats roosting together with R. mehelyi . However, R. mehelyi showed frequency values significantly higher when associated with R. euryale , possibly to minimize the risk of species misrecognition. Main conclusions At least under geographical isolation, character displacement may be a causal mechanism for shifts in call frequency of sympatric rhinolophids. Species recognition and facilitation of intraspecific communication (with possible implications for mate recognition) constitute the best candidate factors for the phenomenon we observed. Aims Because rhinolophids have been hypothesized to use echolocation call frequency to recognize conspecifics, sympatric species calling at similar frequencies should be subject to acoustic character displacement, i.e. a drift in frequency values to minimize the risk of misidentification of conspecifics. However, it has been proposed that insufficient geographical separation between populations in sympatry and allopatry may counter the establishment of frequency differences by character displacement. Here we tested the hypothesis that insular populations should exhibit acoustic divergence, and this should be revealed by comparing call frequencies with those observed in mainland, allopatric populations of conspecifics. We also tested whether the evolutionary pressure towards acoustic divergence should be especially strong at sites where rhinolophid species emitting similar call frequencies roost together in order to minimize interspecific frequency overlap. Location Sardinia and southern Italy (Campania, Lazio, Abruzzo). Methods Time-expanded echolocation calls and body size were recorded from Sardinian populations of Rhinolophus mehelyi Matschie, Rhinolophus hipposideros (Bechstein) and Rhinolophus euryale Blasius. Both call frequencies and forearm length of insular R. hipposideros and R. euryale were compared with those of populations from mainland areas of Italy where R. mehelyi is absent, to explore the hypothesis that the presence of the latter species (which calls at frequency values intermediate between the other two) may determine acoustic divergence in the other species. For Sardinian R. mehelyi and R. euryale, we also carried out intraspecific comparisons of call frequencies between bats from monospecific colonies and those from mixed colonies. Results As hypothesized, Sardinian R. hipposideros and R. euryale called at frequencies higher and lower, respectively, than in the peninsula. In this way, overlap with R. mehelyi is avoided. Body size showed no difference between insular and peninsular populations, i.e. frequency differences are not a by-product of difference in body size determined by insularity. Frequency values in Sardinian R. euryale from monospecific colonies did not differ from those of bats roosting together with R. mehelyi. However, R. mehelyi showed frequency values significantly higher when associated with R. euryale, possibly to minimize the risk of species misrecognition. Main conclusions At least under geographical isolation, character displacement may be a causal mechanism for shifts in call frequency of sympatric rhinolophids. Species recognition and facilitation of intraspecific communication (with possible implications for mate recognition) constitute the best candidate factors for the phenomenon we observed. |
Author | Mucedda, Mauro Pidinchedda, Ermanno Bello, Monica Biscardi, Stefania Russo, Danilo Jones, Gareth |
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Keywords | geographical separation Character displacement Transmission Biogeography Sympatry Resource sharing Island bats Resource repartition Mediterranean Vertebrata Mammalia islands resource partitioning Allopatry Chiroptera Echolocation cultural transmission |
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PublicationDateYYYYMMDD | 2007-12-01 |
PublicationDate_xml | – month: 12 year: 2007 text: December 2007 |
PublicationDecade | 2000 |
PublicationPlace | Oxford, UK |
PublicationPlace_xml | – name: Oxford, UK – name: Oxford |
PublicationTitle | Journal of biogeography |
PublicationYear | 2007 |
Publisher | Oxford, UK : Blackwell Publishing Ltd Blackwell Publishing Ltd Blackwell Publishing Blackwell |
Publisher_xml | – name: Oxford, UK : Blackwell Publishing Ltd – name: Blackwell Publishing Ltd – name: Blackwell Publishing – name: Blackwell |
References | Teeling, E., Madsen, O., Van Den Bussche, R., Jong, W., Stanhope, M. & Springer, M. (2002) Microbat monophyly and the convergent evolution of a key innovation in old world rhinolophoid microbats. Proceedings of the National Academy of Sciences USA, 99, 1431-1436. Mitchell-Jones, A.J., Amori, G., Bogdanowicz, W., Krištufek, B., Reijnders, P.J.H., Spitzenberger, F., Stubbe, M., Thissen, J.B.M., Vohralík, V. & Zima, J. (eds.) (1999) The atlas of European mammals. Academic Press, London. Goiti, U., Aihartza, J. R., Garin, I. & Zabala, J. (2003) Influence of habitat on the foraging behaviour of the Mediterranean horseshoe bat, Rhinolophus euryale. Acta Chiropterologica, 5, 75-84. Bontadina, F., Schofield, H. & Naef-Daenzer, B. (2002) Radiotracking reveals that lesser horseshoe bats (Rhinolophus hipposideros) forage in woodland. Journal of Zoology, 258, 281-290. Springer, M.S., Teeling, E.C., Madsen, O., Stanhope, M.J. & De Jong, W.W. (2001) Integrated fossil and molecular data reconstruct bat echolocation. Proceedings of the National Academy of Sciences USA, 98, 6241-6246. Salsamendi, E., Aihartza, J., Goiti, U., Almenar, D. & Garin, I. (2005) Echolocation calls and morphology in the Mehely's (Rhinolophus mehelyi) and Mediterranean (R. euryale) horseshoe bats: implications for resource partitioning. Hystrix, 16, 149-158. Jones, G., Morton, M., Hughes, P. & Budden, R.M. (1993) Echolocation, flight morphology and foraging strategies in some West African hipposiderid bats. Journal of Zoology, 230, 385-400. Russo, D., Jones, G. & Mucedda, M. (2001) Influence of age, sex and body size on echolocation calls of Mediterranean (Rhinolophus euryale) and Mehely's (Rhinolophus mehelyi) horseshoe bats (Chiroptera: Rhinolophidae). Mammalia, 65, 429-436. Thabah, A., Rossiter, S.J., Kingston, T., Zhang, S., Parsons, S., Mya, K.M., Zubaid, A. & Jones, G. (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. Russo, D., Jones, G. & Migliozzi, A. (2002) Habitat selection by the Mediterranean horseshoe bat, Rhinolophus euryale (Chiroptera: Rhinolophidae) in a rural area of southern Italy and implications for conservation. Biological Conservation, 107, 71-81. Jones, G. & Ransome, R.D. (1993) Echolocation calls of bats are influenced by maternal effects and change over a lifetime. Proceedings of the Royal Society B: Biological Sciences, 252, 125-128. Losos, J.B. (2000) Ecological character displacement and the study of adaptation. Proceedings of the National Academy of Sciences USA, 97, 5693-5695. Siemers, B.M., Beedholm, K., Dietz, C., Dietz, I. & Ivanova, T. (2005) Is species identity, sex, age or individual quality conveyed by echolocation call frequency in European horseshoe bats? Acta Chiropterologica, 7, 259-274. Gerhardt, H. C. (1994) The evolution of the vocalization in frogs and toads. Annual Review of Ecology and Systematics, 25, 293-324. Jacobs, D.S., Barclay, R.M.R & Walker, M.H. (2007). The allometry of echolocation call frequencies of insectivorous bats: why do some species deviate from the pattern? Oecologia, 152, 583-594. Ma, J., Kobayasi, K., Zhang, S. & Metzner, W. (2006) Vocal communication in adult greater horseshoe bats, Rhinolophus ferrumequinum. Journal of Comparative Physiology A, 192, 535-550. Pye, J.D. (1993) Is fidelity futile? The 'true' signal is illusory, especially with ultrasound Bioacoustics, 4, 271-286. Jones, G. (1999) Scaling of echolocation call parameters in bats. Journal of Experimental Biology, 202, 3359-3367. Schuller, G. & Pollak, G. D. (1979) Disproportionate frequency representation in the inferior colliculus of Doppler-compensating greater horseshoe bats, Rhinolophus ferrumequinum. Journal of Comparative Physiology A, 132, 47-54. Teeling, E., Springer, M., Madsen, O., Bates, P., O'Brien, S. & Murphy, W. (2005) A molecular phylogeny for bats illuminates biogeography and the fossil record. Science, 307, 580-584. Hutterer, R., Ivanova, T., Meyer-Cords, C. & Rodrigues, L. (2005) Bat migrations in Europe. A review of banding data and literature. German Federal Agency for Nature Conservation, Bonn. Neuweiler, G. (1989) Foraging ecology and audition in echolocating bats. Trends in Ecology & Evolution, 4, 160-166. Schnitzler, H.U. (1968) Die Ultraschallortungslaute der Hufeisennasen-Fledermäuse (Chiroptera, Rhinolophidae) in verschiedenen Orientierungssituationen. Zeitschrift für Vergleichende Physiologie, 57, 376-408. Schluter, D. (2000) Ecological character displacement in adaptive radiation. The American Naturalist, 156(Suppl.), S4-S16. Vaughan, N., Jones, G. & Harris, S. (1997) Identification of British bat species by multivariate analysis of echolocation call parameters. Bioacoustics, 7, 189-207. Mucedda, M., Murittu, G., Oppes, A. & Pidinchedda, E. (1995) Osservazioni sui Chirotteri troglofili della Sardegna. Bollettino della Società Sarda di Scienze Naturali, 30, 97-129. Neuweiler, G., Metzner, W., Heilmann, U., Rübsamen, U.R., Eckrich, M. & Costa, H.H. (1987) Foraging behaviour and echolocation in the rufous horseshoe bat (Rhinolophus rouxi). Behavioral Ecology and Sociobiology, 20, 53-67. Guillén, A., Juste, J.B. & Ibáñez, C. (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. Marshall, D.C. & Cooley, J.R. (2000) Reproductive character displacement and speciation in periodical cicadas, with description of a new species, 13-year Magicicada neotredecim. Evolution, 54, 1313-1325. Mucedda, M. (1994) Note su Rhinolophus mehelyi (Chiroptera, Rhinolophidae) della Sardegna. Bollettino del Gruppo Speleologico Sassarese, 15, 43-46. Heller, K-G. & Helversen, O. (1989) Resource partitioning of sonar frequency bands in rhinolophoid bats. Oecologia, 80, 178-186. Fenton, M.B. (1994) Echolocation: its impact on the behaviour and ecology of bats. Ecoscience, 1, 21-30. Shaw, K. L. (2000) Further acoustic diversity in Hawaiian forests: two new species of Hawaiian cricket (Orthoptera: Gryllidae: Laupala). Zoological Journal of the Linnean Society, 129, 73-91. Russo, D., Almenar, D., Aihartza, J., Goiti, U., Salsamendi, E. & Garin, I. (2005) Habitat selection in sympatric Rhinolophus mehelyi and R. euryale (Mammalia: Chiroptera). Journal of Zoology, 266, 327-332. Hiryu, S., Katsura, K., Nagato, T., Yamazaki, H., Lin, L.-L., Watanabe, Y. & Riquimaroux, H. (2006) Intra-individual variation in the vocalized frequency of the Taiwanese leaf-nosed bat, Hipposideros terasensis, influenced by conspecific colony members. Journal of Comparative Physiology A, 192, 807-815. Jones, G. & Teeling, E.C. (2006) The evolution of echolocation in bats. Trends in Ecology & Evolution, 21, 149-156. Jones, G. & Van Parijs, S.M. (1993) Bimodal echolocation in pipistrelle bats: are cryptic species present? Proceedings of the Royal Society B: Biological Sciences, 251, 119-125. Schober, W. & Grimmberger, E. (1997) The bats of Europe and North America. TFH Publications, Neptune, NJ. Ficken, M.S. & Weise, C.M. (1984) A complex call of the blackcapped chickadee (Parus atricapillus). I. Microgeographic variation. The Auk, 101, 349-360. Gannon, W.L. & Rácz, G.R. (2006) Character displacement and ecomorphological analysis of two long-eared Myotis (M. auriculus and M. evotis). Journal of Mammalogy, 87, 171-179. Rossiter, S.J., Jones, G., Ransome, R.D. & Barratt, E.M. (2002) Relatedness structure and kin-biased foraging in the greater horseshoe bat (Rhinolophus ferrumequinum). Behavioral Ecology and Sociobiology, 51, 510-518. Russo, D. & Jones, G. (2002) Identification of twenty-two bat species (Mammalia: Chiroptera) from Italy by analysis of time-expanded recordings of echolocation calls. Journal of Zoology, 258, 91-103. Avery, M. & Oring, L.W. (1977) Song dialects in the bobolink (Dolichonyx oryzivorus). The Condor, 79, 113-118. Pedley, R. (2004) Factors affecting echolocation frequency variation in insectivorous bats. Undergraduate final year dissertation, Lancaster University, Lancaster. Andrews, M.M. & Andrews, A.P.T. (2003) Ultrasound social calls made by greater horseshoe bats (Rhinolophus ferrumequinum) in a nursery roost. Acta Chiropterologica, 5, 221-234. Tu, H.-W. & Severinghouse, L.L. (2004) Geographic variation of the highly complex hwamei (Garrulax canorus) songs. Zoological Studies, 43, 629-640. Gerlinde, H. & Gerhardt, C. (2003) Reproductive character displacement in the acoustic communication of green tree frogs (Hyla cinerea). Evolution, 57, 894-904. Jones, G., Gordon, T. & Nightingale, J. (1992) Sex and age differences in the echolocation calls of the lesser horseshoe bat, Rhinolophus hipposideros. Mammalia, 56, 189-193. Kingston, T., Lara, M.C., Jones, G., Akbar, Z., Kunz, T.H. & Schneider, C.J. (2001) Acoustic divergence in two cryptic Hipposideros species: a role for social selection? Proceedings of the Royal Society B: Biological Sciences, 268, 1381-1386. Tracy, T.T. & Baker, M.C. (1999) Geographic variation in syllables of house finch songs. The Auk, 116, 666-676. 1995; 30 2002; 51 1989; 80 2002; 99 2003; 57 1994; 25 1999; 202 1992; 56 2001; 268 1993; 4 1997; 7 1968; 57 2006; 21 2005; 266 2000; 13 2000; 54 2000; 129 2000; 97 2002; 107 1993; 251 2005; 307 2003; 5 1982 1977; 79 1993; 252 1988 2001; 98 2004; 43 1989; 4 1984; 101 1997 2002; 258 2006; 192 2005 2004 2000; 156 1999 2001; 65 1987; 20 1979; 132 2006; 87 2006; 88 2007; 152 2005; 7 1994; 15 1994; 1 2005; 16 1999; 116 1993; 230 e_1_2_6_51_1 e_1_2_6_53_1 e_1_2_6_30_1 Ficken M.S. (e_1_2_6_7_1) 1984; 101 Mucedda M. (e_1_2_6_31_1) 1994; 15 Tu H.‐W. (e_1_2_6_55_1) 2004; 43 e_1_2_6_13_1 Mucedda M. (e_1_2_6_32_1) 1995; 30 e_1_2_6_36_1 e_1_2_6_11_1 e_1_2_6_34_1 Schnitzler H.U. (e_1_2_6_45_1) 2004 e_1_2_6_17_1 e_1_2_6_38_1 e_1_2_6_20_1 e_1_2_6_41_1 Houston R.D. (e_1_2_6_15_1) 2004 e_1_2_6_9_1 e_1_2_6_5_1 e_1_2_6_24_1 e_1_2_6_49_1 e_1_2_6_22_1 e_1_2_6_28_1 e_1_2_6_26_1 e_1_2_6_47_1 e_1_2_6_52_1 e_1_2_6_54_1 e_1_2_6_10_1 e_1_2_6_50_1 Anthony E.L.P. (e_1_2_6_3_1) 1988 Schluter D. (e_1_2_6_43_1) 2000; 156 Schober W. (e_1_2_6_46_1) 1997 Pedley R. (e_1_2_6_35_1) 2004 e_1_2_6_14_1 e_1_2_6_12_1 Hutterer R. (e_1_2_6_16_1) 2005 e_1_2_6_33_1 e_1_2_6_18_1 e_1_2_6_39_1 e_1_2_6_56_1 e_1_2_6_37_1 Jones G. (e_1_2_6_19_1) 2004 e_1_2_6_21_1 e_1_2_6_40_1 Salsamendi E. (e_1_2_6_42_1) 2005; 16 e_1_2_6_8_1 e_1_2_6_4_1 e_1_2_6_6_1 e_1_2_6_25_1 e_1_2_6_48_1 e_1_2_6_23_1 e_1_2_6_2_1 e_1_2_6_29_1 e_1_2_6_44_1 e_1_2_6_27_1 |
References_xml | – reference: Bontadina, F., Schofield, H. & Naef-Daenzer, B. (2002) Radiotracking reveals that lesser horseshoe bats (Rhinolophus hipposideros) forage in woodland. Journal of Zoology, 258, 281-290. – reference: Schober, W. & Grimmberger, E. (1997) The bats of Europe and North America. TFH Publications, Neptune, NJ. – reference: Russo, D. & Jones, G. (2002) Identification of twenty-two bat species (Mammalia: Chiroptera) from Italy by analysis of time-expanded recordings of echolocation calls. Journal of Zoology, 258, 91-103. – reference: Fenton, M.B. (1994) Echolocation: its impact on the behaviour and ecology of bats. Ecoscience, 1, 21-30. – reference: Russo, D., Almenar, D., Aihartza, J., Goiti, U., Salsamendi, E. & Garin, I. (2005) Habitat selection in sympatric Rhinolophus mehelyi and R. euryale (Mammalia: Chiroptera). Journal of Zoology, 266, 327-332. – reference: Springer, M.S., Teeling, E.C., Madsen, O., Stanhope, M.J. & De Jong, W.W. (2001) Integrated fossil and molecular data reconstruct bat echolocation. Proceedings of the National Academy of Sciences USA, 98, 6241-6246. – reference: Mucedda, M., Murittu, G., Oppes, A. & Pidinchedda, E. (1995) Osservazioni sui Chirotteri troglofili della Sardegna. Bollettino della Società Sarda di Scienze Naturali, 30, 97-129. – reference: Schuller, G. & Pollak, G. D. (1979) Disproportionate frequency representation in the inferior colliculus of Doppler-compensating greater horseshoe bats, Rhinolophus ferrumequinum. Journal of Comparative Physiology A, 132, 47-54. – reference: Mucedda, M. (1994) Note su Rhinolophus mehelyi (Chiroptera, Rhinolophidae) della Sardegna. Bollettino del Gruppo Speleologico Sassarese, 15, 43-46. – reference: Gerlinde, H. & Gerhardt, C. (2003) Reproductive character displacement in the acoustic communication of green tree frogs (Hyla cinerea). Evolution, 57, 894-904. – reference: Goiti, U., Aihartza, J. R., Garin, I. & Zabala, J. (2003) Influence of habitat on the foraging behaviour of the Mediterranean horseshoe bat, Rhinolophus euryale. Acta Chiropterologica, 5, 75-84. – reference: Pye, J.D. (1993) Is fidelity futile? The 'true' signal is illusory, especially with ultrasound Bioacoustics, 4, 271-286. – reference: Hiryu, S., Katsura, K., Nagato, T., Yamazaki, H., Lin, L.-L., Watanabe, Y. & Riquimaroux, H. (2006) Intra-individual variation in the vocalized frequency of the Taiwanese leaf-nosed bat, Hipposideros terasensis, influenced by conspecific colony members. Journal of Comparative Physiology A, 192, 807-815. – reference: Tracy, T.T. & Baker, M.C. (1999) Geographic variation in syllables of house finch songs. The Auk, 116, 666-676. – reference: Teeling, E., Springer, M., Madsen, O., Bates, P., O'Brien, S. & Murphy, W. (2005) A molecular phylogeny for bats illuminates biogeography and the fossil record. Science, 307, 580-584. – reference: Shaw, K. L. (2000) Further acoustic diversity in Hawaiian forests: two new species of Hawaiian cricket (Orthoptera: Gryllidae: Laupala). Zoological Journal of the Linnean Society, 129, 73-91. – reference: Vaughan, N., Jones, G. & Harris, S. (1997) Identification of British bat species by multivariate analysis of echolocation call parameters. Bioacoustics, 7, 189-207. – reference: Ma, J., Kobayasi, K., Zhang, S. & Metzner, W. (2006) Vocal communication in adult greater horseshoe bats, Rhinolophus ferrumequinum. Journal of Comparative Physiology A, 192, 535-550. – reference: Neuweiler, G., Metzner, W., Heilmann, U., Rübsamen, U.R., Eckrich, M. & Costa, H.H. (1987) Foraging behaviour and echolocation in the rufous horseshoe bat (Rhinolophus rouxi). Behavioral Ecology and Sociobiology, 20, 53-67. – reference: Jones, G. & Ransome, R.D. (1993) Echolocation calls of bats are influenced by maternal effects and change over a lifetime. Proceedings of the Royal Society B: Biological Sciences, 252, 125-128. – reference: Pedley, R. (2004) Factors affecting echolocation frequency variation in insectivorous bats. Undergraduate final year dissertation, Lancaster University, Lancaster. – reference: Kingston, T., Lara, M.C., Jones, G., Akbar, Z., Kunz, T.H. & Schneider, C.J. (2001) Acoustic divergence in two cryptic Hipposideros species: a role for social selection? Proceedings of the Royal Society B: Biological Sciences, 268, 1381-1386. – reference: Thabah, A., Rossiter, S.J., Kingston, T., Zhang, S., Parsons, S., Mya, K.M., Zubaid, A. & Jones, G. (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. – reference: Marshall, D.C. & Cooley, J.R. (2000) Reproductive character displacement and speciation in periodical cicadas, with description of a new species, 13-year Magicicada neotredecim. Evolution, 54, 1313-1325. – reference: Teeling, E., Madsen, O., Van Den Bussche, R., Jong, W., Stanhope, M. & Springer, M. (2002) Microbat monophyly and the convergent evolution of a key innovation in old world rhinolophoid microbats. Proceedings of the National Academy of Sciences USA, 99, 1431-1436. – reference: Siemers, B.M., Beedholm, K., Dietz, C., Dietz, I. & Ivanova, T. (2005) Is species identity, sex, age or individual quality conveyed by echolocation call frequency in European horseshoe bats? Acta Chiropterologica, 7, 259-274. – reference: Schluter, D. (2000) Ecological character displacement in adaptive radiation. The American Naturalist, 156(Suppl.), S4-S16. – reference: Russo, D., Jones, G. & Migliozzi, A. (2002) Habitat selection by the Mediterranean horseshoe bat, Rhinolophus euryale (Chiroptera: Rhinolophidae) in a rural area of southern Italy and implications for conservation. Biological Conservation, 107, 71-81. – reference: Rossiter, S.J., Jones, G., Ransome, R.D. & Barratt, E.M. (2002) Relatedness structure and kin-biased foraging in the greater horseshoe bat (Rhinolophus ferrumequinum). Behavioral Ecology and Sociobiology, 51, 510-518. – reference: Jones, G. & Teeling, E.C. (2006) The evolution of echolocation in bats. Trends in Ecology & Evolution, 21, 149-156. – reference: Andrews, M.M. & Andrews, A.P.T. (2003) Ultrasound social calls made by greater horseshoe bats (Rhinolophus ferrumequinum) in a nursery roost. Acta Chiropterologica, 5, 221-234. – reference: Jones, G., Gordon, T. & Nightingale, J. (1992) Sex and age differences in the echolocation calls of the lesser horseshoe bat, Rhinolophus hipposideros. Mammalia, 56, 189-193. – reference: Salsamendi, E., Aihartza, J., Goiti, U., Almenar, D. & Garin, I. (2005) Echolocation calls and morphology in the Mehely's (Rhinolophus mehelyi) and Mediterranean (R. euryale) horseshoe bats: implications for resource partitioning. Hystrix, 16, 149-158. – reference: Jacobs, D.S., Barclay, R.M.R & Walker, M.H. (2007). The allometry of echolocation call frequencies of insectivorous bats: why do some species deviate from the pattern? Oecologia, 152, 583-594. – reference: Neuweiler, G. (1989) Foraging ecology and audition in echolocating bats. Trends in Ecology & Evolution, 4, 160-166. – reference: Tu, H.-W. & Severinghouse, L.L. (2004) Geographic variation of the highly complex hwamei (Garrulax canorus) songs. Zoological Studies, 43, 629-640. – reference: Losos, J.B. (2000) Ecological character displacement and the study of adaptation. Proceedings of the National Academy of Sciences USA, 97, 5693-5695. – reference: Avery, M. & Oring, L.W. (1977) Song dialects in the bobolink (Dolichonyx oryzivorus). The Condor, 79, 113-118. – reference: Ficken, M.S. & Weise, C.M. (1984) A complex call of the blackcapped chickadee (Parus atricapillus). I. Microgeographic variation. The Auk, 101, 349-360. – reference: Mitchell-Jones, A.J., Amori, G., Bogdanowicz, W., Krištufek, B., Reijnders, P.J.H., Spitzenberger, F., Stubbe, M., Thissen, J.B.M., Vohralík, V. & Zima, J. (eds.) (1999) The atlas of European mammals. Academic Press, London. – reference: Gannon, W.L. & Rácz, G.R. (2006) Character displacement and ecomorphological analysis of two long-eared Myotis (M. auriculus and M. evotis). Journal of Mammalogy, 87, 171-179. – reference: Gerhardt, H. C. (1994) The evolution of the vocalization in frogs and toads. Annual Review of Ecology and Systematics, 25, 293-324. – reference: Hutterer, R., Ivanova, T., Meyer-Cords, C. & Rodrigues, L. (2005) Bat migrations in Europe. A review of banding data and literature. German Federal Agency for Nature Conservation, Bonn. – reference: Schnitzler, H.U. (1968) Die Ultraschallortungslaute der Hufeisennasen-Fledermäuse (Chiroptera, Rhinolophidae) in verschiedenen Orientierungssituationen. Zeitschrift für Vergleichende Physiologie, 57, 376-408. – reference: Jones, G. & Van Parijs, S.M. (1993) Bimodal echolocation in pipistrelle bats: are cryptic species present? Proceedings of the Royal Society B: Biological Sciences, 251, 119-125. – reference: Heller, K-G. & Helversen, O. (1989) Resource partitioning of sonar frequency bands in rhinolophoid bats. Oecologia, 80, 178-186. – reference: Guillén, A., Juste, J.B. & Ibáñez, C. (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. – reference: Jones, G. (1999) Scaling of echolocation call parameters in bats. 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Snippet | Because rhinolophids have been hypothesized to use echolocation call frequency to recognize conspecifics, sympatric species calling at similar frequencies... Aims Because rhinolophids have been hypothesized to use echolocation call frequency to recognize conspecifics, sympatric species calling at similar frequencies... Aims Because rhinolophids have been hypothesized to use echolocation call frequency to recognize conspecifics, sympatric species calling at similar... Aims Because rhinolophids have been hypothesized to use echolocation call frequency to recognize conspecifics, sympatric species calling at similar... |
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SubjectTerms | Acoustic echoes acoustics Allopatry Animal and plant ecology Animal, plant and microbial ecology arms (limbs) Audio frequencies Bats Biogeography Biological and medical sciences body size character displacement Character Displacement and Release in Insular Vertebrates Chiroptera cultural transmission Ecology Euryale Foraging Forearm Fundamental and applied biological sciences. Psychology General aspects geographical separation Hipposideros Horseshoes islands Italy Mammalia Mediterranean Niche differentiation resource partitioning Rhinolophus Rhinolophus hipposideros risk roosting behavior Sardinia Sympatric species sympatry Synecology Vertebrates: general zoology, morphology, phylogeny, systematics, cytogenetics, geographical distribution |
Title | Divergent echolocation call frequencies in insular rhinolophids (Chiroptera): a case of character displacement |
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