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Nyanasengeran Movin, Tatjana Gamova, Sergei G. Surmach, Jonathan C. Slaght, A.A. Kisleiko, James A. Eaton, Frank E. Rheindt. 2022: Using bioacoustic tools to clarify species delimitation within the Blakiston's Fish Owl (Bubo blakistoni) complex. Avian Research, 13(1): 100021. doi: 10.1016/j.avrs.2022.100021
Citation: Nyanasengeran Movin, Tatjana Gamova, Sergei G. Surmach, Jonathan C. Slaght, A.A. Kisleiko, James A. Eaton, Frank E. Rheindt. 2022: Using bioacoustic tools to clarify species delimitation within the Blakiston's Fish Owl (Bubo blakistoni) complex. Avian Research, 13(1): 100021. doi: 10.1016/j.avrs.2022.100021
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Using bioacoustic tools to clarify species delimitation within the Blakiston's Fish Owl (Bubo blakistoni) complex

doi: 10.1016/j.avrs.2022.100021
  • a.

    Department of Biological Sciences, National University of Singapore, 16 Science Drive 4, Singapore, 117558, Singapore

  • b.

    Federal Scientific Center for Biodiversity of Terrestrial Biota of East Asia FEB RAS. Vladivostok, Russia

  • c.

    Wildlife Conservation Society, 2300 Southern Blvd, Bronx, NY, USA, 10460

  • d.

    Kurilskii State Nature Reserve, Yuzhno-Kurilsk, Russia

  • e.

    A-3A-5, Casa Indah I, Persiaran Surian, 47810, Petaling Jaya, Malaysia

More Information
  • Corresponding author: E-mail address: dbsrfe@nus.edu.sg (F. Rheindt)
  • Received Date: 12 Oct 2021
  • Accepted Date: 16 Feb 2022
  • Publish Date: 12 Mar 2022
    Abstract
  • Although Blakiston's Fish Owl (Bubo blakistoni) is widely treated as a single species, marked differences in the structure of pair duets between continental and insular populations have been documented. However, no study has quantitatively assessed these vocal differences. We obtained 192 duets from 22 pairs of Blakiston's Fish Owl: 15 pairs of B. b. blakistoni from the Japanese island of Hokkaido and the Russian Kuril island of Kunashir, and seven pairs of B. b. doerriesi from Primorye on the Russian mainland. This is a sizeable dataset for such a large, retiring, and rare owl. We conducted bioacoustic examinations of 14 vocal parameters using principal component analysis and the Isler criterion to quantitatively test species boundaries within the B. blakistoni complex. We found that the insular populations on Hokkaido and Kunashir emerged as vocally similar to each other but markedly different from the continental populations of B. blakistoni, corresponding closely with presently accepted subspecies limits. Bioacoustic differences in the duets of the insular and continental groups are greater than the pairwise comparisons of territorial vocalisations between other sympatric owl species. Based on the reproductive importance of vocal duets in owl biology, we propose the taxonomic elevation of the continental subspecies to species level as Northern Fish Owl B. doerriesi. Our study corroborates the importance of bioacoustics in ascertaining species boundaries in owls and has important implications for the management of the two newly delimited species, each likely to be assessed as Endangered. Both species should be managed independently to optimise conservation outcomes.

     

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  • Bardin, A.V., 2006. Autumn encounter with a Blakiston’s fish owl Ketupa blakistoni on Sakhalin. Russkii Orn. Zhurnal Ekspress-vypusk. 15, 738-739 (in Russian)
    Berzan, A.P., 2005. Analysis of modern distribution and population size of Blakiston’s fish owls in the southern Kuril Islands and Sakhalin. In: Volkov, S.V., Morozov, V.V., Sharikov, A.V. (Eds.), Owls of Northern Eurasia. Working Group of Birds of Prey and Owls, Moscow, Russia, pp. 447–449 (in Russian with English summary).
    Binney, H., Edwards, M., Macias-Fauria, M., Lozhkin, A., Anderson, P., Kaplan, J.O., et al. 2017. Vegetation of Eurasia from the last glacial maximum to present: Key biogeographic patterns. Q. Sci. Rev. 157, 80-97 doi: 10.1016/j.quascirev.2016.11.022
    Bird, J.P., Martin, R., Akcakaya, H.R., Gilroy, J., Burfield, I.J., Garnett, S.T., et al., 2020. Generation lengths of the world's birds and their implications for extinction risk. Conserv. Biol. 34, 1252-1261 doi: 10.1111/cobi.13486
    BirdLife International, 2016. Bubo blakistoni. The IUCN Red List of Threatened Species 2016: e.T22689007A93214159. https://doi.org/10.2305/IUCN.UK.2016-3.RLTS.T22689007A93214159.en. (Accessed 15 March 2021).
    Brazil, M.A., Yamamoto, S., 1989. The behavioural ecology of Blakiston’s Fish Owl Ketupa blakistoni in Japan: calling behaviour. In: Meyburg, B.-U., Chancellor, R.D. (Eds.), Raptors in the Modern World: Proceedings of the III World Conference on Birds of Prey and Owls. World Working Group on Birds of Prey and Owls, Berlin, Germany, pp. 403–410.
    Chung, M.Y., Lopez-Pujol, J., Chung, M.G., 2017. The role of the Baekdudaegan (Korean Peninsula) as a major glacial refugium for plant species: A priority for conservation. Biol. Conserv. 206, 236-248 doi: 10.1016/j.biocon.2016.11.040
    Courtin, J., Andreev, A.A., Raschke, E., Bala, S., Biskaborn, B.K., Liu, S., et al., 2021. Vegetation changes in southeastern Siberia during the Late Pleistocene and the Holocene. Front. Ecol. Evol. 26, 9
    Cros, E., Rheindt, F.E., 2017. Massive bioacoustic analysis suggests introgression across Pleistocene land bridges in Mixornis tit-babblers. J. Ornithol. 158, 407-419 doi: 10.1007/s10336-016-1411-x
    del Hoyo, J., Collar, N.J., 2014. HBW and BirdLife International Illustrated Checklist of the Birds of the World. Non-passerines, vol. 1. Lynx Edicions, Barcelona.
    Dantas, S.M., Weckstein, J.D., Bates, J., Oliveira, J.N., Catanach, T.A., Aleixo, A., 2021. Multi-character taxonomic review, systematics, and biogeography of the Black-capped/Tawny-bellied Screech Owl (Megascops atricapilla-M. watsonii) complex (Aves: Strigidae). Zootaxa 4949, 401-444 doi: 10.11646/zootaxa.4949.3.1
    Drovetski, S.V., Zink, R.M., Fadeev, I.V., Nesterov, E.V., Koblik, E.A., Red’kin, Y.A., et al., 2004. Mitochondrial phylogeny of Locustella and related genera. J. Avian Biol. 35, 105–110 doi: 10.1111/j.0908-8857.2004.03217.x
    Dykhan, M.B., Kisleiko, A.A., 1988. Number and distribution of Blakiston's fish owls on Kunashir Island during the breeding period. In: Litvinenko, N.M. (Ed.), Rare Birds of the Russian Far East and Their Protection. Dalnevostochnoe Otdeleniye Akademii Nauk SSSR, Vladivostok, Russia, pp. 29–32 (in Russian).
    Flint, P.D., Whaley, G.M., Kirwan, M., Charalambides, M.S., Wink, W., 2015. Reprising the taxonomy of Cyprus Scops Owl Otus (scops) cyprius, a neglected island endemic. Zootaxa 4040, 301-316 doi: 10.11646/zootaxa.4040.3.3
    Gwee, C.Y., Christidis, L., Eaton, J.A., Norman, J.A., Trainor, C.A., Verbelen P, et al., 2017. Bioacoustic and multi-locus DNA data of Ninox owls support high incidence of extinction and recolonisation on small, low-lying islands across Wallacea. Mol. Phylogenet. Evol. 109, 246-258 doi: 10.1016/j.ympev.2016.12.024
    Gwee, C.Y., Eaton, J.A., Garg, K.M., Alstrom, P., van Balen, S., Hutchinson, R.O., et al., 2019a. Cryptic diversity in Cyornis (Aves: Muscicapidae) jungle-flycatchers flagged by simple bioacoustic approaches. Zool. J. Linn. Soc. 186, 725-741 doi: 10.1093/zoolinnean/zlz003
    Gwee, C.Y., Eaton, J.A., Ng, E.Y., Rheindt, F.E., 2019b. Species delimitation within the Glaucidium brodiei owlet complex using bioacoustic tools. Avian Res. 10, 36 doi: 10.1186/s40657-019-0175-4
    Harrison, S.P., Yu, G., Takahara, H., Prentice, I.C., 2001. Diversity of temperate plants in east Asia. Nature 413, 129-130 doi: 10.1038/35093166
    Hebert, P.D., Stoeckle, M.Y., Zemlak, T.S., Francis, C.M., 2004. Identification of birds through DNA barcodes. PLoS Biol. 2, e312 doi: 10.1371/journal.pbio.0020312
    Howell, S.N.G., Robbins, M.B., 1995. Species limits of the least pygmy-owl (Glaucidium minutissimum) complex. Wilson Bull. 107, 7-25
    Hussain, S.T., 2021. The hooting past. Re-evaluating the role of owls in shaping human-place relations throughout the Pleistocene. Anthropozoologica 56, 39-56 doi: 10.32593/jstmu/vol4.iss1.131
    Isler, M.L., Chesser, R.T., Robbins, M.B., Cuervo, A.M., Cadena, C.D., Hosner, P.A., 2020. Taxonomic evaluation of the Grallaria rufula (Rufous Antpitta) complex (Aves: Passeriformes: Grallariidae) distinguishes sixteen species. Zootaxa 4817, zootaxa-4817
    Isler M.L., Isler P.R., Whitney, B., 1998. Use of vocalizations to establish species limits in Antbirds (Passeriformes: Thamnophilidae). Auk 115, 577-590 doi: 10.2307/4089407
    Iwase, A., Hashizume, J., Izuho, M., Takahashi, K., Sato, H., 2012. Timing of megafaunal extinction in the late Late Pleistocene on the Japanese Archipelago. Q. Int. 255, 114-124 doi: 10.1016/j.quaint.2011.03.029
    Kerr, K.C., Stoeckle, M.Y., Dove, C.J., Weigt, L.A., Francis, C.M., Hebert, P.D., 2007. Comprehensive DNA barcode coverage of North American birds. Mol. Ecol. Notes 7, 535-543 doi: 10.1111/j.1471-8286.2007.01670.x
    King, B. 2002. Species limits in the Brown Boobook Ninox scutulata complex. Bull. Br. Ornithol. Club 122, 250-256
    Krabbe, N.K. 2017. A new species of Megascops (Strigidae) from the Sierra Nevada de Santa Marta, Colombia, with notes on voices of New World screech-owls. Ornitol. Colomb. 16, 1-27
    Lovette, I.J., 2004. Mitochondrial dating and mixed support for the “2% rule” in birds. Auk 121, 1-6
    Mayr, E., Ashlock, P.D., 1991. Principles of Systematic Zoology, second ed. McGraw-Hill Inc, Now York, p. 475.
    Nechaev, V.A., 1991. Birds of Sakhalin Island. Amur-Ussuri Center for Avian Biodiversity, Vladivostok (in Russian).
    Ng, N.S.R., Rheindt, F.E., 2016. Species delimitation in the White-faced Cuckoo-dove (Turacoena manadensis) based on bioacoustic data. Avian Res. 7, 2 doi: 10.1186/s40657-015-0036-8
    Ng, E.Y.X., Eaton, J.A., Verbelen, P., Hutchinson, R.O., Rheindt, F.E., 2016. Using bioacoustic data to test species limits in an Indo-Pacific island radiation of Macropygia cuckoo doves. Biol. J. Linn. Soc. 118, 786-812 doi: 10.1111/bij.12768
    Nunn, G.B., Stanley, S.E., 1998. Body size effects and rates of cytochrome b evolution in tube-nosed seabirds. Mol. Biol. Evol. 15, 1360-1371 doi: 10.1093/oxfordjournals.molbev.a025864
    Omote, K., Surmach, S.G., Kohyama, T.I., Takenaka, T., Nishida, C., Masuda, R., 2018. Phylogeography of continental and island populations of Blakiston’s Fish-Owl (Bubo blakistoni) in Northeastern Asia. J. Raptor Res. 52, 31-41 doi: 10.3356/JRR-16-65.1
    Prawiradilaga, D.M., Baveja, P., Suparno, S., Ashari, H., Ng, N.S., Gwee, C.Y., et al., 2018. A colourful new species of Myzomela honeyeater from Rote Island in Eastern Indonesia. Treubia 44, 77-100 doi: 10.14203/treubia.v44i0.3414
    Penteriani, V., 2002. Variation in the function of Eagle Owl vocal behaviour: territorial defence and intra-pair communication? Ethol. Ecol. Evol. 14, 275-281 doi: 10.1080/08927014.2002.9522746
    Pons, J.-M., Kirwan, G.M., Porter, R.F., Fuchs, J., 2013. A reappraisal of the systematic affinities of Socotran, Arabian and East African scops owls (Otus, Strigidae) using a combination of molecular, biometric and acoustic data. Ibis 155, 518-533 doi: 10.1111/ibi.12041
    Price, J.J., Friedman, N.R., Omland, K.E., 2007. Song and plumage evolution in the New World orioles (Icterus) show similar lability and convergence in patterns. Evol. Int. J. Organ. Evol. 61, 850-863 doi: 10.1111/j.1558-5646.2007.00082.x
    Pukinskii, Y.B., 1973. Ecology of Blakiston’s Fish Owl in the Bikin river basin. Byull. Mosk. O-va Ispyt. Prir. Otd. Biol. 78, 40-47 (In Russian with English summary)
    Pukinskii, Y.B., 1974. Blakiston’s Fish Owl vocal reactions. Vestn. Leningr. Univ. 3, 35-39 (In Russian with English summary)
    Pukinskii, Y.B., 1993. Blakiston’s fish owl – Ketupa blakistoni. In: Numerov, A.D. (Ed.), The Birds of Russia and Contiguous Regions: Pterocliformes, Columbiformes, Cuculiformes, Strigiformes. Nauka, Moskow, pp. 290–302 (in Russian).
    R Core Team, 2018. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna. https://www.R-project.org. (Accessed 1 February 2020).
    Rasmussen, P.C., Allen, D.N.S., Collar, N.J., DeMeulemeester, B., Hutchinson, R.O., Jakosalem, P.G.C., et al., 2012. Vocal divergence and new species in the Philippine Hawk Owl Ninox philippensis complex. Forktail 28, 1-20
    Rheindt, F.E., Eaton, J.A., Verbelen, F., 2011. Vocal trait evolution in a geographic leapfrog pattern: speciation of the Maroon-chinned Fruit Dove (Ptilinopus subgularis) complex from Wallacea. Wilson J. Ornit. 123, 429-440 doi: 10.1676/10-148.1
    Rheindt, F.E., Edwards, S.V., 2011. Genetic introgression: an integral but neglected component of speciation in birds. Auk. 128, 620-632 doi: 10.1525/auk.2011.128.4.620
    Reeves, A.B., Drovetski, S.V., Fadeev, I.V., 2008. Mitochondrial DNA data imply a stepping-stone colonization of Beringia by arctic warbler Phylloscopus borealis. J. Avian Biol. 39, 567-575 doi: 10.1111/j.0908-8857.2008.04421.x
    Sadanandan, K.R., Tan, D.J., Schjoelberg, K., Round, P.D., Rheindt, F.E., 2015. DNA reveals long-distance partial migratory behavior in a cryptic owl lineage. Avian Res. 6, 25 doi: 10.1186/s40657-015-0035-9
    Saitoh, T., Sugita, N., Someya, S., Iwami, Y., Kobayashi, S., Kamigaichi, H., et al., 2015. DNA barcoding reveals 24 distinct lineages as cryptic bird species candidates in and around the Japanese Archipelago. Mol. Eco. Resour. 15, 177-186 doi: 10.1111/1755-0998.12282
    Sangster, G., King, B.F., Verbelen, P., Trainor, C.R., 2013. A new owl species of the genus Otus (Aves: Strigidae) from Lombok, Indonesia. PLoS ONE 8, e53712 doi: 10.1371/journal.pone.0053712
    Sangster, G., Rozendaal, F.G., 2004. Systematic notes on Asian birds. Territorial songs and species-level taxonomy of nightjars of the Caprimulgus macrurus complex, with the description of a new species. Zool Verh Leiden. 350, 7-45
    Seebohm, H., 1895. Bulletin of the British Ornithologists’ Club. Ibis 5, 4
    Slaght, J.C., Surmach, S.G., 2008. Biology and conservation of Blakiston’s Fish-Owls (Ketupa blakistoni) in Russia: a review of the primary literature and an assessment of the secondary literature. J. Raptor Res. 42, 29-37 doi: 10.3356/JRR-06-89.1
    Slaght, J.C., Takenaka, T., Surmach, S.G., Fujimaki, Y., Utekhina, I.G., Potapov, E.R., 2018. Global distribution and population estimates of Blakiston's Fish Owl. In: Nakamura, F. (Ed.), Biodiversity Conservation Using Umbrella Species. Ecological Research Monographs. Springer, Singapore, pp. 9–18.
    Sun, C.H., Liu, H.Y., Lu, C.H., 2020. Five new mitogenomes of Phylloscopus (Passeriformes, Phylloscopidae): Sequence, structure, and phylogenetic analyses. Int. J. Biol. Macromol. 146, 638-647 doi: 10.1016/j.ijbiomac.2019.12.253
    Taczanowski, L., 1891. Faune Ornitologique de la Siberie orientale. Premiere partie. Memoris de l’Academie Imperiale des Sciences de St Petersbourg. Serie 7, 1278 (in French)
    Takenaka, T., 1998. Distribution, Habitat Environments, and Reasons for Reduction of the Endangered Blakiston’s Fish Owl in Hokkaido, Japan. Ph.D thesis. Hokkaido University, Sapporo, Japan.
    Takenaka, T., 2018. Ecology and conservation of Blakiston's fish owl in Japan. In: Nakamura, F. (Ed.), Biodiversity Conservation Using Umbrella Species. Ecological Research Monographs. Springer, Singapore, pp. 19–46.
    Talebinejad, M.R., Dastjerdi, H.V., 2005. A cross-cultural study of animal metaphors: When owls are not wise! Metaphor Symb. 20, 133-150 doi: 10.1207/s15327868ms2002_3
    Turner, D.A., Pearson, D.J., 2015. Systematic and taxonomic issues concerning some East African bird species, notably those where treatment varies between authors. Scopus 34, 1-23
    Turner, D.A., Pearson, D.J., Zimmerman, D.A., 1991. Taxonomic notes on some East African birds. Pt. 1, Nonpasserines. Scopus. 14, 84-91 doi: 10.1017/S0003975600006160
    Wang, S., Xu, X., Shrestha, N., Zimmermann, N.E., Tang, Z., Wang, Z. 2017. Response of spatial vegetation distribution in China to climate changes since the Last Glacial Maximum (LGM). PLoS ONE 12, e0175742 doi: 10.1371/journal.pone.0175742
    Weir, J.T., Schluter, D., 2004. Ice sheets promote speciation in boreal birds. Proc. Royal Soc. B. 271, 1881-1887 doi: 10.1098/rspb.2004.2803
    Winkler, D.W., Billerman, S.M., Lovette, I.J., 2020. Owls (Strigidae), version 1.0. In: Billerman, S.M., Keeney, B.K., Rodewald, P.G., Schulenberg, T.S. (Eds.), Birds of the World. Cornell Lab of Ornithology, Ithaca, NY, USA. https://doi.org/10.2173/bow.strigi1.01.
    Yakovlev, B.P., 1929. Animal world of Manchuria: birds. Obshchestvo Izucheniya Manchzhurskovo Kraiya, Kharbin. Serie A. 33, 1-51 (in Russian)
    Yamamoto, S., 1999. The Blakiston's Fish Owl. Hokkaido Shinbun Press, Japan (in Japanese).
    Yoshii, C., Yamaura, Y., Nakamura, F., 2018. Predicting future range expansions of Blakiston's fish owl subject to conservation efforts. In: Nakamura, F. (Ed.), Biodiversity Conservation Using Umbrella Species. Ecological Research Monographs. Springer, Singapore, pp. 221–236.
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