Abstract
The Changeable Hawk-Eagle Nisaetus cirrhatus complex is represented by two taxa in mainland India: N. c. cirrhatus in the northern plains and peninsula and N. c. limnaeetus in the Himalayan foothills. Traditionally these taxa have been regarded as subspecies of one species, but recently they have been proposed to be different species. Here, we use an integrative taxonomic approach based on considerations of plumage, biometrics, genetics and vocalizations. Several plumage characters are significantly different between the two taxa, but crest length was the only one of 56 characters that was diagnostically different, with no overlap. About 30% of the birds had intermediate crest lengths, suggesting that they are hybrids or backcrosses, as also supported by the microsatellite results. PCAs of adult plumage show many intermediate individuals, irrespective of whether these birds were collected near a putative contact zone. There is restricted gene flow between the two taxa, presumably as a result of their largely allopatric distributions. On current knowledge, reproductive isolation appears to be weak at best, and we therefore recommend continuing to regard limnaeetus and cirrhatus as conspecific.
References
Baptista, L.F. & Gaunt, S.L.L. (1994) Advances in studies of avian sound communication. Condor, 96, 817–830.
https://doi.org/10.2307/1369489
Blackburn, T.M. & Gaston, K.L. (1998) Some methodological issues in macroecology. American Naturalist, 51, 6814–6883.
https://doi.org/10.1086/286103
Bortolotti, G.R. (1984) Sexual size dimorphism and age-related size variation in Bald Eagles. Journal of Wildlife Management, 48, 72–81.
https://doi.org/10.2307/3808454
Brandon-Jones, D. (1996) The Asian Colobinae (Mammalia: Cercopithecidae) as indicators of Quaternary climatic change. Biological Journal of the Linnean Society, 59, 327–350.
https://doi.org/10.1006/bijl.1996.0068
Bretagnolle, V. & Thibault, J.-C. (1993) Communicative behaviour in breeding Ospreys (Pandion haliaetus): description and relationship of signals to life history. Auk, 110, 736–751.
https://doi.org/10.2307/4088629
Brown, L. (1979) Birds of Prey, their Biology and Ecology. Hamlyn Publishing Group, London, 400 pp.
Brown, L. & Amadon, D. (1968) Eagles, Hawks, and Falcons of the World. Country Life Books, London, 945 pp.
Clark, W.S., Boesman, P. & Marks, J.S. (2020) Changeable Hawk-eagle (Nisaetus cirrhatus). In: del Hoyo, J., Elliott, A., Sargatal, J., Christie, D.A. & de Juana, E. (Eds.), Handbook of the Birds of the World Alive. Lynx Edicions, Barcelona. Available from: https://www.hbw.com/node/53175 (accessed 13 January 2020)
https://doi.org/10.2173/bow.y00839.01
Dawson, D.A., Horsburgh, G.J., Küpper, C., Stewart, I.R., Ball, A.D., Durrant, K.L., Hansson, B., Bacon, I., Bird, S., Klein, Á., Krupa, A.P., Lee, J.W., Martín-Gálvez, D., Simeoni, M., Smith, G., Spurgin, L.G. & Burke, T. (2010) New methods to identify conserved microsatellite loci and develop primer sets of high cross-species utility—as demonstrated for birds. Molecular Ecology Resources, 10, 475–494.
https://doi.org/10.1111/j.1755-0998.2009.02775.x
Dayrat, B. (2005) Towards integrative taxonomy. Biological Journal of the Linnean Society, 85, 407–415.
https://doi.org/10.1111/j.1095-8312.2005.00503.x
Dickinson, E.C. & Remsen, J.V. Jr. (Eds.) (2013) The Howard and Moore Complete Checklist of the Birds of the World. Vol. 1. 4th Edition. Aves Press, Eastbourne, 512 pp.
Excoffier, L. & Lischer, H.E.L. (2010) Arlequin suite ver. 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Molecular Ecology Resources, 10, 564–567.
https://doi.org/10.1111/j.1755-0998.2010.02847.x
Ferguson-Lees, J. & Christie, D.A. (2005) Raptors of the World: a Field Guide. Christopher Helm, London, 320 pp.
Fleischer, R.C., McIntosh, C.E. & Tarr, C.L. (1998) Evolution on a volcanic conveyor belt: using phylogenetic reconstructions and K-Ar-based ages of the Hawaiian Islands to estimate molecular evolution rates. Molecular Evolution, 7, 533–545.
https://doi.org/10.1046/j.1365-294x.1998.00364.x
Gamauf, A. (2018) Changeable Hawk-eagle Nisaetus cirrhatus. In: Sundev, G. & Yamazaki, T. (Eds.), A Field Guide to the Raptors of Asia. Vol. 2. Sedentary Raptors of Oriental Asia. Asian Raptor Research and Conservation Network, Shiga, pp. 158–159.
Gamauf, A., Gjershaug, J.O., Røv, N., Kvaløy, K. & Haring, E. (2005) Species or subspecies? The dilemma of taxonomic ranking of some south-east Asian hawk-eagles (genus Spizaetus). Bird Conservation International, 15, 99–117.
https://doi.org/10.1017/S0959270905000080
Gamauf, A., Preleuthner, M. & Winkler, H. (1998) Philippine birds of prey: interrelations among habitat, morphology, and behaviour. Auk, 115, 713–726.
https://doi.org/10.2307/4089419
Gautschi, B., Tenzer, I., Müller, J.P. & Schmid, B. (2000), Isolation and characterization of microsatellite loci in the Bearded Vulture (Gypaetus barbatus) and cross-amplification in three Old World vulture species. Molecular Ecology, 9, 2193–2195.
https://doi.org/10.1046/j.1365-294X.2000.105321.x
Gill, F., Donsker, D. & Rasmussen, P.C. (2020) IOC World Bird List. Version 10.1. Available from: https://doi.org/10.14344/IOC.ML.10.1 (accessed 12 May 2020)
Gjershaug, J.O., Kvaløy, K., Røv, N., Prawiradilaga, D.M., Suparman, U. & Rahman, Z. (2004) The taxonomic status of Flores Hawk Eagle Spizaetus floris. Forktail, 20, 55–62.
Gjershaug, J.O., Espmark, Y., Forseth, O.A. & Woldvik, K. (2006) Hybridization between Common Buzzard Buteo buteo and Rough-legged Buzzard B. lagopus in Norway. Bulletin of the British Ornithological Club, 126, 73–80.
Grant, P.R. & Grant, B.R. (1992) Hybridization of bird species. Science, 256, 193–197.
https://doi.org/10.1126/science.256.5054.193
Helbig, A., Knox, A.G., Parkin, D.T., Sangster, G. & Collinson, M. (2002) Guidelines for assigning species rank. Ibis, 144, 518–525.
https://doi.org/10.1046/j.1474-919X.2002.00091.x
Hertel, F. (1995) Ecomorphological indicators of feeding behavior in recent and fossil raptors. Auk, 112, 890–903.
https://doi.org/10.2307/4089021
Hirai, M. & Yamazaki, T. (2010) Isolation and characterization of eleven microsatellite loci in an endangered species, Mountain Hawk-Eagle (Spizaetus nipalensis). Conservation Genetics Resources, 2 (Supplement 1), 113–115.
https://doi.org/10.1007/s12686-010-9226-1 del Hoyo, J., Elliott, A. & Sargatal, J. (Eds.) (1994) Handbook of the Birds of the World. Vol. 4. Lynx Edicions, Barcelona, 638 pp. Isler, M.L., Isler, P.R. & Whitney, B.M. (1999) Species limits in antbirds (Passeriformes: Thamnophilidae): the Myrmotherula surinamensis complex. Auk, 116, 83–96.
https://doi.org/10.2307/4089456
Johnson, P.C., Fowlie, M.K. & Amos, W. (2005) Isolation of microsatellite loci from the Common Buzzard, Buteo buteo (Aves: Accipitridae). Molecular Ecology Notes, 5, 208–211.
https://doi.org/10.1111/j.1471-8286.2005.00878.x
Kipp, S.A. (1959) Die Handflügel-Index als biologisches Mass. Vogelwarte, 20, 77–86.
Mayr, E. & Ashlock, P.D. (1991) Principles of Systematic Zoology. McGraw-Hill, New York, 475 pp.
Mayr, E. & Short Jr., L.L. (1970) Species taxa of North American birds: A contribution to comparative systematics. Bulletin of the Nuttall Ornithological Club, 9, 1–127.
https://doi.org/10.5962/bhl.title.155019
Naoroji, R.K. (1985) Notes on some common breeding raptors of the Rajpipla forest. Journal of Bombay Natural History Society, 82, 278–308.
Naoroji, R.K. (2006) Birds of Prey of the Indian Subcontinent. Christopher Helm, London, 692 pp.
Peakall, R. & Smouse, P.E. (2012) GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research—an update. Bioinformatics, 28 (19), 2537–2539.
https://doi.org/10.1093/bioinformatics/bts460
Preleuthner, M. & Gamauf, A. (1998) A possible new subspecies of the Philippine Hawk-eagle (Spizaetus philippensis) and its future prospects. Journal of Raptor Research, 32, 126–135.
R Core Team (2018) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. Availabel from: https://www.R-project.org/ (accessed 12 May 2020)
Rasmussen, P.C. & Anderton, J.C. (2005) Birds of South Asia: the Ripley guide. Vol. 1 & 2. Lynx Edicions, Barcelona, 378 + 683 pp.
Rasmussen, P.C. & Anderton, J.C. (2012) Birds of South Asia: the Ripley guide. Vols. 1 & 2. Second Edition. National Museum of Natural History, Smithsonian Institution, Michigan State University and Lynx Edicions, Washington, D.C., East Lansing, Michigan and Barcelona, 1062 pp.
Rice, W.R. (1989) Analysing tables of statistical tests. Evolution, 43, 223–225.
https://doi.org/10.1111/j.1558-5646.1989.tb04220.x
Ryan, M.J. & Brenowitz, E.A. (1985) The role of body size, phylogeny, and ambient noise in the evolution of bird song. American Naturalist, 126, 87–100.
https://doi.org/10.1086/284398
Selås, V., Kleven, O. & Steen, O.F. (2017) Female turnover rate differs between two Northern Goshawk Accipiter gentilis nesting areas, as revealed by DNA analysis of moulted feathers. Ibis, 159, 554–566.
https://doi.org/10.1111/ibi.12475
Slate J., Hale, M.C. & Birkhead, T.R. (2007) Simple sequence repeats in Zebra Finch (Taeniopygia guttata) expressed sequence tags: a new resource for evolutionary genetic studies of passerines. BMC Genomics, 8, 52.
https://doi.org/10.1186/1471-2164-8-52
Tobias, J.A., Seddon, N., Spottiswoode, C.N., Pilgrim, J.D., Fishpool, L.D.C. & Collar, N.J. (2010) Quantitative criteria for species delimitation. Ibis, 152, 724–746.
https://doi.org/10.1111/j.1474-919X.2010.01051.x
Venables, W.N. & Ripley, B.D. (2002) Modern Applied Statistics with S. 4th Edition. Springer, New York, XII + 498 pp.
https://doi.org/10.1007/978-0-387-21706-2
Wattel, J. (1973) Geographical Differentiation in the Genus Accipiter. Publications of the Nuttall Ornithological Club No. 13. The Club, Cambridge, Massachusetts, 231 pp.
https://doi.org/10.5962/bhl.title.155250
Zar, J.H. (1999) Biostatistical Analysis. 4th Edition. Prentice Hall, New Jersey, 663 pp.