Abstract
Euscarthmus pygmy-tyrants include two species of tiny passerines that inhabit semi-open landscapes in South America. One of these, Euscarthmus meloryphus is a taxonomic complex comprising three recognized subspecies for which previously proposed splits and lumps were not founded on proper taxonomic analysis. We assessed morphology (morphometrics and plumage), distribution models, and vocalizations of a substantial dataset with the aim of evaluating species limits within the E. meloryphus complex. Our results support the recognition of two species, the widespread E. meloryphus from east-central South America, and E. fulviceps from Ecuador and Peru, which are clearly diagnosable on morphological and vocal characters. We consider that E. meloryphus paulus from Colombia and Venezuela is a synonym of the nominotypical taxon based on the absence of diagnostic vocal and morphological characters. The allopatric distribution of the two populations of E. meloryphus may be related to the savannah connections during the LGM in South America. Further, we show that Lepturus ruficeps Swainson, 1838 is a synonym of E. rufomarginatus instead of E. meloryphus as it has long been treated.
References
Aleixo, A. (2007) Conceitos de espécie e o eterno conflito entre continuidade e operacionalidade: uma proposta de normatização de critérios para o reconhecimento de espécies pelo Comitê Brasileiro de Registros Ornitológicos. Revista Brasileira de Ornitologia, 15 (2), 297–310.
Ames, P.L. (1971) The Morphology of the Syrinx in Passerine Birds. Peabody Museum of Natural History Bulletin 37. Peabody Museum of Natural History, New Haven, 194 pp.
Benson, C.W. (1999) Type Specimens of Bird Skins in the University Museum of Zoology, Cambridge, United Kingdom. Cambridge University Museum of Zoology, Cambridge, 221 pp.
Bioacoustics Research Program (2014) Raven Pro: Interactive Sound Analysis Software. Version 1.5. The Cornell Lab of Ornithology, Ithaca. [program]
Cory, C.B. & Hellmayr, C.E. (1927) Catalogue of birds of the Americas and the adjacent islands, Part V, Tyrannidae. Field Museum of Natural History Zoological Series, 13, 1–517.
Cracraft, J. (1983) Species concepts and speciation analysis. Current Ornithology, 1, 159–187.
https://doi.org/10.1007/978-1-4615-6781-3_6
Cracraft, J. (1987) Species concepts and the ontology of evolution. Biology and Philosophy, 2, 329–346.
https://doi.org/10.1007/BF00128837
Cuervo, A.M., Stiles, F.G., Lentino, M., Brumfield, R.T. & Derryberry, E.P. (2014) Geographic variation and phylogenetic relationships of Myiopagis olallai (Aves: Passeriformes; Tyrannidae), with the description of two new taxa from the northern Andes. Zootaxa, 3873 (1), 1–24.
https://doi.org/10.11646/zootaxa.3873.1.1
del Hoyo, J., Collar, N. & Kirwan, G.M. (2019) Tawny-fronted Pygmy-tyrant (Euscarthmus fulviceps). 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://birdsoftheworld.org/bow/species/tcptyr1/cur/introduction (accessed 23 June 2020)
Dubois, A. (2000) Synonymies and related lists in zoology: general proposals, with examples in herpetology. Dumerilia, 4, 33–98.
Dunn, O.J. (1961) Multiple comparisons among means. Journal of the American Statistical Association, 56 (293), 52–64.
https://doi.org/10.1080/01621459.1961.10482090
Eck, S., Fiebig, J., Fiedler, W., Heynen, I., Nicolai, B., Töpfer, T., van den Elzen, R., Winkler, R. & Woog, F. (2011) Measuring Birds. Deutsche Ornithologischen-Gesellschaft, Wilhelmshaven, 118 pp.
Elith, J., Phillips, S.J., Hastie, T., Dudík, M., Chee, Y.E. & Yates, C.J. (2011) A statistical explanation of MaxEnt for ecologists. Diversity and Distributions, 17, 43–57.
https://doi.org/10.1111/j.1472-4642.2010.00725.x
Fitzpatrick, J.W. (2004) Family Tyrannidae (Tyrant-flycatchers). In: del Hoyo, J., Elliott, A. & Christie, D. (Eds.), Handbook of the Birds of the World. Vol. 9. Cotingas to Pipits and Wagtails. Lynx Edicions, Barcelona, pp. 170–462.
Fjeldså, J. & Krabbe, N. (1990) Birds of the High Andes. Apollo Books, Svendborg, 880 pp.
Garzón-Orduña, I.J., Benetti-Longhini, J.E. & Brower, A.V. (2014) Timing the diversification of the Amazonian biota: butterfly divergences are consistent with Pleistocene refugia. Journal of Biogeography, 41 (9), 1631–1638.
https://doi.org/10.1111/jbi.12330
Gill, F., Donsker, D. & Rasmussen, P. (2020) IOC World Bird List. Version 10.1. Available from: http://www.worldbirdnames.org/ (accessed 13 April 2020)
Haffer, J. (1969) Speciation in Amazonian forest birds. Science, 165, 131–137.
https://doi.org/10.1126/science.165.3889.131
Haffer, J. (1974) Avian Speciation in Tropical South America, with a Systematic Survey of the Toucans (Ramphastidae) and Jacamars (Galbulidae). Publications of the Nuttall Ornithological Club No. 14. Nuttall Ornithological Club, Cambridge, Massachusetts, 390 pp.
Hazzi, N.A., Moreno, J.S., Ortiz-Movliav, C. & Palacio, R.D. (2018) Biogeographic regions and events of isolation and diversification of the endemic biota of the tropical Andes. Proceedings of the National Academy of Sciences, 115 (31), 7985–7990.
https://doi.org/10.1073/pnas.1803908115
Hijmans, R.J., Cameron, S.E., Parra, J.L., Jones, P. & Jarvis, A. (2005) Very high resolution interpolated climate surfaces for global land areas. International Journal of Climatology, 25, 1965–1978.
https://doi.org/10.1002/joc.1276
ICZN International Commission on Zoological Nomenclature (1999) International Code of Zoological Nomenclature. The International Trust for Zoological Nomenclature, Natural History Museum, London, 306 pp.
Isler, M.L., Isler, P.R. & Whitney, B.M. (1998) Use of vocalizations to establish species limits in antbirds (Passeriformes: Thamnophilidae). The Auk, 115, 577–590.
https://doi.org/10.2307/4089407s
Kroodsma, D.E. (1984) Songs of the Alder Flycatcher (Empidonax alnorum) and Willow Flycatcher (Empidonax traillii) are innate. The Auk, 101, 13–24.
https://doi.org/10.1093/auk/101.1.13
Kroodsma, D.E. & Konishi, M. (1991) A suboscine bird (Eastern Phoebe, Sayornis phoebe) develops normal song without auditory feedback. Animal Behavior, 42, 477–487.
https://doi.org/10.1016/S0003-3472(05)80047-8
Lanyon, W.E. (1988) A phylogeny of the thirty-two genera in the Elaenia assemblage of tyrant flycatchers. American Museum Novitates, 2914, 1–57.
Lopes, L.E. (2017) Variation of plumage patterns, geographic distribution and taxonomy of the Unicolored Blackbird (Aves: Icteridae). Zootaxa, 4221 (4), 431–456.
https://doi.org/10.11646/zootaxa.4221.4.2
McKitrick, M. & Zink, R. (1988) Species concepts in ornithology. The Condor, 90, 1–14.
https://doi.org/10.2307/1368426
Mittermeier, J.C., Zyskowski, K., Stowe, E.S. & Lai, J.E. (2010) Avifauna of the Sipaliwini Savanna (Suriname) with insights into its biogeographic affinities. Bulletin of the Peabody Museum of Natural History, 51 (1), 97–122.
https://doi.org/10.3374/014.051.0101
Mlíkovskyì, J. (2009) Types of birds in the collections of the Museum and Institute of Zoology, Polish Academy of Sciences, Warszawa, Poland. Part 3: South American birds. Journal of the National Museum, Natural History Series, 178 (5), 17–180.
Ohlson, J.I., Fjeldså, J. & Ericson, P.G.P. (2008) Tyrant flycatchers coming out in the open: phylogeny and ecological radiation of Tyrannidae (Aves: Passeriformes). Zoologica Scripta, 37, 315–335.
https://doi.org/10.1111/j.1463-6409.2008.00325.x
Ohlson, J.I., Irestedt, M., Ericson, P.G.P. & Fjeldså, J. (2013) Phylogeny and classification of the New World suboscines (Aves, Passeriformes). Zootaxa, 3613 (1), 1–35.
https://doi.org/10.11646/zootaxa.3613.1.1
Paynter, R.A. Jr. (1982) Ornithological Gazetteer of Venezuela. Museum of Comparative Zoology, Cambridge, iv + 245 pp.
https://doi.org/10.5962/bhl.title.14633
Paynter, R.A. Jr. (1989) Ornithological Gazetteer of Paraguay. 2nd Edition. Harvard University, Cambridge, iv + 61 pp.
https://doi.org/10.5962/bhl.title.14584
Paynter, R.A. Jr. (1992) Ornithological Gazetteer of Bolivia, 2nd ed. Museum of Comparative Zoology, Cambridge, vi + 185 pp.
https://doi.org/10.5962/bhl.title.14591
Paynter, R.A. Jr. (1993) Ornithological Gazetteer of Ecuador. 2nd Edition. Museum of Comparative Zoology, Cambridge, xi + 247 pp.
Paynter, R.A. Jr. (1994) Ornithological Gazetteer of Uruguay. 2nd Edition. Harvard University, Cambridge, vi + 113 pp.
https://doi.org/10.5962/bhl.title.14632
Paynter, R.A. Jr. (1995) Ornithological Gazetteer of Argentina. 2nd Edition. Harvard University, Cambridge, ix + 1043 pp.
https://doi.org/10.5962/bhl.title.14627
Paynter, R.A. Jr. (1997) Ornithological Gazetteer of Colombia. 2nd Edition. Harvard University, Cambridge, ix + 537 pp.
https://doi.org/10.5962/bhl.title.14638
Paynter, R.A. Jr. & Traylor, M.A. Jr. (1991) Ornithological Gazetteer of Brazil. 2 Vols. Museum of Comparative Zoology, Cambridge, vii + 788 pp.
Pinto, O.M.O. (1944) Catálogo das Aves do Brasil e Lista dos Exemplares Existentes na Coleção do Departamento de Zoologia, 2a parte. Ordem Passeriformes (continuação): Superfamília Tyrannoidea e Subordem Passeres. Departamento de Zoologia, Secretaria da Agricultura, Indústria e Comércio, São Paulo, xii + 700 pp.
https://doi.org/10.5962/bhl.title.100764
R Development Core Team (2016) R: A language and environment for statistical computing. Version 3.1.0. Accessible from http://www.r-project.org/ (accessed 21 August 2016)
Revelle, W.R. (2017) psych: procedures for personality and psychological research. Accessible from http://CRAN.R-project.org/package=psych (accessed 13 May 2017)
Rheindt, F.E., Krabbe, N., Wee, A.K.S. & Christidis, L. (2015) Cryptic speciation in the Lesser Elaenia Elaenia chiriquensis (Aves: Passeriformes: Tyrannidae). Zootaxa, 4032 (3), 251–263.
https://doi.org/10.11646/zootaxa.4032.3.1
Rheindt, F.E., Norman, J.A. & Christidis, L. (2008) DNA evidence shows vocalizations to be a better indicator of taxonomic limits than plumage patterns in Zimmerius tyrant-flycatchers. Molecular Phylogenetics and Evolution, 46, 150–156.
https://doi.org/10.1016/j.ympev.2008.04.016
Ribeiro, V., Werneck, F.P. & Machado, R.B. (2016) Distribution dynamics of South American savanna birds in response to Quaternary climate change. Austral Ecology, 42, 1–6.
https://doi.org/10.1111/aec.12363
Ridgely, R.S. & Tudor, G. (1994) The Birds of South America. Vol. 2. University of Texas Press, Austin, 940 pp.
Ridgway, R. (1905) Descriptions of some new genera of Tyrannidae, Pipridae, and Cotingidae. Proceedings of the Biological Society of Washington, 18, 207–210.
Rull, V. (2011) Neotropical biodiversity: timing and potential drivers. Trends in Ecology & Evolution, 26 (10), 508–513.
https://doi.org/10.1016/j.tree.2011.05.011
Smithe, F.B. (1975) Naturalist’s Color Guide. The American Museum of Natural History, New York, 22 pp.
Stephens, L. & Traylor, M.A. Jr. (1983) Ornithological Gazetteer of Peru. Museum of Comparative Zoology, Cambridge, vi + 271 pp.
Straube, F.C. & Urben-Filho, A. (2006) Dicionário geográfico das expedições zoológicas polonesas ao Paraná. Atualidades Ornitológicas, 133, 1–21.
Sueur, J., Aubin, T. & Simonis, C. (2008) Seewave: a free modular tool for sound analysis and synthesis. Bioacoustics, 18, 213–226.
https://doi.org/10.1080/09524622.2008.9753600
Swainson, W. (1838) The Natural Arrangement and Relations of the Family of Flycatchers, or Muscicapidae. W.H. Lizars, Edinburgh, 256 pp.
Tello, J.G., Moyle, R.G., Marchese, D.J. & Cracraft, J. (2009) Phylogeny and phylogenetic classification of the tyrant flycatchers, cotingas, manakins, and their allies (Aves: Passeriformes: infraorder Tyrannides). Cladistics, 25, 1–39.
https://doi.org/10.1111/j.1096-0031.2009.00254.x
Title, P.O. & Bemmels, J.B. (2017) ENVIREM: An expanded set of bioclimatic and topographic variables increase flexibility and improves performance of ecological niche modeling. Ecography, 41, 291–307.
https://doi.org/10.1111/ecog.02880
Traylor, M.A. Jr. (1979) Subfamily Elaeniinae. In: Traylor, M.A. Jr. (Ed.), Check-list of Birds of the World. Vol. 8. Museum of Comparative Zoology, Cambridge, pp. 3–112.
van Buuren, S. & Groothuis-Oudshoorn, K. (2011) mice: Multivariate Imputation by Chained Equations in R. Journal of Statistical Software, 45 (3), 1–67.
https://doi.org/10.18637/jss.v045.i03
Vanzolini, P.E. (1992) A Supplement to the Ornithological Gazetteer of Brazil. Museu de Zoologia, Universidade de São Paulo, São Paulo, 252 pp.
Wetmore, A. (1926) Observations on the birds of Argentina, Paraguay, Uruguay, and Chile. Bulletin of the United States National Museum, 133, 1–448.
https://doi.org/10.5479/si.03629236.133.i
Willis, E.O. (1967) Behavior of Bicolored Antbirds. University of California Publications in Zoology, 79, 1–132.
Winker, K. (2010) Subspecies represent geographically partitioned variation, a gold mine of evolutionary biology, and a challenge for conservation. Ornithological Monographs, 67, 6–23.
https://doi.org/10.1525/om.2010.67.1.6
Wolfe, J.D., Ryder, T.B. & Pyle, P. (2010) Using molt cycles to categorize the age of tropical birds: an integrative new system. Journal of Field Ornithology, 81, 186–194.
https://doi.org/10.1111/j.1557-9263.2010.00276.x
Zank, C., Becker, F.G., Abadie, M., Baldo, D., Maneyro, R. & Borges-Martins, M. (2014) Climate change and the distribution of Neotropical red-bellied toads (Melanophryniscus, Anura, Amphibia): how to prioritize species and populations? Plos One, 9, 1–11.
https://doi.org/10.1371/journal.pone.0094625
Zimmer, J.T. (1940) Studies of Peruvian birds, No. XXXV. Notes on the genera Phylloscartes, Euscarthmus, Pseudocolopteryx, Tachuris, Spizitornis, Yanacea, Uromyias, Stigmatura, Serpophaga, and Mecocerculus. American Museum Novitates, 1095, 1–19.
Zimmer, J.T. (1955) Further notes on Tyrant Flycatchers (Tyrannidae). American Museum Novitates, 1749, 1–24.