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Background

Some studies have indicated that the Horned Larks (Eremophila alpestris) should be considered as a species complex. Recently it split into four species or clades and seven subclades based on genetic, morphological, and biogeographic data. However, other aspects like song divergence have not been studied and several subspecies have not been evaluated, leading to important information gaps in this group of birds. In this work, we aimed to assess the differences in song traits and playback response between the Nearctic subclade and the Neotropical or Colombian subspecies E. a. peregrina.

Methods

We compared six song traits between these groups and performed field playback experiments, to test the response of the Neotropical larks to both songs. We tested the difference in the variables for separate as well as by principal component analysis (PCA).

Results

We found significant differences (p < 0.05) in the individual song traits and the PCA analysis between the two groups. Further, the PCA analysis showed a clearer divergence of the Neotropical songs in comparison to the Nearctic songs of different locations within North America. Similarly, the playback analysis showed a significantly lower response of E. a. peregrina to the songs of the Nearctic larks.

Conclusions

Besides this song divergence, there are important ecological and biogeographic differences between the Neotropical and Nearctic Horned Larks, that indicate an unclear relationship between these two groups. Thus, further morphological and genetic studies are required to clarify the taxonomy of the Neotropical Horned Lark and define if they share the same evolutionary history as the other subspecies of the Nearctic subclade.


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Song divergence indicates an unclear relationship between the Neotropical and Nearctic Horned Larks

Show Author's information Jimmy Alexander Vargas-PuentesLuis Alejandro Arias-Sosa( )Carolina Ramos-Montaño
Grupo Ecología de Organismos (GEO-UPTC), Escuela de Ciencias Biológicas, Universidad Pedagógica Y Tecnológica de Colombia, Tunja, Colombia

Abstract

Background

Some studies have indicated that the Horned Larks (Eremophila alpestris) should be considered as a species complex. Recently it split into four species or clades and seven subclades based on genetic, morphological, and biogeographic data. However, other aspects like song divergence have not been studied and several subspecies have not been evaluated, leading to important information gaps in this group of birds. In this work, we aimed to assess the differences in song traits and playback response between the Nearctic subclade and the Neotropical or Colombian subspecies E. a. peregrina.

Methods

We compared six song traits between these groups and performed field playback experiments, to test the response of the Neotropical larks to both songs. We tested the difference in the variables for separate as well as by principal component analysis (PCA).

Results

We found significant differences (p < 0.05) in the individual song traits and the PCA analysis between the two groups. Further, the PCA analysis showed a clearer divergence of the Neotropical songs in comparison to the Nearctic songs of different locations within North America. Similarly, the playback analysis showed a significantly lower response of E. a. peregrina to the songs of the Nearctic larks.

Conclusions

Besides this song divergence, there are important ecological and biogeographic differences between the Neotropical and Nearctic Horned Larks, that indicate an unclear relationship between these two groups. Thus, further morphological and genetic studies are required to clarify the taxonomy of the Neotropical Horned Lark and define if they share the same evolutionary history as the other subspecies of the Nearctic subclade.

Keywords: Birdsong, Eremophila alpestris peregrina, Song features, Speciation, Reproductive barrier

References(52)

Alström P, Olsson U. On the taxonomic status of Phylloscopus affinis and Phylloscopus subaffinis. Bull Br Ornithol Club. 1992;112: 112–25.

Alström P, Ranft R. The use of sounds in avian systematics and the importance of bird sound archives. Bull Ornithol Club. 2003;123A: 114–35.

Alström P, Rasmussen PC, Olsson U, Sundberg P. Species delimitation based on multiple criteria: the Spotted Bush Warbler Bradypterus thoracicus complex (Aves: Megaluridae). Zool J Linn Soc. 2008;154: 291–307.

Alström P, Barnes KN, Olsson U, Barker FK, Bloomer P, Khan AA, et al. Multilocus phylogeny of the avian family Alaudidae (larks) reveals complex morphological evolution, non-monophyletic genera and hidden species diversity. Mol Phylogenet Evol. 2013;69: 1043–56.

Areta JI, Pearman M. Species limits and clinal variation in a widespread high Andean Furnariid: the Buff-breasted Earthcreeper (Upucerthia validirostris). Condor. 2013;115: 131–42.

Arias-Sosa LA, Vargas-Puentes JA, Ramos-Montaño C, Espinosa-Blanco AS. Population status, habitat use and breeding biology of the endangered Colombian Horned Lark in an Andean wetland. Ardea. 2021;109: 5–14.

Balakrishnan CN, Sorenson MD. Song discrimination suggests premating isolation among sympatric indigobird species and host races. Behav Ecol. 2006;17: 473–8.

Ballentine B, Hyman J, Nowicki S. Vocal performance influences female response to male bird song: an experimental test. Behav Ecol. 2004;15: 163–8.

Beason RC. Horned Lark (Eremophila alpestris). In: Poole A, Gill F, editors. The birds of North America, No. 195. Washington, D. C. : The Academy of Natural Sciences, Philadelphia and the American Ornithologists' Union; 1995. p. 24.https://doi.org/10.2173/bna.horlar.02
DOI

Beason RC, Franks EC. Breeding behavior of the Horned Lark. Auk. 1974;91: 65–74.

Bircher N, van Oers K, Hinde CA, Naguib M. Extraterritorial forays by great tits are associated with dawn song in unexpected ways. Behav Ecol. 2020;31: 873–83.

Botía-Becerra J, Echeverry-Galvis MÁ. First nesting records of the Horned Lark (Eremophila alpestris peregrina) in Colombia. Ornitol Colomb. 2010;10: 55–60.

Cadena CD. Eremophila alpestris. In: Renjifo L, Franco A, Amaya-Espinel J, Kattan G, López-Lanus, editors. Libro rojo aves Colombia Serie Libro Rojos Especies Amenazadas Colomb. Bogotá: Instituto de Investigación de Recursos Biológicos Alexander von Humboldt y Ministerio del Medio Ambiente; 2002. p. 371–4.

Camfield AF, Pearson SF, Martin K. Life history variation between high and low elevation subspecies of horned larks Eremophila spp. J Avian Biol. 2010;41: 273–81.

Cannings RJ, Threlfall W. Horned lark breeding biology at Cape St. Mary's. Newfoundland Wilson Bull. 1981;93: 519–30.

de Gordinho LO, Matheu E, Hasselquist D, Neto JM. Song divergence between subspecies of reed bunting is more pronounced in singing styles under sexual selection. Anim Behav. 2015;107: 221–31.

de Oliveira GL, Hasselquist D, Neto JM. Asymmetric song recognition between recently diverged subspecies of reed bunting. Behav Ecol. 2016;27: 1413–23.

DeGraaf RM, Yamasaki M. New England wildlife: habitat, natural history, and distribution. New Hampshire: University Press of New England; 2001.

Derryberry EP, Seddon N, Derryberry GE, Claramunt S, Seeholzer GF, Brumfield RT, et al. Ecological drivers of song evolution in birds: disentangling the effects of habitat and morphology. Ecol Evol. 2018;8: 1890–905.

Dingle C, Halfwerk W, Slabbekoorn H. Habitat-dependent song divergence at subspecies level in the grey-breasted wood-wren. J Evol Biol. 2008;21: 1079–89.

Dingle C, Poelstra JW, Halfwerk W, Brinkhuizen DM, Slabbekoorn H. Asymmetric response patterns to subspecies-specific song differences in allopatry and parapatry in the gray-breasted wood-wren. Evolution (N Y). 2010;64: 3537–48.

Drovetski SV, Raković M, Semenov G, Fadeev IV, Redkin YA. Limited phylogeographic signal in sex-linked and autosomal loci despite geographically, ecologically, and phenotypically concordant structure of mtDNA variation in the Holarctic avian genus Eremophila. PLoS ONE. 2014;9: e87570.

Freeman BG, Montgomery GA. Using song playback experiments to measure species recognition between geographically isolated populations: a comparison with acoustic trait analyses. Auk. 2017;134: 857–70.

Freeman BG, Class Freeman AM, Hochachka WM. Asymmetric interspecific aggression in New Guinean songbirds that replace one another along an elevational gradient. Ibis. 2016;158: 726–37.

Garry Oak Ecosystems Recovery Team. Eremophila alpestris strigata. Species at risk in Garry Oak and associated ecosystems in British Columbia. 1st ed. Victoria: Garry Oak Ecosystems Recovery Team; 2003.

Ghorbani F, Aliabadian M, Olsson U, Donald PF, Khan AA, Alström P. Mitochondrial phylogeography of the genus Eremophila confirms underestimated species diversity in the Palearctic. J Ornithol. 2019;161: 297–312.

Hamao S, Sugita N, Nishiumi I. Geographical variation in mitochondrial DNA and vocalizations in two resident bird species in the Ryukyu Archipelago. Jpn Bull Natl Mus Nat Sci-A. 2013;39: 51–62.

Hammer Ø, Harper DAT, Ryan PD. Past: paleontological statistics software package for education and data analysis. Palaeontol Electron. 2001;4: 99.

Illes AE, Yunes-Jimenez L. A female songbird out-sings male conspecifics during simulated territorial intrusions. Proc R Soc B. 2009;276: 981–6.

Jankowski JE, Robinson SK, Levey DJ. Squeezed at the top: interspecific aggression may constrain elevational ranges in tropical birds. Ecology. 2010;91: 1877–84.

Kroodsma DE. Falkland Island Sedge Wrens (Cistothorus platensis) imitate rather than improvise large song repertoires. Auk. 2002;119: 523–8.

Leonardo A. Experimental test of the birdsong error-correction model. Proc Natl Acad Sci USA. 2004;101: 16935–40.

Mason NA, Unitt P. Rapid phenotypic change in a native bird population following conversion of the Colorado Desert to agriculture. J Avian Biol. 2018;49: e01507.

Matessi G, Dabelsteen T, Pilastro A. Responses to playback of different subspecies songs in the Reed Bunting Emberiza schoeniclus. J Avian Biol. 2000;31: 96–101.

Matessi G, Dabelsteen T, Pilastro A. Subspecies song discrimination in a Mediterranean population of the reed bunting Emberiza schoeniclus intermedia. Ital J Zool. 2001;68: 311–4.

Mockford EJ, Marshall RC. Effects of urban noise on song and response behaviour in great tits. Proc R Soc B Biol Sci. 2009;276: 2979–85.

Morton ES. The effects of distance and isolation on song-type sharing in the Carolina Wren. Wilson Bull. 1987;99: 601–10.

Pegan TM, Rumelt RB, Dzielski SA, Ferraro MM, Flesher LE, Young N, et al. Asymmetric response of Costa Rican White-breasted Wood-Wrens (Henicorhina leucosticta) to vocalizations from allopatric populations. PLoS ONE. 2015;10: e0144949.

Pieplow ND, Francis CD. Song differences among subspecies of Yellow-eyed Juncos (Junco phaeonotus). Wilson J Ornithol. 2011;123: 464–71.

R Core Team. R: a language and environment for statistical computing; 2020. https://www.r-project.org/.

Rimell AN, Mansfield NJ, Paddan GS. Design of digital filters for frequency weightings (A and C) required for risk assessments of workers exposed to noise. Ind Health. 2015;53: 21–7.

Renjifo LM, Amaya-Villarreal AM, Burbano-Girón J, Velásquez-Tibatá J. Libro rojo de aves de Colombia, Volumen II: Ecosistemas abiertos, secos, insulares, acuáticos continentales, marinos, tierras altas del Darién y Sierra Nevada de Santa Marta y bosques húmedos del centro, norte y oriente del país. Bogotá, D. C., Colombia: Editorial Pontificia Universidad Javeriana e Instituto Alexander von Humboldt; 2016.

Sagario MC, Cueto VR. Evaluación del comportamiento territorial de cuatro especies de aves granívoras en el Monte Central. Hornero. 2014;29: 81–92.

Searcy WA. Measuring responses of female birds to male song. In: McGregor PK, editor. Playback and studies animal communication. Boston: Springer; 1992. p. 175–89.

Slabbekoorn H, Smith TB. Bird song, ecology and speciation. Philos Trans R Soc Lond B Biol Sci. 2002;357: 493–503.

Slater PJB, Mann NI. Why do the females of many bird species sing in the tropics? J Avian Biol. 2004;35: 289–94.

Slender AL, Louter M, Gardner MG, Kleindorfer S. Thick-billed grasswren (Amytornis modestus) songs differ across subspecies and elicit different subspecific behavioural responses. Trans R Soc South Aust. 2018;142: 105–21.

Snijders L, van Oers K, Naguib M. Sex-specific responses to territorial intrusions in a communication network: evidence from radio-tagged great tits. Ecol Evol. 2017;7: 918–27.

Toews DPL, Irwin DE. Cryptic speciation in a Holarctic passerine revealed by genetic and bioacoustic analyses. Mol Ecol. 2008;17: 2691–705.

Turčoková L, Osiejuk TS, Pavel V, Glapan J, Petrusková T. Song divergence of two Bluethroat subspecies (Luscinia s. svecica and L. s. cyanecula). Ornis Fenn. 2010;87: 168–79.

Valencia ID, Armenteras D. Habitat and distribution model of the Horned Lark (Eremophila alpestris peregrina) in the Altiplano of Cundinamarca and Boyacá. Colombia Ornitol Colomb. 2004;2: 25–36.

Zuluaga-Bonilla JE, Macana-García DC. Eremophila alpestris. In: Renjifo LM, Amaya-Villarreal AM, Burbano-Girón J, Velásquez-Tibatá J, editors. Libr. rojo aves Colomb. Vol. II Ecosistemas abiertos, secos, Insul. acuáticos Cont. Mar. tierras altas del Darién y Sierra Nevada St. Marta y bosques húmedos del centro, norte y oriente del país. 2nd ed. Bogotá-Colombia; 2016. p. 335–9.
Publication history
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Publication history

Received: 24 September 2020
Accepted: 30 March 2021
Published: 15 April 2021
Issue date: January 2021

Copyright

© The Author(s) 2021.

Acknowledgements

Acknowledgements

Special thanks to professor Pablo Emilio Rodríguez Africano who managed the resources to develop this research and coordinated the data collection. To the "Corporación Autónoma Regional de Boyacá (CORPOBOYACÁ)" and the "Universidad Pedagógica y Tecnológica de Colombia UPTC", for the financial and logistical support.

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