Volume 13 Issue 1
Mar.  2022
Turn off MathJax
Article Contents
Sook-Young Cho, Hyun-Young Nam, Se-Young Park, Chang-Yong Choi. 2022: Sexual dimorphism and sex-differential migration of Little Buntings (Emberiza pusilla) at an East Asian stopover site. Avian Research, 13(1): 100014. doi: 10.1016/j.avrs.2022.100014
Citation: Sook-Young Cho, Hyun-Young Nam, Se-Young Park, Chang-Yong Choi. 2022: Sexual dimorphism and sex-differential migration of Little Buntings (Emberiza pusilla) at an East Asian stopover site. Avian Research, 13(1): 100014. doi: 10.1016/j.avrs.2022.100014

Sexual dimorphism and sex-differential migration of Little Buntings (Emberiza pusilla) at an East Asian stopover site

doi: 10.1016/j.avrs.2022.100014
More Information
  • Corresponding author: E-mail address: sub95@snu.ac.kr (C. Choi)
  • Received Date: 09 Nov 2021
  • Accepted Date: 21 Feb 2022
  • Publish Date: 02 Mar 2022
  • Sex differences in morphology provide key information for understanding a species' morphological adaptations in relation to the evolution of sexual selection. In migratory birds, morphological traits have adapted to long-distance travel, and sexual dimorphism is typically related to sex-differential migration phenology. Little Buntings (Emberiza pusilla) have one of the longest migrations and are the least dichromatic species among the Emberiza buntings. In this study, we measured sexual size dimorphism and sexual dichromatism of Little Buntings in relation to the spring arrival dates at a stopover site in Korea. Wing length was the most important predictor for identifying sex; the wings of males were longer than those of females. Males also had a significantly stronger chestnut color of the head feathers than females, but this color difference was more prominent in the spring than in the fall. Males arrived earlier than females by four days. Arrival dates correlated with both size and color, but unlike other bunting species previously studied in the same area, there was no clear sex-differential trend in the relationship between arrival date and morphological characteristics. Seasonal differences in the degree of sexual dichromatism suggest that chestnut plumage coloration can be used as a social or sexual signal of males in the breeding season. The correlation of size and color to early arrival regardless of sex may indicate that a preference for assortative mating exists or that a sex-differential migration strategy is not clearly defined in the early stages of northward migration. Our findings on the sexual dimorphism of Little Buntings provide insight into the evolution of the sex-differential migration of buntings in the East Asian Flyway.


  • 1 These authors contributed equally to this work.
  • loading
  • Alstrom, P., Olsson, U., Lei, F., Wang, H., Gao, W., Sundberg, P., 2008. Phylogeny and classification of the Old World Emberizini (Aves, Passeriformes). Mol. Phylogen. Evol. 47, 960-973 doi: 10.1016/j.ympev.2007.12.007
    Badyaev, A.V., Hill, G.E., Dunn, P.O., Glen, J.C., 2001. Plumage color as a composite trait: developmental and functional integration of sexual ornamentation. Am. Nat. 159, 221-235
    Bavoux, C., Burneleau, G., Bretagnolle, V., 2006. Gender determination in the Western Marsh Harrier (Circus aeruginosus) using morphometric and discriminant analysis. J. Raptor Res. 40, 57-64 doi: 10.3356/0892-1016(2006)40[57:GDITWM]2.0.CO;2
    BirdLife International, 2021. Species Factsheet: Emberiza pusilla. http://www.birdlife.org. (Accessed 10 September 2021).
    Bjorklund, M., 1990. A phylogenetic interpretation of sexual dimorphism in body size and ornament in relation to mating system in birds. J. Evol. Biol. 3, 171-183 doi: 10.1046/j.1420-9101.1990.3030171.x
    Brazil, M., 2009. Birds of East Asia: China, Taiwan, Korea, Japan, and Russia. Princeton University Press, Princeton.
    Burnham, K.P., Anderson, D.R., 2002. Model Selection and Multimodel Inference. A Practical Information-Theoretic Approach. Springer-Verlag, New York.
    Byers, C., Olsson, U., Curson, J., 1995. Buntings and Sparrows. Pica Press, Sussex.
    Choi, C-Y., Nam, H-Y., Park, J-G., Bing, G-C., 2019. Migration pattern of Yellow-throated buntings revealed by isotope-based geographic assignment. Int. J. Geogr. Inf. Sci. 34, 504-519
    Cohen, J., 1988. Statistical Power Analysis for the Behavioral Sciences. Routledge Academic, New York.
    Copete, J.L., Marine, R., Bigas, D., Martinez-Vilalta, A., 1999. Differences in wing shape between sedentary and migratory Reed Buntings Emberiza schoeniclus. Bird Study 46, 100-103 doi: 10.1080/00063659909461119
    Cristol, D.A., 1995. Early arrival, initiation of nesting, and social status: an experimental study of breeding female red-winged blackbirds. Behav. Ecol. 6, 87-93 doi: 10.1093/beheco/6.1.87
    Dechaume-Moncharmont, F-X., Monceau, K., Cezilly, F., 2011. Sexing birds using discriminant function analysis: a critical appraisal. Auk 128, 78-86 doi: 10.1525/auk.2011.10129
    Dmitrenok, M., Puglisi, L., Demongin, L., Gilbert, G., Polak, M., Bretagnolle, V., 2007. Geographical variation, sex and age in Great Bittern Botaurus stellaris using coloration and morphometrics. Ibis 149, 37-44 doi: 10.1111/j.1474-919X.2007.00645.x
    Edenius, L., Choi, C-Y., Heim, W., Jaakkonen, T., De Jong, A., Ozaki, K., et al., 2017. The next common and widespread bunting to go? Global population decline in the Rustic Bunting Emberiza rustica. Bird Conserv. Int. 27, 35-44 doi: 10.1017/S0959270916000046
    Fargallo, J.A., Laaksonen, T., Korpimaki, E., Wakamatsu, K., 2007. A melanin-based trait reflects environmental growth conditions of nestling male Eurasian kestrels. Evol. Ecol. 21, 157-171 doi: 10.1007/s10682-006-0020-1
    Francis, C.M., Cooke, F., 1986. Differential timing of spring migration in wood warblers (Parulinae). Auk 103, 548-556
    Galvan, I., Moeller, A.P., 2013. Pheomelanin-based plumage coloration predicts survival rates in birds. Physiol. Biochem. Zool. 86, 184-192 doi: 10.1086/668871
    Giraudeau, M., Toomey, M.B., McGraw, K.J., 2012. Can House Finches (Carpodacus mexicanus) use non-visual cues to discriminate the carotenoid content of foods? J. Ornithol. 153, 1017-1023 doi: 10.1007/s10336-012-0829-z
    Giraudeau, M., Friesen, C.R., Sudyka, J., Rollings, N., Whittington, C.M., Wilson, M.R., et al., 2016. Ageing and the cost of maintaining coloration in the Australian painted dragon. Biol. Lett. 12, 20160077 doi: 10.1098/rsbl.2016.0077
    Griffiths, R., Double, M.C., Orr, K., Dawson, R.J.G., 1998. A DNA test to sex most birds. Mol. Ecol. 7, 1071-1075 doi: 10.1046/j.1365-294x.1998.00389.x
    Hill, G.E., 2006. Female mate choice for ornamental coloration. In: Hill, G.E., McGraw, K. (Eds.), Bird Coloration II – Function and Evolution. Havard University Press, Massachusetts, pp. 137–200.
    Jenni, L., Winkler, R., 1994. Moult and Ageing of European Passerines. Academic Press, London.
    Kamp, J., Oppel, S., Ananin, A.A., Durnev, Y.A., Gashev, S.N., Holzel, N., et al., 2015. Global population collapse in a superabundant migratory bird and illegal trapping in China. Conserv. Biol. 29, 1684-1694 doi: 10.1111/cobi.12537
    Ketterson, E.D., Nolan, V., 1983. The evolution of differential bird migration. Curr. Ornithol. 1, 357-402 doi: 10.1007/978-1-4615-6781-3_12
    Kissner, K.J., Weatherhead, P.J., Francis, C.M., 2003. Sexual size dimorphism and timing of spring migration in birds. J. Evol. Biol. 16, 154-162 doi: 10.1046/j.1420-9101.2003.00479.x
    KNPRI, 2013. 2012–2013 Annual Report of Migratory Bird Research. Korea National Park Research Institute, Wonju.
    Kristensen, D.L., Erikstad, K.E., Reiertsen, T.K., Moum, T., Barrett, R.T., Jenni-Eiermann, S., 2012. Are female offspring from a single-egg seabird more costly to raise? Behav. Ecol. 24, 136-143
    Lee, W.-S., Koo, T.-H., Park, J.-Y., 2000. Field Guide to the Birds of Korea. LG Evergreen Foundation, Seoul.
    Lendvai, A.Z., Giraudeau, M., Nemeth, J., Bako, V., McGraw, K.J., 2013. Carotenoid-based plumage coloration reflects feather corticosterone levels in male house finches (Haemorhous mexicanus). Behav. Ecol. Sociobiol. 67, 1817-1824 doi: 10.1007/s00265-013-1591-9
    Luttrell, S.A.M., Gonzalez, S.T., Lohr, B., Greenberg, R., 2015. Digital photography quantifies plumage variation and salt marsh melanism among Song Sparrow (Melospiza melodia) subspecies of the San Francisco Bay. Auk 132, 277-287 doi: 10.1642/AUK-14-107.1
    MacDougall, A.K., Montgomerie, R., 2003. Assortative mating by carotenoid-based plumage colour: a quality indicator in American goldfinches, Carduelis tristis. Naturwissenschaften 90, 464-467 doi: 10.1007/s00114-003-0459-7
    Mackinnon, J., Phillipps, K., 2000. A Field Guide to the Birds of China. Oxford University Press, New York.
    Maynard Smith, J., Harper, D.G.C., 1988. The evolution of aggression: can selection generate variability? Philos. T. Roy. Soc. B. 319, 557-570
    McGraw, K.J., 2006. Mechanics of melanin-based coloration. In: Hill, G.E., McGraw, K. (Eds.), Bird Coloration I – Mechanisms and Measurements. Harvard University Press, Massachusetts, pp. 243–294.
    McGraw, K.J., Mackillop, E.A., Dale, J., Hauber, M.E., 2002. Different colors reveal different information: how nutritional stress affects the expression of melanin- and structurally based ornamental plumage. J. Exp. Biol. 205, 3747-3755 doi: 10.1242/jeb.205.23.3747
    McKay, B.D., 2013. The use of digital photography in systematics. Biol. J. Linn. Soc. 110, 1-13 doi: 10.1111/bij.12086
    Moeller, A.P., 1994. Phenotype-dependent arrival time and its consequences in a migratory bird. Behav. Ecol. Sociobiol. 35, 115-122 doi: 10.1007/BF00171501
    Monti, F., Gremillet, D., Sforzi, A., Dominici, J.M., Bagur, R.T., Navarro, A.M., et al., 2018. Migration distance affects stopover use but not travel speed: contrasting patterns between long- and short-distance migrating ospreys. J. Avian Biol. 49, e01839 doi: 10.1111/jav.01839
    Morbey, Y., Ydenberg, R.C., 2001. Protandrous arrival timing to breeding areas: a review. Ecol. Lett. 4, 663-673 doi: 10.1046/j.1461-0248.2001.00265.x
    Morrison, D.F., 1976. Multivariate Statistical Methods. McGraw-Hill, New York.
    Mougeot, F., Martinez-Padilla, J., Perez-Rodriguez, L., Bortolotti, G.R., 2007. Carotenoid-based colouration and ultraviolet reflectance of the sexual ornaments of grouse. Behav. Ecol. Sociobiol. 61, 741-751 doi: 10.1007/s00265-006-0304-z
    Nam, H-Y., Choi, C-Y., Park, J-G., Hong, G-P., Won, I-J., Kim, S-J., et al., 2011. Protandrous migration and variation in morphological characters in Emberiza buntings at an East Asian stopover site. Ibis 153, 494-501 doi: 10.1111/j.1474-919X.2011.01134.x
    Nam, H.-Y., Cho, S.-Y., Kim, H.-J., Park, J.-G., Choi, C.-Y., Kwon, Y.-S., 2014. Bird Banding Manual for Constant Effort Surveys in National Parks of Korea. Korea National Park Research Institute, Wonju.
    Nilsson, C., Klaassen, R.H.G., Alerstam, T., 2013. Differences in speed and duration of bird migration between spring and autumn. Am. Nat. 181, 837-845 doi: 10.1086/670335
    Oh, K.P., Badyaev, A.V., 2006. Adaptive genetic complementarity in mate choice coexists with selection for elaborate sexual traits. P. Roy. Soc. Lond. B. 273, 1913-1919 doi: 10.1098/rspb.2006.3528
    Owens, I.P.F., Hartley, I.R., 1998. Sexual dimorphism in birds: why are there so many different forms of dimorphism? P. Roy. Soc. Lond. B. 265, 397-407 doi: 10.1098/rspb.1998.0308
    Piault, R., Gasparini, J., Bize, P., Jenni-Eiermann, S., Roulin, A., 2009. Pheomelanin-based coloration and the ability to cope with variation in food supply and parasitism. Am. Nat. 174, 548-556 doi: 10.1086/605374
    Rohwer, S., 1975. The social significance of avian winter plumage variability. Evolution 29, 593-610 doi: 10.1111/j.1558-5646.1975.tb00853.x
    Rowe, K.M.C., Weatherhead, P.J., 2011. Assortative mating in relation to plumage traits shared by male and female American Robins. Condor 113, 881-889 doi: 10.1525/cond.2011.100207
    Rubolini, D., Spina, F., Saino, N., 2004. Protandry and sexual dimorphism in trans-Saharan migratory birds. Behav. Ecol. 15, 592-601 doi: 10.1093/beheco/arh048
    Safran, R.J., McGraw, K.J., 2004. Plumage coloration, not length or symmetry of tail-streamers, is a sexually selected trait in North American barn swallows. Behav. Ecol. 15, 455-461 doi: 10.1093/beheco/arh035
    Saino, N., Rubolini, D., Serra, L., Caprioli, M., Morganti, M., Ambrosini, R., et al., 2010. Sex-related variation in migration phenology in relation to sexual dimorphism: a test of competing hypotheses for the evolution of protandry. J. Evol. Biol. 23, 2054-2065 doi: 10.1111/j.1420-9101.2010.02068.x
    SAS Institute Inc, 1999. SAS/STAT® User's Guide, Version 8. SAS Institute Inc., Cary.
    Siefferman, L., Wang, Y-J., Wang, Y-P., Yuan, H-W., 2007. Sexual dichromatism, dimorphism, and condition-dependent coloration in blue-tailed bee-eaters. Condor 109, 577-584 doi: 10.1093/condor/109.3.577
    Silva, N., Aviles, J.M., Danchin, E., Parejo, D., 2008. Informative content of multiple plumage-coloured traits in female and male European Rollers. Behav. Ecol. Sociobiol. 62, 1969 doi: 10.1007/s00265-008-0628-y
    Smith, R.J., Moore, F.R., 2005. Arrival timing and seasonal reproductive performance in a long-distance migratory landbird. Behav. Ecol. Sociobiol. 57, 231-239 doi: 10.1007/s00265-004-0855-9
    Svensson, L., 1992. Identification Guide to European Passerines. British Trust for Ornithology, Norfolk.
    Tamada, K., Tomizawa, M., Umeki, M., Takada, M., 2014. Population trends of grassland birds in Hokkaido, focussing on the drastic decline of the Yellow-breasted Bunting. Ornithol. Sci. 13, 29-40 doi: 10.2326/osj.13.29
    Tokolyi, J., Bokony, V., Barta, Z., 2008. Seasonal colour change by moult or by the abrasion of feather tips: a comparative study. Biol. J. Linn. Soc. 94, 711-721 doi: 10.1111/j.1095-8312.2008.01027.x
    Tomek, T., 2002. The birds of North Korea: Passeriformes. Acta Zool. Cracov. 45, 1-235
    Weatherhead, P.J., Clark, R.G., 1994. Natural selection and sexual size dimorphism in red-winged blackbirds. Evolution 48, 1071-1079 doi: 10.1111/j.1558-5646.1994.tb05294.x
    Winkler, H., Leisler, B., 1992. On the ecomorphology of migrants. Ibis 134, 21-28
    Wobker, J., Heim, W., Schmaljohann, H., 2021. Sex, age, molt strategy, and migration distance explain the phenology of songbirds at a stopover along the East Asian flyway. Behav Ecol and Sociobiol 75, 25 doi: 10.1007/s00265-020-02957-3
    Yong, D.L., Liu, Y., Low, B.W., Espanola, C.P., Choi, C-Y., Kawakami, K., 2015. Migratory songbirds in the East Asian-Australasian Flyway: a review from a conservation perspective. Bird Conserv. Int. 25, 1-37 doi: 10.1017/S0959270914000276
    Zuk, M., Johnson, K., Thornhill, R., Ligon, J.D., 1990. Mechanisms of female choice in red jungle fowl. Evolution 44, 477-485 doi: 10.1111/j.1558-5646.1990.tb05933.x
  • 加载中


    通讯作者: 陈斌, bchen63@163.com
    • 1. 

      沈阳化工大学材料科学与工程学院 沈阳 110142

    1. 本站搜索
    2. 百度学术搜索
    3. 万方数据库搜索
    4. CNKI搜索

    Figures(3)  / Tables(3)

    Article Metrics

    Article views (92) PDF downloads(1) Cited by()
    Proportional views


    DownLoad:  Full-Size Img  PowerPoint