ENVIRONMENTAL STRESS AND FLUCTUATING ASYMMETRY IN ANTILOPHIA GALEATA, MYIOTHLYPIS FLAVEOLA AND BASILEUTERUS CULICIVORUS IN BRAZILIAN SAVANNA
DOI:
https://doi.org/10.4257/oeco.2021.2501.12Keywords:
anthropogenic disturbance, biomonitors, environmental quality.Abstract
Fluctuating asymmetry (FA), defined as the random difference between two sides of a bilaterally symmetrical character, is often used to monitor biological populations in altered habitats. We aimed to compare the values of FA for wing and tarsi of three bird species (Antilophia galeata, Myiothlypis flaveola and Basileuterus culicivorus) in areas with different environmental stresses and to analyze their potential use as biomonitors. The birds were captured between March 2010 and March 2011, in seven forest fragments. In areas of high environmental stress, FA was higher for the wings of A. galeata and M. flaveola and the tarsi of B. culicivorus. FA depends on the functional importance of the character for each species. Thus, this study demonstrated that FA in wings and tarsi is a useful tool to assess the quality of the Brazilian Savanna (Cerrado) forest habitat.
References
Abeli, T., Zubani, L., Bonomi, C., Parolo, G., & Gargano, D. 2016. Is phenotypic canalization involved in the decline of the endemic Aquilegia thalictrifolia? Rethinking relationships between fluctuating asymmetry and species conservation status. Plant Species Biology, 31, 247–255. DOI: 10.1111/1442-1984.12110
Almeida, R. C. V. 2003. Assimetria flutuante em esqueletos de aves Passeriformes do Estado de Minas Gerais: aspectos metodológicos e implicações sobre a utilização de coleções osteológicas como objeto de estudos de variação temporal de comunidades. Master thesis. Departamento de Zoologia da Pontifícia Universidade Católica de Minas Gerais. p. 59.
Alvares, C. A, Stape, J. L., Sentelhas, P. C., Gonçalves, J. L., & Sparovek, G. 2013. Köppen’s climate classification map for Brazil. Meteorologische Zeitschrift, 22(6), 711–728. DOI: 10.1127/0941-2948/2013/0507
Anciães M., & Marini M. Â. 2000. The effects of fragmentation on fluctuating asymmetry in passerine birds of Brazilian tropical forests. Journal of Applied Ecology, 37, 1013–1028. DOI: 10.1046/j.1365-2664.2000.00554.x
Balmford A., Jones I. L., & Thomas A. L. R. 1993. On avian asymmetry: evidence of natural selection for symmetrical tails and wings in birds. Proceeding of the Royal Society, 252, 245–251. DOI: 10.1098/rspb
Baranov, S. G. 2018. Morphometric analyses of (hidden) directional asymmetry in leaf blades. Emerging Science Journal, 2(4), 170–180. DOI:10.28991/esj-2018-01141
Beasley, D. A. E., Bonisoli-Alquati, A., & Mousseau, T. A. 2013. The use of fluctuating asymmetry as a measure of environmentally induced developmental instability: A meta-analysis. Ecological Indicators, 30, 218–226. DOI: 10.1016/j.ecolind.2013.02.024
Boesing, A. L., Nichols, E., & Metzger, J. P. 2018. Land use type, forest cover and forest edges modulate avian cross-habitat spillover. Journal of Applied Ecology, 55(3), 1252–1264.
CBRO - COMITÊ BRASILEIRO DE REGISTROS ORNITOLÓGICOS. 2015. Listas das aves do Brasil. (Retrieved on April 11th 2020, from http://www.cbro.org.br).
CEMAVE - CENTRO NACIONAL DE PESQUISA E CONSERVAÇÃO DE AVES SILVESTRES. 1994. Manual de Anilhamento de Aves Silvestres – 2ª edição, Brasília: DF. (Retrieved on April 10th 2020, from http: www.icmbio.gov.br/cemave/downloads/finish/7-sna/13-manual-de-anilhamento-de-aves silvestres.html.
Clarke G. M. 1992. Fluctuating asymmetry: a technique for measuring developmental stress of genetic and environmental origin. Acta Zoologica Fennica, 191, 31–35. DOI: 10.1071/BI9860145
Coda, J. J. M., Steinmann, A. R., Priotto, J., & Gomez, M. D. 2017. Fluctuating asymmetry as an indicator of environmental stress in small mammals. Mastozoologia Neotropical, 24(2), 313–321.
Curson, J. 2019. White-striped Warbler (Basileuterus leucophrys). In: J. Del Hoyo, A. Elliott, J. Sargatal, D. A. Christie & E. de Juana (Ed.): Handbook of the birds of the world alive, Barcelona: Lynx Edicions, p. 812
de Godoy, F. I., & Gabriel, V. 2018. Provável híbrido entre Myiothlypis flaveola (Baird, 1865) e M. leucophrys (Pelzeln, 1868) (Passeriformes: Parulidae). Boletim Do Museu Paraense Emílio Goeldi - Ciências Naturais, 14(1), 111–117.
De Coster, G., Van Dongen, S., Malaki, P., Muchane, M., Alcántara-Exposito, A., Matheve, H., & Lens, L. 2013. Fluctuating Asymmetry and Environmental Stress: Understanding the Role of Trait History. PLoS ONE, 8(3), e57966. DOI: 10.1371/journal.pone.0057966
Franchin, A. G., & Marçal Júnior, O. 2004. A riqueza da avifauna no Parque do Sabiá. Biotemas, 17(1), 179–202. DOI: 10.5007/%25x
Gebremichael, G., Tsegaye, D., Bunnefeld, N., Zinner, D., & Atickem A. 2019. Fluctuating asymmetry and feather growth bars as biomarkers to assess the habitat quality of shade coffee farming for avian diversity conservation. Royal Society Open Science, 6, 190013. DOI: 10.1098/rsos.190013
Gonçalves, V. F., & Melo, C. 2012 Fluctuating asymmetry in three Basileuterus (Passeriformes, Parulidae) species in a semideciduous forest fragment in the Brazilian Cerrado. Brazilian Journal of Ecology, 1, 77–81.
Hansbauer, M. M., Storch, I., Leu, S., Nieto-Holguin, J. P., Pimentel, R. G., Knauer, F., & Metzger, J. P. W. 2008. Movements of neotropical understory passerines affected by anthropogenic forest edges in the Brazilian Atlantic rainforest. Biological Conservation, 141(3), 782–791. DOI: 10.1016/j.biocon.2008.01.002
Herring, G., Eagles-Smith, C., & Ackerman, J. T. 2017. Mercury exposure may influence fluctuating asymmetry in waterbirds. Environmental Toxicology and Chemistry, 36(6), 1599–1605. DOI: 10.1002/etc.3688
Hutchison, D. W., & Cheverud, J. M. 1995. Fluctuating asymmetry in Tamarin (Saguinus) cranial morphology: Intra- and interspecific comparisons between taxa with varying levels of genetic heterozygosity. Journal of Hereditary, 86, 280–288. DOI: 10.1093/oxfordjournals.jhered.a111582
Klingenberg, C. P. 2015. Analyzing fluctuating asymmetry with geometric morphometrics: concepts, methods and applications. Symmetry (Basel), 7, 843–934. DOI: 10.3390/sym7020843
Lee, A. C., & Peres C. A. 2008. Conservation value of remnant riparian forest corridors of varying quality for Amazonian birds and mammals. Conservation Biology, 22, 439–449. DOI: 10.1111/j.1523-1739.2007.00870.x
Lens, L., Van Dongen S., & Mathysen, E. 2002a. Fluctuating asymmetry as an early warning system in the critically endangered taita trush. Conservation Biology 16, 479–487. DOI: 10.1046/j.1523-1739.2002.00516.x
Lens, L., Van Dongen S., & Mathysen, E. 2002b. Fluctuating asymmetry as an indicator of fitness: can we bridge the gap between studies? Biological Review, 77, 27–38. DOI: 10.1017/S1464793101005796
Malacco, G. B, Pioli, D., Junior, E. S, Franchin, A. G., Melo, C., Silva, A. M., & Pedroni, F. 2013. Avifauna da Reserva do Clube Caça e Pesca Itororó de Uberlândia [Birds of Clube Caça e Pesca Itororó Reserve from the municipality of Uberlândia]. Atualidades Ornitológicas. 173, 58–71.
Mamedova, A. O. 2009. Bioindication of environmental quality based on plant mutational and modification variability. Cytology and Genetics Journal, 43, 123–125. DOI: 10.3103/S009545270902008X
Manhães, M. A., & Loures-Ribeiro, A. 2011. Avifauna da Reserva Biológica Municipal Poço D'Anta, Juiz de Fora, MG. Biota Neotropica, 11(3), 275–286. DOI: 10.1590/S1676-06032011000300023
Marçal-Júnior, O., Frachin, A. G., Alteff, E. F., Silva-Júnior, E. L., & Melo, C. 2009. Levantamento da avifauna na Reserva Ecológica Panga (Uberlândia, MG, Brasil). Bioscience Journal, 25(6), 149-164.
Marini, M. A. 1992 Foraging behavior and diet of the Helmeted Manakin. Condor, 94, 151–158. DOI: 10.2307/1368804
Marini, M. A., & Cavalcanti R. B. 1993. Habitat and foraging substrate use of three Basileuterus warblers from Central Brazil. Ornitologia Neotropical, 4(2), 69–76.
Martensen, A. C., Pimentel, R. G., & Metzger, J. P. 2008. Relative effects of fragment size and connectivity on bird community in the Atlantic Rainforest: implications for conservation. Biological Conservation, 141(9), 2184–2192. DOI: 10.1016/j.biocon.2008.06.008
Palmer, A. R., & Strobeck, C. 1986. Fluctuating asymmetry: measurement, analysis, patterns. Annual Review of Ecology and Systematic, 45, 391–421. DOI: 10.1146/annurev.es.17.110186.002135
Palmer, A. R., & Strobeck, C. 2003. Fluctuating asymmetry revisited. In: M. Polak (Eds), Developmental instability: causes and consequences. pp. 279–319. New York: Oxford University Press.
Pfeifer, M., Lefebvre, V., Peres, C., Banks-Leite, C., Wearn, O. R., Marsh, C. J., Butchart, S. H. M., Arroyo-Rodríguez, V., Barlow. J., Cerezo, A., Cisneros, L., D’Cruze, N., Faria, D., Hadley, A., Harris, S. M., Klingbeil, B. T., Kormann, U., Lens, L., Medina-Rangel, G. F., Morante-Filho, J. C., Olivier, P., Peters, S. L., Pidgeon, A., Ribeiro, D. B., Scherber, C., Schneider-Maunoury, L., Struebig, M., Urbina-Cardona, N., Watling, J. I., Willig, M. R., Wood, E. M., & Ewers, R. M. 2017. Creation of forest edges has a global impact on forest vertebrates. Nature, 551, 187–191. DOI:10.1038/nature24457
Piacentini, V. Q., Aleixo, A., Agne, C. E., Maurício, G. N., Pacheco, J. F., Bravo, G. A., Brito, G. R. R., Naka, L. N., Olmos, F., Posso, S., Silveira, L. F., Betini, G. S., Carrano, E., Franz, I., Lees, A. C., Lima, L. M., Pioli, D., Schunck, F., Amaral, F. R., Bencke, G. A., Cohn-Haft, M., Figueiredo, L. F. A., Straube, F. C., & Cesari, E. 2015. Annotated checklist of the birds of Brazil by the Brazilian Ornithological Records Committee. Revista Brasileira de Ornitologia, 23(2), 90–298.
Pires, L., & Melo, C. 2019. Individual–resource networks reveal distinct fruit preferences of selective individuals from a generalista population of the Helmeted Manakin. Ibis 162(3), 713–722. DOI: 10.1111/ibi.12794
Rasmuson, M. 2002. Fluctuating asymmetry: indicator of what? Hereditas, 136, 177–183. DOI: 10.1034/j.1601-5223.2002.1360301.x
Rodrigues, A. S. L., & Castro, P. T. A. 2008. Adaptation of a rapid assessment protocol for rivers on rocky meadows. Acta Limnologica Brasiliensia, 20(4), 291–303.
Roos, A. L. 2010. Capturando aves. Ornitologia e conservação: ciência aplicada, técnicas de pesquisa e levantamento, Rio de Janeiro: Technical Books Editora: p. 516.
Sigrist, T. 2006. Aves do Brasil: uma visão artística, 2ª edição, São Paulo: Editora Leitura Dinâmica, p. 672.
Silva, A. M., & Melo C. 2011. Frugivory and seed dispersal by the Helmeted Manakin (Antilophia galeata) in forests of Brazilian Cerrado. Ornitologia Neotropical, 22, 69–77.
Trokovic, N., Herczeg, G., Ghani, N. I., Shikano, T., & Merilä, J. 2012. High levels of fluctuating asymmetry in isolated stickleback populations. BMC Evolutionary Biology, 12(1), 115. DOI: 10.1186/1471-2148-12-115
Van Dongen, S. 2006. Fluctuating asymmetry and developmental instability in evolutionary biology past, present and future. Journal of Evolutionary Biology, 19, 1727–1743. DOI: 10.1111/j.1420-9101.2006.01175.x
Vangestel, C., & Lens, L. 2011. Does fluctuating asymmetry constitute a sensitive biomarker of nutritional stress in house sparrows (Passer domesticus)? Ecological Indicators, 11, 389–394. DOI: 10.1016/j.ecolind.2010.06.009
Zar, J. H. 2010. Biostatistical analysis. New Jersey: Prentice Hall, p. 929.
