Revista de Biología Tropical ISSN Impreso: 0034-7744 ISSN electrónico: 2215-2075

OAI: https://revistas.ucr.ac.cr/index.php/rbt/oai
Fluctuating asymmetry in Apis mellifera (Hymenoptera: Apidae) as bioindicator of anthropogenic environments
PDF
HTML

Keywords

tamaño de centroide
alas anteriores
morfometría geométrica
abejas
forma
antropización.
centroid size
forewings
geometric morphometrics
honeybees
shape
anthropization.

How to Cite

Andrade Nunes, L., Divino de Araújo, E., & Marchini, L. C. (2015). Fluctuating asymmetry in Apis mellifera (Hymenoptera: Apidae) as bioindicator of anthropogenic environments. Revista De Biología Tropical, 63(3), 673–682. https://doi.org/10.15517/rbt.v63i3.15869

Abstract

The successful distribution of A. mellifera is due to their ability to adjust to seasonal variations, considerable control over their internal physical environment and exploration of different resources. However, their populations have experienced different forms and levels of environmental pressure. This research aimed to verify the phenotypic plasticity in both size and shape of wings in A. mellifera using fluctuating asymmetry, based on geometric morphometrics from apiaries located in sites with high and low levels of anthropization. We sampled 16 locations throughout all five geographic regions of Brazil. At each site, samples were collected from 20 beehives installed in apiaries: 10 installed near high anthropogenic environments (Cassilândia - MS, Fortaleza - CE, Maringá - PR, Aquidauana - MS, Rolim de Moura - RO, Riachuelo - SE, Ubiratã - PR and Piracicaba - SP), and 10 in sites with low levels of human disturbance (Cassilândia - MS, Itapiúna CE, União da Vitória - PR, Aquidauana - MS, Rolim de Moura - RO, Pacatuba - SE, Erval Seco - RS, Rio Claro - SP). A sample of 10 individuals was taken in each hive, totaling 200 per location, for a total of 1 600 individuals. We used fluctuating asymmetry (FA) in size and shape of the forewing through geometric morphometrics. The FA analysis was conducted in order to check bilateral differences. The indexes of size and shape were submitted to analysis of variance (ANOVA), where the characters evaluated were used as factors to verify the size and shape differences. The results indicated an asymmetry on the shape of the wing (P < 0.001) but no asymmetry was observed on wing size. Considering FA as an environmental response and high and low impacted areas as a fixed factor, we observed significant differences (P < 0.05). The results for the wing shape in A. mellifera demonstrated that this feature undergoes more variation during ontogeny compared to the variation in size. We concluded that bee samples collected from colonies with higher levels of human disturbance had higher wing-shape asymmetry; the variation of fluctuating asymmetry in the wing shape of honeybees can be used as an indicator of the degree of environmental anthropization.
https://doi.org/10.15517/rbt.v63i3.15869
PDF
HTML

References

Abaga, N. O. Z., Alibert, P., Dousset, S., Savadogo, P. W., Savadogo, M., & Sedogo, M. (2011). Insecticide residues in cotton soils of Burkina Faso and effects of insecticides on fluctuating asymmetry in honey bees (Apis mellifera Linnaeus). Chemosphere, 83(4), 585-592.

Abou-Shaara, H. F., & Al-Ghamdi, A. A. (2012). Studies on wings symmetry and honey bee races discrimination by using standard and geometric morphometrics. Biotechnology in Animal Husbandry, 28(3), 575-584. doi:10.2298/BAH1203575A

Clarke, G. M., & Oldroyd, B. P. (1996). The genetic basis of developmental stability in Apis mellifera II. Relationships between character size, asymmetry and single-locus heterozygosity. Genetica, 97(2), 211-224. doi:10.1007/BF00054628

Clarke, G. M., Oldroyd, B. P., & Hunt, P. (1992). The genetic basis of developmental stability in Apis mellifera: Heterozygosity versus Genic Balance. Evolution, 46, 753-762.

Del Lama, M. A., Gruber, C. V., & Godóy, I. C. de. (2002). Heterozigosidade e assimetria do número de hâmulos em operárias adultas de Apis mellifera (Hymenoptera, Apidae). Revista Brasileira de Entomologia, 46(4), 591-595. doi:10.1590/S0085-56262002000400014

Falconer, D. S. (1989). Introduction to Quantitative Genetics (3rd edn, 438 p.). New York: Longmans Halow, Longman Sci e Tech.

Fuller, R. C., & Houle, D. (2002) Inheritance of developmental instability. In M. Polak (Ed.). Developmental Instability: Causes and Consequences (pp. 157-183). Oxford, United Kingdom: Oxford University Press.

Goodall, C. R. (1991). Procrustes methods in the statistical analysis of shape. Journal of the Royal Statistical Society B, 53, 285-339.

Gotthard, K., & Nylin, S. (1995). Adaptive Plasticity and Plasticity as an Adaptation: A Selective Review of Plasticity in Animal Morphology and Life History. Oikos, 74(1), 3. doi:10.2307/3545669

Klingenberg, C. P., & McIntyre, G. S. (1998). Geometric Morphometrics of Developmental Instability: Analyzing Patterns of Fluctuating Asymmetry with Procrustes Methods. Evolution, 52(5), 1363. doi:10.2307/2411306

Knierim, U., Van Dongen, S., Forkman, B., Tuyttens, F. A. M., Špinka, M., Campo, J. L., & Weissengruber, G. E. (2007). Fluctuating asymmetry as an animal welfare indicator — A review of methodology and validity. Physiology & Behavior, 92(3), 398-421. doi:10.1016/j.physbeh.2007.02.014

Leamy, L. J., & Klingenberg, C. P. (2005). The genetics and evolution of Fluctuating Asymmetry. Annual Review of Ecology, Evolution, and Systematics, 36(1), 1-21. doi:10.1146/annurev.ecolsys.36.102003.152640

Leary, R. F., & Allendorf, F. W. (1989). Fluctuating asymmetry as an indicator of stress: Implications for conservation biology. Trends in Ecology & Evolution, 4(7), 214-217. doi:10.1016/0169-5347(89)90077-3

Lempa, K., Martel, J., Koricheva, J., Haukioja, E., Ossipov, V., Ossipova, S., & Pihlaja, K. (2000). Covariation of fluctuating asymmetry, herbivory and chemistry during birch leaf expansion. Oecologia, 122(3), 354-360. doi:10.1007/s004420050041

Lens, L., Dongen, S. V., Wilder, C. M., Brooks, T. M., & Matthysen, E. (1999). Fluctuating asymmetry increases with habitat disturbance in seven bird species of a fragmented afrotropical forest. Proceedings of the Royal Society B: Biological Sciences, 266(1425), 1241-1246. doi:10.1098/rspb.1999.0769

Mazeed, A. M. M. (2011). Anomalies and asymmetry of wing venation pattern in Carniolan and Egyptian bee populations in Egypt. Egyptian Academic Journal of Biological Sciences, 4(1), 149-161.

Monteiro, L. R., Diniz-Filho, J. A. F., dos Reis, S. F., & Araújo, E. D. (2002). Geometric estimates of heritability in biological shape. Evolution, 56(3), 563. doi:10.1554/0014-3820(2002)056[0563:GEOHIB]2.0.CO;2

Nunes, L. A., Araújo, E. D. de, Marchini, L. C., & Moreti, A. C. de C. C. (2012). Variation morphogeometrics of Africanized honey bees (Apis mellifera) in Brazil. Iheringia. Série Zoologia, 102(3), 321-326. doi:10.1590/S0073-47212012005000002

Oliveira, M. L. de, & Cunha, J. A. (2005). Abelhas africanizadas Apis mellifera scutellata Lepeletier, 1836 (Hymenoptera: Apidae: Apinae) exploram recursos na floresta amazônica? Acta Amazonica, 35(3), 389-394. doi:10.1590/S0044-59672005000300013

Palmer, A. R. (1994). Fluctuating Asymmetry Analyses: A Primer. In T. A. Markow (ed.). Developmental Instability: its Origins and Evolutionary Implications (pp. 335-364). Dordrecht, The Netherlands: Kluwer Academic Publishers.

Palmer, A. R. (1996). Waltzing with Asymmetry: Is fluctuating asymmetry a powerful new tool for biologists or just an alluring new dance step? BioScience, 46(7), 518-532. doi:10.2307/1312930

Palmer, A. R., & Strobeck, C. (1986). Fluctuating Asymmetry: Measurement, Analysis, Patterns. Annual Review of Ecology and Systematics, 17(1), 391-421. doi:10.1146/annurev.es.17.110186.002135

Palmer, R. A., & Strobeck, C. (2003) Fluctuating asymmetry analyses revisited. In M. Polak (Ed.) Developmental instability (DI): causes and consequences (pp. 279-319). Oxford University Press.

Parsons, P. A. (1990). Fluctuating Asymmetry: an epigenetic measure of stress. Biological Reviews, 65(2), 131-145. doi:10.1111/j.1469-185X.1990.tb01186.x

Parsons, P. A. (1992). Fluctuating asymmetry: a biological monitor of environmental and genomic stress. Heredity, 68(4), 361-364. doi:10.1038/hdy.1992.51

Pickett, S. T. A., Cadenasso, M. L., Grove, J. M., Nilon, C. H., Pouyat, R. V., Zipperer, W. C., & Costanza, R. (2001). URBAN ECOLOGICAL SYSTEMS: Linking Terrestrial Ecological, Physical, and Socioeconomic Components of Metropolitan Areas1. Annual Review of Ecology and Systematics, 32(1), 127-157. doi:10.1146/annurev.ecolsys.32.081501.114012

Polak, M., Opoka, R., & Cartwright, I. L. (2002). Response of fluctuating asymmetry to arsenic toxicity: support for the developmental selection hypothesis. Environmental Pollution, 118(1), 19-28. doi:10.1016/S0269-7491(01)00281-0

Rohlf, F. J. (1998). On Applications of Geometric Morphometrics to Studies of Ontogeny and Phylogeny. Systematic Biology, 47(1), 147-158. doi:10.1080/106351598261094

Scheiner, S. M. (1993). Genetics and Evolution of Phenotypic Plasticity. Annual Review of Ecology and Systematics, 24(1), 35-68. doi:10.1146/annurev.es.24.110193.000343

Schneider, S. S., Leamy, L. J., Lewis, L. A., & DeGrandi-Hoffman, G. (2003). The influence of hybridization between african and european honeybees, Apis mellifera, on asymmetries in wing size and shape. Evolution, 57(10), 2350. doi:10.1554/02-609

Silva, M. C., Lomonaco, C., Augusto, S. C., & Kerr, W. E. (2009). Climatic and anthropic influence on size and fluctuating asymmetry of Euglossine bees (Hymenoptera, Apidae) in a semideciduous seasonal forest reserve. Genetics and Molecular Research, 8(2), 730-737. doi:10.4238/vol8-2kerr037

Smith, D. R., Crespi, B. J., & Bookstein, F. L. (1997). Fluctuating asymmetry in the honey bee, Apis mellifera: effects of ploidy and hybridization. Journal of Evolutionary Biology, 10(4), 551-574. doi:10.1046/j.1420-9101.1997.10040551.x

Sokal, R. R., & Rohlf, F. J. 1995. Biometry: the principles and practice of statistics in biological research (3rd ed., p. 887). New York: Freeman.

Swaddle, J. P., Witter, M. S., & Cuthill, I. C. (1994). The analysis of fluctuating asymmetry. Animal Behaviour, 48(4), 986-989. doi:10.1006/anbe.1994.1327

Via, S., Gomulkiewicz, R., De Jong, G., Scheiner, S. M., Schlichting, C. D., & Van Tienderen, P. H. (1995). Adaptive phenotypic plasticity: consensus and controversy. Trends in Ecology & Evolution, 10(5), 212-217. doi:10.1016/S0169-5347(00)89061-8

Via, S., & Lande, R. (1985). Genotype-environment interaction and the evolution of phenotypic plasticity. Evolution, 39, 505-522.

Weller, B., & Ganzhorn, J. U. (2004). Carabid beetle community composition, body size, and fluctuating asymmetry along an urban-rural gradient. Basic and Applied Ecology, 5(2), 193-201. doi:10.1078/1439-1791-00220

Comments

Creative Commons License

This work is licensed under a Creative Commons Attribution 4.0 International License.

Copyright (c) 2015 Revista de Biología Tropical

Downloads

Download data is not yet available.