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No support for fluctuating asymmetry as a biomarker of chemical residues in livestock dung1

Published online by Cambridge University Press:  02 April 2012

Kevin D. Floate*
Affiliation:
Lethbridge Research Centre, Agriculture and Agri-Food Canada, 5403 1st Avenue South, P.O. Box 3000, Lethbridge, Alberta, Canada T1J 4B1
Paul C. Coghlin
Affiliation:
Lethbridge Research Centre, Agriculture and Agri-Food Canada, 5403 1st Avenue South, P.O. Box 3000, Lethbridge, Alberta, Canada T1J 4B1
*
2 Corresponding author (e-mail: [email protected]).

Abstract

Fluctuating asymmetries (FAs) are small random deviations between left- and right-side measurements of normally symmetrical traits in a given organism. Changes in FA have frequently been proposed as biomarkers for organisms exposed to stress during development and may have value for detecting low levels of chemical residues or other stressors in the environment. We tested this hypothesis in three replicated laboratory experiments and failed to find any effect of chemical residues (ivermectin) in cattle dung on levels of FAs (wing and leg traits) for the dung-breeding fly Scathophaga stercoraria L. (Diptera: Scathophagidae). In trying to resolve this discrepancy with previous reports, we found that many studies failed to replicate measurements of FA traits within an experiment, which increases the likelihood of spurious positive results. Furthermore, experiments were rarely replicated either within or between studies, so the repeatability of positive results has usually gone untested. These issues have been raised by others, but are still not being adequately addressed. Discussions regarding the value of FAs as biomarkers will not advance until this is done.

Résumé

Les asymétries fluctuantes (FA) sont de petites déviations aléatoires entre les mesures du côté gauche et du côté droit de caractères d'un organisme donné qui sont normalement symétriques. On a souvent proposé d'utiliser les changements dans les FA comme biomarqueurs chez des organismes exposés au stress durant leur développement; ces changements pourraient être utiles pour déceler des concentrations faibles de résidus chimiques ou d'autres facteurs de stress dans le milieu. Nous avons examiné cette hypothèse dans chacune de trois expériences répétées de laboratoire et n’avons pas réussi à trouver d'effet de résidus chimiques (ivermectine) dans les bouses de bétail sur les niveaux des FA (caractères des ailes et des pattes) chez la mouche Scathophaga stercoraria L. (Diptera: Scathophagidae) qui se reproduit dans le fumier. En essayant de comprendre le désaccord entre nos résultats et ceux d'études antérieures, nous observons que plusieurs études avaient négligé de répéter les mesures des caractères de FA dans les expériences, ce qui augmente la possibilité de faux résultats positifs. De plus, les expériences étaient rarement répétées au sein d'une étude ou entre différentes études, si bien que la répétabilité des résultats positifs demeurait invérifiée. Ces problèmes ont été signalés par d'autres chercheurs, mais ils continuent d'être négligés. Les discussions sur la valeur des FA comme biomarqueurs ne pourront progresser tant qu’on ne tiendra pas compte de ces problèmes.

[Traduit par le Rédaction]

Type
Articles
Copyright
Copyright © Entomological Society of Canada 2010

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Footnotes

1

Contribution No. 387-09036 from the Lethbridge Research Centre.

References

Blanckenhorn, W.U., Pemberton, A.J., Bussière, L.F., Römbke, J., and Floate, K.D. 2010. A review of the natural history and laboratory culture methods of the yellow dung fly, Scathophaga stercoraria. Journal of Insect Science, 10: 11. Available from http://www.insectscience.org/ 10.11/i1536-2442-10-11.pdf [accessed 29 March 2010].Google Scholar
Bonada, N., and Williams, D.D. 2002. Exploration of the utility of fluctuating asymmetry as an indicator of river condition using larvae of the caddisfly Hydropsyche morosa (Trichoptera: Hydropsychidae). Hydrobiologia, 481: 147156.Google Scholar
Cárcamo, H.A., Floate, K.D., Lee, B.L., Beres, B.L., and Clarke, F.R. 2008. Developmental instability in a stem-mining sawfly: can fluctuating asymmetry detect plant host stress in a model system? Oecologia, 156: 505513.Google Scholar
Chang, X., Zhai, B., Liu, X., and Wang, M. 2007. Effects of temperature stress and pesticide exposure on fluctuating asymmetry and mortality of Copera annulata (Selys) (Odonata: Zygoptera) larvae. Ecotoxicology and Environmental Safety, 67: 120127. doi:10.1016/j.ecoenv.2006.04.004.Google Scholar
Clarke, G.M. 1993 a. Fluctuating asymmetry of invertebrate populations as a biological indicator of environmental quality. Environmental Pollution, 82: 207211. doi:10.1016/0269-7491(93)90119-9.CrossRefGoogle ScholarPubMed
Clarke, G.M. 1993 b. Patterns of developmental stability of Chrysopa perla L. (Neuroptera: Chrysopidae) in response to environmental pollution. Environmental Entomology, 22: 13621366.Google Scholar
Clarke, G.M., and Ridsdill-Smith, T.J. 1990. The effect of avermectin B1 on developmental stability in the bush fly, Musca vetustissima, as measured by fluctuating asymmetry. Entomologia Experimentalis et Applicata, 54: 265269.Google Scholar
Dobrin, M., and Corkum, L.D. 1999. Can fluctuating asymmetry in adult burrowing mayflies (Hexagenia rigida, Ephemeroptera) be used as a measure of contaminant stress? Journal of Great Lakes Research, 25: 339346.Google Scholar
Floate, K.D., and Fox, A.S. 2000. Flies under stress: a test of fluctuating asymmetry as a biomonitor of environmental quality. Ecological Applications, 10: 15411550.Google Scholar
Floate, K.D., Wardhaugh, K.G., Boxall, A.B., and Sherratt, T.N. 2005. Fecal residues of veterinary parasiticides: nontarget effects in the pasture environment. Annual Review of Entomology, 50: 153179.Google Scholar
Floate, K.D., Bouchard, P., Holroyd, G., Poulin, R., and Wellicome, T.I. 2008. Does doramectin use on cattle indirectly affect the endangered burrowing owl? Rangeland Ecology and Management, 61: 543553.CrossRefGoogle Scholar
Görür, G. 2009. Zinc and cadmium accumulation in cabbage aphid (Brevicoryne brassicae) host plants and developmental instability. Insect Science, 16: 6571.CrossRefGoogle Scholar
Graham, J.H., Roe, K.E., and West, T.B. 1993. Effects of lead and benzene on the developmental stability of Drosophila melanogaster. Ecotoxicology, 2: 185195.Google Scholar
Hardersen, S. 2000. Effects of carbaryl exposure on the last larval instar of Xanthocnemis zealandica — fluctuating asymmetry and adult emergence. Entomologia Experimentalis et Applicata, 96: 221230.Google Scholar
Hardersen, S., Wratten, S.D., and Frampton, C.M. 1999. Does carbaryl increase fluctuating asymmetry in damselflies under field conditions? A mesocosm experiment with Xanthocnemis zealandica (Odonata: Zygoptera). Journal of Applied Ecology, 36: 534543.Google Scholar
Hempel, H., Scheffczyk, A., Schallna, H.J., Lumaret, J.P., Alvinerie, M., and Rombke, J. 2006. Toxicity of four veterinary parasiticides on larvae of the dung beetle Aphodius constans in the laboratory. Environmental Toxicology and Chemistry, 25: 31553163.Google Scholar
Hogg, I.D., Eadie, J.M., Williams, D.D., and Turner, D. 2001. Evaluating fluctuating asymmetry in a stream-dwelling insect as an indicator of low-level thermal stress: a large-scale field experiment. Journal of Applied Ecology, 38: 13261339.Google Scholar
Hosken, D.J., Blanckenhorn, W.U., and Ward, P.I. 2000. Developmental stability in yellow dung flies (Scathophaga stercoraria): fluctuating asymmetry, heterozygosity and environmental stress. Journal of Evolutionary Biology, 13: 919926.Google Scholar
Kokko, E.G., Floate, K.D., Colwell, D.D., and Lee, B. 1996. Measurement of fluctuating asymmetry in insect wings using image analysis. Annals of the Entomological Society of America, 89: 398404.Google Scholar
Labrie, G., Prince, C., and Bergeron, J.M. 2003. Abundance and developmental stability of Pterostichus melanarius (Coleoptera: Carabidae) in organic and integrated pest management orchards of Quebec, Canada. Population Ecology, 32: 123132.Google Scholar
Leung, B., Forbes, M.R., and Houle, D. 2000. Fluctuating asymmetry as a bioindicator of stress: comparing efficacy of analyses involving multiple traits. The American Naturalist, 155: 101115.Google Scholar
Leung, B., Knopper, L.D., and Mineau, P. 2003. A critical assessment of the utility of fluctuating asymmetry as a bioindicator of anthropogenic stress. In Developmental instability: causes and consequences. Edited by Polak, M.. Oxford University Press, Oxford, United Kingdom. pp. 415426.Google Scholar
Liggett, A.C., Harvey, I.F., and Manning, J.T. 1993. Fluctuating asymmetry in Scatophaga stercoraria L.: successful males are more symmetrical. Animal Behavior, 45: 10411043.Google Scholar
Maryanski, M., Kramarz, P., Laskowski, R., and Niklinska, M. 2002. Decreased energetic reserves, morphological changes and accumulation of metals in carabid beetles (Poecilus cupreus L.) exposed to zinc- or cadmium-contaminated food. Ecotoxicology, 11: 127139.Google Scholar
McKenzie, J.A., and Yen, J.L. 1995. Genotype, environment and the asymmetry phenotype. Dieldrin-resistance in Lucilia cuprina (the Australian sheep blowfly). Heredity, 75: 181187.Google Scholar
Mpho, M., Holloway, G.J., and Callaghan, A. 2001. A comparison of the effects of organophosphate insecticide exposure and temperature stress on fluctuating asymmetry and life history traits in Culex quinquefasciatus. Chemosphere, 45: 713720. doi:10.1016/s0045-6535(01)00140-0.Google Scholar
Palmer, A.R. 1994. Fluctuating asymmetry analyses: a primer. In Developmental instability: its origins and evolutionary implications. Edited by Markow, T.. Kluwer, Dordrecht, The Netherlands. pp. 335364.Google Scholar
Palmer, A.R., and Strobeck, C. 2003. Fluctuating asymmetry analysis revisited. In Developmental instability: causes and consequences. Edited by Polack, M.. Oxford University Press, Oxford, United Kingdom. pp. 279319.Google Scholar
Polak, M., Opoka, R. and Cartwright, I.L. 2002. Response of fluctuating asymmetry to arsenic toxicity: support for the developmental selection hypothesis. Environmental Pollution 118: 1928. doi:10.1016/s0269-7491(01)00281-0.Google Scholar
Römbke, J., Floate, K.D., Jochmann, R., Schaäfer, M.A., Puniamoorthy, N., Knaäbe, S., et al. 2009. Lethal and sublethal toxic effects of a test chemical (ivermectin) on the yellow dung fly (Scathophaga stercoraria) based on a standardized international ring test. Environmental Toxicology and Chemistry, 28: 21172124.CrossRefGoogle ScholarPubMed
Rourke, J.W. 2004. An evaluation of fluctuating asymmetry as a tool in identifying imperiled bird populations. M.S. thesis, San Diego State University, San Diego, California.Google Scholar
SAS Institute Inc. 2004. SASH. Version 9.1.3 [computer program]. SAS Institute Inc., Cary, North Carolina.Google Scholar
Strong, L., and James, S. 1992. Some effects of rearing the yellow dung fly Scatophaga stercoraria in cattle dung containing invermectin. Entomologia Experimentalis et Applicata, 63: 3945.Google Scholar
Strong, L., and James, S. 1993. Some effects of ivermectin on the yellow dung fly, Scatophaga stercoraria. Veterinary Parasitology, 48: 181191.Google Scholar
Suárez, V.H., Lifschitz, A.L., Sallovitz, J.M., and Lanusse, C.E. 2009. Effects of faecal residues of moxidectin and doramectin on the activity of arthropods in cattle dung. Ecotoxicology and Environmental Safety, 72: 15511558. doi:10.1016/j.ecoenv.2007.11.009.Google Scholar
Swaddle, J.P. 1997. Developmental stability and predation success in an insect predator–prey system. Behavioral Ecology, 8: 433436. doi:10.1093/beheco/8.4.433.Google Scholar
Systat Software, Inc. 2004. SYSTATH. Version 11. Systat Software, Inc., Point Richmond, California.Google Scholar
Veterinary International Co-operative on Harmonization (VICH). 2004. International cooperation on harmonization of technical requirements for registration of veterinary products: environmental impact assessment (EIAs) for veterinary medicinal products (VMPs)—Phase II. VICH GL38 (Ecotoxicity Phase II). VICH, London, United Kingdom.Google Scholar
Wardhaugh, K.G., Mahon, R.J., Axelsen, A., Rowland, M.W., and Wanjura, W. 1993. Effects of ivermectin residues in sheep dung on the development and survival of the bushfly, Musca vetustissima Walker and a scarabaeine dung beetle, Euoniticellus fulvus Goeze. Veterinary Parasitology, 48: 139157.Google Scholar
Webb, L., Beaumont, D.J., Nager, R.G., and McCracken, D.I. 2007. Effects of avermectin residues in cattle dung on yellow dung fly Scathophaga stercoraria (Diptera: Scathophagidae) populations in grazed pastures. Bulletin of Entomological Research, 97: 129138.Google Scholar