Skip to main content Accessibility help

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

  • Kevin D. Floate (a1) and Paul C. Coghlin (a1)


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.

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]


Corresponding author

2 Corresponding author (e-mail:


Hide All

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



Hide All
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 10.11/i1536-2442-10-11.pdf [accessed 29 March 2010].
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.
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.
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.
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.
Clarke, G.M. 1993 b. Patterns of developmental stability of Chrysopa perla L. (Neuroptera: Chrysopidae) in response to environmental pollution. Environmental Entomology, 22: 13621366.
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.
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.
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.
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.
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.
Görür, G. 2009. Zinc and cadmium accumulation in cabbage aphid (Brevicoryne brassicae) host plants and developmental instability. Insect Science, 16: 6571.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
SAS Institute Inc. 2004. SASH. Version 9.1.3 [computer program]. SAS Institute Inc., Cary, North Carolina.
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.
Strong, L., and James, S. 1993. Some effects of ivermectin on the yellow dung fly, Scatophaga stercoraria. Veterinary Parasitology, 48: 181191.
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.
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.
Systat Software, Inc. 2004. SYSTATH. Version 11. Systat Software, Inc., Point Richmond, California.
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.
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.
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.

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

  • Kevin D. Floate (a1) and Paul C. Coghlin (a1)


Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed