Community Ecology

, Volume 15, Issue 2, pp 131–138 | Cite as

No increase in fluctuating asymmetry in ground beetles (Carabidae) as urbanisation progresses

  • Z. ElekEmail author
  • G. L. Lövei
  • M. Bátki


Environmental stress can lead to a reduction in developmental homeostasis, which could be reflected in increased variability of morphological traits. Fluctuating asymmetry (FA) is one possible manifestation of such a stress, and is often taken as a proxy for individual fitness. To test the usefulness of FA in morphological traits as an indicator of environmental quality, we studied the effect of urbanisation on FA in ground beetles (Carabidae) near a Danish city. First, we performed a critical examination whether morphological character traits suggested in the literature displayed true fluctuating asymmetry in three common predatory ground beetles, Carabus nemoralis, Nebria brevicollis and Pterostichus melanarius. Eight metrical (length of the second and third antennal segments, elytral length, length of the first tarsus segment, length of the first and second tibiae, length of the proximal and distal spines on the first femurs) and one meristic (the number of spines on the second tibiae) traits were examined. Most of them showed FA but not consistently. Females generally displayed a higher level of FA than males. Finally, we examined the changes in the level of FA in bilateral morphological traits along an urbanisation gradient (forest - suburban forest - forest fragments in urban park) to test whether environmental stress created by urbanisation is reflected in FA. Ground beetles common along a Danish urbanisation gradient did not seem to indicate differences in habitat quality by their level of FA.


Developmental instability Fluctuating asymmetry Ground beetles Urbanisation 



analysis of variance


fluctuating asymmetry




measurement error




Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

Supplementary material

42974_2014_15020131_MOESM1_ESM.pdf (179 kb)
Supplementary material, approximately 184 KB.


  1. Aukema, B. 1990. Taxonomy, life-history and distribution of three closely related species of the genus Calathus (Coleoptera: Carabidae). Tijdschr. Entomol. 133: 121–141.Google Scholar
  2. Blair, R.B. 1996. Land use and avian species diversity along an urban gradient. Ecol. Appl. 6: 506–519.CrossRefGoogle Scholar
  3. Blair, R.B. 2004. The effects of urban sprawl on birds at multiple levels of biological organization. Ecol. and Soc. 9(5), <
  4. Bolker, B.M., M.E. Brooks, C.J. Clark, S.W. Geange, J.R. Poulsen, M.H.H. Stevens and J-S.S. White. 2009. Generalized linear mixed models: a practical guide for ecology and evolution. Trends Ecol. Evol. 24: 127–135.CrossRefPubMedGoogle Scholar
  5. Bots, J., S. Van Dongen, T. Adriaens, H.J. Dumont, R. Stoks and H. Van Gossum. 2009. Female morphs of a colour polymorphic damselfly differ in developmental instability and fecundity. Anim. Biol. 59: 41–54.CrossRefGoogle Scholar
  6. Clarke, G.M. 1993. Fluctuating asymmetry of invertebrate populations as a biological indicator of environmental quality. Environ. Pollut. 82: 207–211.CrossRefPubMedGoogle Scholar
  7. Clarke, G.M. 1994. Developmental stability analysis: an early-warning system for biological monitoring of water quality. Aust. J. Biol. 7: 94–104.Google Scholar
  8. Clarke, G.M. 1995. Relationships between developmental stability and fitness: Application for conservation biology. Conserv. Biol. 9: 18–24.CrossRefGoogle Scholar
  9. Clarke, G.M. and T.J. Ridsdill-Smith. 1990. The effect of avermectin B1 on developmental stability in the bush fly, Musca vetustissima, as measured by fluctuating asymmetry. Entomol. Exp. Appl. 54: 265–269.CrossRefGoogle Scholar
  10. Csiki, E. 1908. Magyarország bogárfaunája, vezérfonal a magyar szent korona országainak területén elöforduló bogarak megismerésére. Magyar Nemzeti Múzeum, Budapest.Google Scholar
  11. Elek, Z. and G.L. Lövei. 2005. Ground beetle (Coleoptera, Carabidae) assemblages along an urbanisation gradient near Sorø, Zealand, Denmark. Entomologiske Meddelelser 73: 115–121.Google Scholar
  12. Elek, Z. and G.L. Lövei. 2007. Patterns of ground beetle (Coleoptera: Carabidae) assemblages along an urbanisation gradient in Denmark. Acta Oecol. 32: 104–111.CrossRefGoogle Scholar
  13. Eversham, B.C., D.B. Roy and M.G. Telfer. 1996. Urban industrial and other manmade sites as analogues of natural habitats for Carabidae. Ann. Zool. Fenn. 33: 149–156.Google Scholar
  14. Floate, K.D. and P.C. Coghlin. 2010. No support for fluctuating asymmetry as a biomarker of chemical residues in livestock dung. Can. Entomol. 142: 354–368.CrossRefGoogle Scholar
  15. Floate, K.D. and A.S. Fox. 2000. Flies under stress: a test of fluctuating asymmetry as a biomonitor of environmental quality. Ecol. Appl. 10: 1541–1550.CrossRefGoogle Scholar
  16. Garnier, S., N. Gidaszewski, M. Charlot, J. Rasplus and P. Alibert. 2006. Hybridization, developmental stability, and functionality of morphological traits in the ground beetle Carabus solieri (Coleoptera, Carabidae). Biol. J. Linn. Soc. 89: 151–158.CrossRefGoogle Scholar
  17. Gray, J.S. 1989. Effects of environmental stress on species rich assemblages. Biol. J. Linn. Soc. 37: 19–32.CrossRefGoogle Scholar
  18. Hendrickx, F., J. Maelfait and L. Lens. 2003. Relationship between fluctuating asymmetry and fitness within and between stressed and unstressed populations of the wolf spider Pirata piraticus. J. Evol. Biol. 16: 1270–1279.CrossRefPubMedGoogle Scholar
  19. Henríquez, P., D.S. Donoso and A.A. Grez. 2009. Population density, sex ratio, body size and fluctuating asymmetry of Ceroglossus chilensis (Carabidae) in the fragmented Maulino forest and surrounding pine plantations. Acta Oecol. 35: 811–818.CrossRefGoogle Scholar
  20. Hurd, P. 2010. R script for calculating G test. University of Alberta, Canada. < Scholar
  21. Hurka, K. 1996. Carabidae of the Czech and Slovak Republics. Kabourek, Zlin.Google Scholar
  22. Kowarik, L. 1995. On the role of alien species in urban flora and vegetation. In: Pysek, P.K., M. Parch, M. Rejmanek and P.M. Wade. (ed.), Plant Invasions: General Aspects and Special Problems. SPB Academic, Amsterdam The Netherlands. pp. 85–103.Google Scholar
  23. Labrie, G., C. Prince and J. Bergeron. 2003. Abundance and developmental stability of Pterostichus melanarius (Coleoptera: Carabidae) in organic and integrated pest management orchards of Quebec. Canada. Environ. Entomol. 32: 123–132.CrossRefGoogle Scholar
  24. Légendre, P. 2005. Species associations: the Kendall coefficient of concordance revisited. J. Agr. Biol. Envir. St. 10: 226–245.CrossRefGoogle Scholar
  25. Leung, B. and M. R. Forbes. 1996. Fluctuating asymmetry in relation to stress and fitness: Effects of trait type as revealed by meta-analysis. Ecoscience 3: 400–413.CrossRefGoogle Scholar
  26. Leung, B., M.R. Forbes and D. Houle. 2000. Fluctuating asymmetry as a bioindicator of stress: comparing efficacy of analyses involving multiple traits. Am. Nat. 155: 101–115.CrossRefPubMedPubMedCentralGoogle Scholar
  27. Magura, T., R. Horváth and B. Tóthmérész. 2010a. Effects of urbanization on ground-dwelling spiders in forest patches, in Hungary. Landscape Ecol. 25: 621–629.CrossRefGoogle Scholar
  28. Magura, T., G.L. Lövei and B. Tóthmérész. 2010b. Does urbanization decrease diversity in ground beetle (Carabidae) assemblages? Global Ecol. Biogeogr. 19: 16–26.CrossRefGoogle Scholar
  29. Magura, T., B. Tóthmérész and T. Molnár. 2008. A species-level comparison of occurrence patterns in carabids along an urbanisation gradient. Landscape Urban Plan. 86: 134–140.CrossRefGoogle Scholar
  30. Marzluff, J.M., R. Bowman and R. Donnely. 2001. A historical perspective on urban bird research: trends, terms, and approaches. In: Marzluff, J.M., R. Bowman and R. Donnely (ed.), Avian Ecology in an Urbanizing World. Kluwer Academic, Norwell Massachusetts. pp. 1–17.CrossRefGoogle Scholar
  31. McCabe, J. and L. Partridge. 1997. An interaction between environmental temperature and genetic variation for body size for the fitness of adult female Drosophila melanogaster. Evolution 51: 1164–1174.CrossRefPubMedGoogle Scholar
  32. McIntyre, N.E., J. Rango, W. F. Fagan and S. H. Faeth. 2001. Ground arthropod community structure in a heterogeneous urban environment. Landscape Urban Plan. 52: 257–274.CrossRefGoogle Scholar
  33. Møller, A.P. 1995. Developmental stability and ideal despotic distribution of blackbirds in a patchy environment. Oikos 72: 228–234.CrossRefGoogle Scholar
  34. Møller, A.P. and R. Thornhill. 1997. A meta-analysis of the heritability of developmental stability. J. Evol. Biol. 10: 1–16.CrossRefGoogle Scholar
  35. Niemelä, J., J. Kotze, A. Ashworth, P. Brandmayr, K. Desender, T. New, L. Penev, M. Samways, and J. Spence. 2000. The search for common anthropogenic impacts on biodiversity: a global network. J. Insect Conserv. 4: 3–9.CrossRefGoogle Scholar
  36. Palmer, A.R. 1994. Fluctuating asymmetry analyses: A primer, In: Markow, T.A. (ed.) Developmental Instability: Its Origins and Evolutionary Implications. Kluwer, Dordrecht. pp. 335–364.CrossRefGoogle Scholar
  37. Palmer, A.R. and C. Strobeck. 1986. Fluctuating asymmetry: measurement, analysis, patterns. Annu. Rev. Ecol. Evol. Syst. 17: 391–421.CrossRefGoogle Scholar
  38. Palmer, A.R. and C. Strobeck. 1992. Fluctuating asymmetry as a measure of developmental instability: implications of non-normal distributions and power of statistical tests. Acta Zool-Stockholm 191: 57–72.Google Scholar
  39. Parsons, P.A. 1992. Fluctuating asymmetry: a biological monitor of environmental and genomic stress. Heredity 68: 361–364.CrossRefPubMedGoogle Scholar
  40. Pinheiro, J., D. Bates, S. DebRoy, D. Sarkar and R Development Core Team 2012. nlme: Linear and Nonlinear Mixed Effects Models. R package version 3.1-102. URL:
  41. R Development Core Team 2012. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0, URL: Scholar
  42. Rasband, W. 2003. ImageJ Image processing and analysis in Java. National Institutes of Health, USA. < Scholar
  43. Sapia, M., G.L. Lövei and Z. Elek. 2006. Effects of varying sampling effort on the observed diversity of carabid (Coleoptera: Carabidae) assemblages in the Danglobe Project, Denmark. Ent. Fenn. 17: 345–350.Google Scholar
  44. Smith, B.H., S.M. Garn and P.E. Cole. 1982. Problems of sampling and inference in the study of fluctuating dental asymmetry. Am. J. Phys. Anthropol. 58: 281–289.CrossRefPubMedGoogle Scholar
  45. Soulé, M. 1967. Phenetics of natural populations. II. Asymmetry and evolution in a lizard. Am. Nat. 101: 141–160.CrossRefGoogle Scholar
  46. Valentine, D.W., M.A. Soulé and P. Samollow. 1973. Asymmetry analyses in fishes: a possible statistical indicator of environmental stress. Fish. B-NOAA 71: 357–370.Google Scholar
  47. Van Dongen, S. and L Lens. 2000. The evolutionary potential of developmental stability. J. Evol. Biol. 13: 326–335.CrossRefGoogle Scholar
  48. Vilisics, F., P. Sólymos and E. Hornung. 2005. Measuring fluctuating asymmetry of the terrestrial isopod Trachelipus rathkii (Crustacea: Isopoda, Oniscidea). Eur. J. Soil Biol. 41: 85–90.CrossRefGoogle Scholar
  49. Warnes, G.R. 2012. Gplots: various R programming tools for plotting data. R package version 2.10.1. Url:
  50. Weller, B. and J.U. Ganzhorn. 2004. Carabid beetle community composition, body size, and fluctuating asymmetry along an urban-rural gradient. Basic Appl. Ecol. 5: 193–201.CrossRefGoogle Scholar

Copyright information

© Akadémiai Kiadó, Budapest 2014

This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (, which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made.

Authors and Affiliations

  1. 1.Department of AgroecologyAarhus University, Flakkebjerg Research CentreSlagelseDenmark
  2. 2.Department of Systematic Zoology and EcologyEötvös Loránd UniversityBudapestHungary

Personalised recommendations