Arthropod-Plant Interactions

, Volume 5, Issue 1, pp 59–69 | Cite as

Similar responses of insect herbivores to leaf fluctuating asymmetry

Original Paper


Fluctuating asymmetry (FA) represents small, random variation from symmetry and it has been used as an indicator of plant quality and susceptibility to herbivory. In this study, the effects of FA on the responses of distinct herbivore species belonging to several guilds were examined along an environmental gradient in south Florida. This approach was chosen because it relies on a multi-species approach to the study of fluctuating asymmetry and patterns of herbivory between and within plants along an environmental gradient of salinity and plant stress. To examine differences in FA between and within plant communities, seven plant species were investigated. Four of these plants were coastal species and three species occurred in upland communities. Levels of FA were assessed before herbivory and plants were followed for the whole herbivory season in 2006. Coastal plants exhibited significantly higher salt concentration, higher percentage of asymmetric leaves and higher asymmetry levels than upland plants. Herbivore abundance varied widely amongst the seven species studied, but quantitative syntheses of our results indicated significant and positive responses of insect herbivores to leaf asymmetry: insects were 25.11% more abundant on more asymmetric plants and stronger effects of asymmetry were observed for leaf miners compared to gall-formers. As demonstrated by other recent studies, FA might be used as a reliable stress indicator, leading to similar responses of insect herbivores to variation in leaf symmetry.


Fluctuating asymmetry Plant stress Leaf miners Gall-formers Herbivory Coastal-upland comparisons 



This research was supported by the National Science Foundation (NSF grant DEB 03-15190) and T. Cornelissen was partially supported by the Brazilian National Research Council CNPq through a graduate fellowship (grant number 200064/01-0). We thank Andrey Castro and Tere Albarracin for their invaluable help in the field and Sylvia Luckanewick for help in laboratory analyses and leaf measurements.

Supplementary material

11829_2010_9116_MOESM1_ESM.doc (394 kb)
Supplementary material 1 (DOC 394 kb)


  1. Adam P (1990) Saltmarsh ecology. Cambridge University press, Cambridge, UKGoogle Scholar
  2. Anne P, Mawri F, Gladstone S et al (1998) Is fluctuating asymmetry a reliable biomonitor of stress? A test using life history parameters in soybean. Int J Plant Sci 159:559–565CrossRefGoogle Scholar
  3. Bjorksten TA, Fowler K, Pomiankowski A (2000) What does sexual trait FA tell us about stress? Trends Ecol. Evolution 15:163–166Google Scholar
  4. Connor EF, Taverner MP (1997) The evolution and adaptive significance of the leaf-mining habit. Oikos 79:6–25CrossRefGoogle Scholar
  5. Cornelissen TG, Stiling P (2005) Perfect is best: low leaf fluctuating asymmetry reduces herbivory by leaf miners. Oecologia 142:46–56CrossRefPubMedGoogle Scholar
  6. Cornelissen TG, Stiling P (2010) Small variations over large scales: fluctuating asymmetry over the range of two oak species. Int J Plant Sci 171:303–309CrossRefGoogle Scholar
  7. Cornelissen TG, Stiling P, Drake B (2003) Elevated CO2 decrease leaf fluctuating asymmetry and herbivory by leaf miners on two oak species. Glob Change Biol 10:27–36CrossRefGoogle Scholar
  8. Diaz M, Pulido FJ, Moller AP (2004) Herbivore effects on developmental instability and fecundity of holm oaks. Oecologia 139:224–234CrossRefPubMedGoogle Scholar
  9. Escos J, Alados CL, Pugnaire FI et al (2000) Stress resistance strategy in an arid land shrub: interactions between developmental instability and fractal dimension. J Arid Environ 45:325–336CrossRefGoogle Scholar
  10. Falconer DS (1981) Introduction to quantitative genetics, 2nd edn. Longman, New YorkGoogle Scholar
  11. Freeman DC, Brown ML, Duda JJ et al (2004) Developmental instability in Rhus copallinum: multiple stressors, years, and responses. Int J Plant Sci 165:53–63CrossRefGoogle Scholar
  12. Gagné RJ (2004) A catalog of the cecidomyiidae (Diptera) of the world. Memoirs of the Entomological society of Washington, 25. Allen Press, Lawrence, KansasGoogle Scholar
  13. Graham JH, Raz S, Hel-Or H, Nevo E (2010) Fluctuating asymmetry: methods, theory, and applications. Symmetry 2:466–540CrossRefGoogle Scholar
  14. Hochwender CG, Fritz RS (1999) Fluctuating asymmetry in a Salix hybrid system: the importance of genetic versus environmental causes. Evolution 53:408–416CrossRefGoogle Scholar
  15. Hódar JA (2002) Leaf fluctuating asymmetry of Holm oak in response to drought under contrasting climatic conditions. J Arid Environ 52:233–243CrossRefGoogle Scholar
  16. Hoffman AA, Woods RE (2003) Associating environmental stress with developmental stability: problems and patterns. In: Polak M (ed) Developmental Instability—causes and consequences. University Press, Oxford, pp 387–401Google Scholar
  17. Hosken DJ, Blanckenhorn WU, Ward PI (2000) Developmental stability in yellow dung flies (Scathophaga stercoraria): fluctuating asymmetry, heterozygosity and environmental stress. J Evolution Biol 13:919–926CrossRefGoogle Scholar
  18. Huberty AF, Denno RF (2004) Plant water stress and its consequences for herbivorous insects–a new synthesis. Ecology 85:1383–1398CrossRefGoogle Scholar
  19. Hunt J, Allen GR (1998) Fluctuating asymmetry, call structure and the risk of attack from phonotactic parasitoids in the bushcricket Sciarasaga quadrata (Orthoptera: Tettigoniidae). Oecologia 116:356–364CrossRefGoogle Scholar
  20. Inbar M, Kark S (2007) Gender-related developmental instability and herbivory of Pistacia atlantica across a steep environmental gradient. Folia Geobot 42:401–410CrossRefGoogle Scholar
  21. Jentzsch A, Kohler G, Schumacher J (2003) Environmental stress and fluctuating asymmetry in the grasshopper Chorthippus parallelus (Acrididae : Gomphocerinae). Zoology 106:117–125CrossRefPubMedGoogle Scholar
  22. Kanaga MK, LC Latta IV, Mock KE et al (2009) Plant genotypic diversity and environmental stress interact to negatively affect arthropod community diversity. Arthropod-Plant Inte 3:249–258CrossRefGoogle Scholar
  23. Kozlov MV, Wilsey BJ, Koricheva J et al (1996) Fluctuating asymmetry of birch leaves increases under pollution impact. J Appl Ecol 33:1489–1495CrossRefGoogle Scholar
  24. Leamy LJ, Klingenberg CP (2005) The genetics and evolution of fluctuating asymmetry. Annu Rev Ecol Evol S 36:1–21CrossRefGoogle Scholar
  25. Lempa K, Martel J, Koricheva J et al (2000) Covariation of fluctuating asymmetry, herbivory and chemistry during birch leaf expansion. Oecologia 122:354–360CrossRefGoogle Scholar
  26. McKenzie JA, Clarke GM (1988) Diazinon resistance, fluctuating asymmetry and fitness in the Australian sheep blowfly. Genetics 120:213–220PubMedGoogle Scholar
  27. Moller AP (1995) Leaf-mining insects and fluctuating asymmetry in elm Ulmus glabra leaves. J Anim Ecol 64:697–707CrossRefGoogle Scholar
  28. Moller AP, Swaddle JP (1997) Asymmetry, developmental stability, and evolution. University Press, Oxford 291 pGoogle Scholar
  29. Moller AP, VanDongen S (2003) Ontogeny of asymmetry and compensational growth in elm Ulmus glabra leaves under different environmental conditions. Int J Plant Sci 164:519–526CrossRefGoogle Scholar
  30. Moon DC, Stiling P (2004) The influence of salinity and nutrient gradient on coastal vs. upland tritrophic complexes. Ecology 85:2709–2716CrossRefGoogle Scholar
  31. Palmer AR (1996) Waltzing with asymmetry. Bioscience 46:518–553CrossRefGoogle Scholar
  32. Palmer RA, Strobeck C (1986) Fluctuating asymmetry: measurement, analysis, and patterns. Annu Rev Ecol Syst 17:391–421CrossRefGoogle Scholar
  33. Perez-Contreras T, Soler JJ, Soler M (2008) Needle asymmetry, pine vigour and pine selection by the processionary moth Thaumetopoea pityocampa. Acta Oecologica 33:213–221CrossRefGoogle Scholar
  34. Polak M (2003) Developmental instability–causes and consequences. University Press, Oxford, p 459 pGoogle Scholar
  35. Puerta-Pinheiro C, Goméz JM, Hódar JA (2008) Shade and herbivory influence fluctuating asymmetry in a Mediterranean oak. Int J Plant Sci 169:631–635CrossRefGoogle Scholar
  36. Reimchen TE (1997) Parasitism of asymmetrical pelvic phenotypes in threespine stickleback. Can J Zool 75:2084–2094CrossRefGoogle Scholar
  37. Rettig JE, Fuller RC, Corbett AL, Getty T (1997) Fluctuating asymmetry indicates levels of competition in an even-aged poplar clone. Oikos 80:123–127CrossRefGoogle Scholar
  38. Rosenberg MS, Adams DC, Gurevitch J (2000) MetaWin: statistical software for meta-analysis. Version 2.0, Sinauer Associates, SunderlandGoogle Scholar
  39. Roy BA, Stanton ML (1999) Asymmetry in wild mustard, Sinapis arvensis (Brassicaceae), in response to severe physiological stresses. J Evol Biol 12:440–449CrossRefGoogle Scholar
  40. Sakai KI, Shimamoto Y (1965) Developmental instability in leaves and flowers of Nicotinia tabacum. Genetics 51:801–813PubMedGoogle Scholar
  41. Sherry RA, Lord EM (1996) Developmental stability in leaves of Clarkia tembloriensis (Onagraceae) as related to population outcrossing rates and heterozygosity. Evolution 50:80–91CrossRefGoogle Scholar
  42. Sinclair RJ, Hughes L (2010) Leaf miners: the hidden herbivores. Austral Ecol 35:300–313CrossRefGoogle Scholar
  43. Sinclair C, Hoffmann AA (2003) Developmental stability as a potential tool in the early detection of salinity stress in wheat. Int J Plant Sci 164:325–331CrossRefGoogle Scholar
  44. Telhado C, Esteves D, Cornelissen T, Fernandes GW, Carneiro MA (2010) Insect herbivores of Coccoloba cereifera do not select asymmetric plants. Environ Entomol 39:849–855CrossRefPubMedGoogle Scholar
  45. Valkama J, Kozlov MV (2001) Impact of climatic factors on the developmental stability of mountain birch growing in a contaminated area. J Appl Ecol 38:665–673CrossRefGoogle Scholar
  46. Wakefield J, Harris K, Markow TA (1993) Parental age and developmental stability in Drosophila melanogaster. Genetica 89:235–244CrossRefGoogle Scholar
  47. Waring GL, Cobb NS (1992) The impact of plant stress on herbivore population dynamics. In: Bernays E (ed) Insect-Plant interactions, volume IV. CRC Press, Boca Raton, pp 167–226Google Scholar
  48. Weller B, Ganzhorn JU (2004) Carabid beetle community composition, body size, and fluctuating asymmetry along an urban-rural gradient. Basic Appl Ecol 5:193–201CrossRefGoogle Scholar
  49. Wilsey BJ, Haukioja E, Koricheva J, Sulkinoja M (1998) Leaf fluctuating asymmetry increases with hybridization and elevation in tree-line birches. Ecology 79:2092–2099CrossRefGoogle Scholar
  50. Wunderlin RP, Hansen BF (2004) Atlas of Florida Vascular Plants ( [Landry SM, Campbell KN (application development), Florida Center for Community Design and Research.] Institute for Systematic Botany, University of South Florida, Tampa

Copyright information

© Springer Science+Business Media B.V. 2010

Authors and Affiliations

  1. 1.Department of Bioengineering, Ecosystem Bioengineering Building, Campus Tancredo NevesUniversidade Federal de São João Del ReiSão João Del ReiBrazil
  2. 2.Department of Biology SCA 110University of South FloridaTampaUSA

Personalised recommendations