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Environmental Science and Pollution Research

, Volume 21, Issue 22, pp 12928–12940 | Cite as

Fluctuating asymmetry in Robinia pseudoacacia leaves—possible in situ biomarker?

  • Nataša Barišić Klisarić
  • Danijela Miljković
  • Stevan Avramov
  • Uroš Živković
  • Aleksej Tarasjev
Research Article

Abstract

In this study, we analyzed fluctuating asymmetry (FA) of black locust (Robinia pseudoacacia) leaf traits as a measure of developmental instability in polluted and unpolluted habitats. We aimed to evaluate the potential of this method as a biomarker and its applicability on widely distributed species under in situ conditions. Leaf samples were taken from seven sites—three categorized as unpolluted (natural protected and rural) and four categorized as polluted covering the broad spectrum of intense pollution (industrial and traffic), from 1,489 individual trees in total. Results revealed significant differences in FA with expected higher values in polluted environments. Applicability of FA of R. pseudoaccacia leaf traits as a biomarker for testing potential pollution level, as well as the amount and distribution of sampling effort needed for its application, are discussed.

Keywords

Biomonitoring Biomarker Developmental instability Fluctuating asymmetry Pollution Robinia pseudoacacia 

Notes

Acknowledgments

This study was supported by the Ministry of Science and Technological Development of the Republic of Serbia research grant no. 173025 “Evolution in heterogeneous environments: mechanisms of adaptation, biomonitoring and conservation of biodiversity.” We thank Ph.D. Biljana Stojković for her assistance in data collection and processing and English language reader, Ph.D. Krinka Vidaković Petrov for her suggestions. We would like to extend our thanks to the anonymous referees for their comments on an earlier draft of this manuscript.

References

  1. Adams SM, Giesy JP, Tremblay LA, Eason CT (2001) The use of biomarkers in ecological risk assessment: recommendations from the Christchurch conference on Biomarkers in Ecotoxicology. Biomarkers 6:1–6CrossRefGoogle Scholar
  2. Agency for Environmental Protection (2012) State of the environment in the Republic of Serbia, report for 2011 Ministry of Energy, development and environmental protection of the Republic of Serbia (in Serbian)Google Scholar
  3. Aksoy A, Sahn U, Duman F (2000) Robinia pseudoacacia L. as a possible biomonitor of heavy metal pollution in Kayseri Turk. J Bot 2:279–284Google Scholar
  4. Alados CL, Navarro T, Esco J, Cabezudo B, Emlen JM (2001) Translational and fluctuating asymmetry as tools to detect stress in stress-adapted and nonadapted plants. Int J Plant Sci 162:67–616CrossRefGoogle Scholar
  5. Allenbach DM (2010) Fluctuating asymmetry and exogenous stress in fishes: a review. Rev Fish Biol Fish 21:355–376CrossRefGoogle Scholar
  6. Ambo-Rappe R, Lajus DL, Schreider MJ (2011) Heavy metal impact on growth and leaf asymmetry of seagrass, Halophila ovalis. J Chem Ecotoxicol 3:149–159Google Scholar
  7. Auty RM (1997) Pollution patterns during the industrial transition. 77th. Geogr J 163:206–215CrossRefGoogle Scholar
  8. Barrett RP, Mebrahtu T, Hanover JW (1990) Black locust: a multi-purpose tree species for temperate climates. In: Janick J, Simon JE (eds) Advances in new crops. Timber Press, Portland, pp 278–283Google Scholar
  9. Beasley DE, Bonisoli-Alquati A, Mousseau TA (2013) The use of fluctuating asymmetry as a measure of environmentally induced developmental instability: a meta-analysis. Ecol Indic 30:218–226CrossRefGoogle Scholar
  10. Burger J, Gochfeld M, Kosson DS, Powers CW (2006) Biomonitoring for ecosystem and human health protection at Amchitka Island. Consortium for Risk Evaluation with Stakeholder Participation II. An organization of The Institute for Responsible Management Piscataway, New JerseyGoogle Scholar
  11. Cairns JJ (1979) Biological monitoring—concept and scope. In: Cairns JJ, Patil GP, Waters WE (eds) Environmental Biomonitoring, Assessment, Prediction and Management—Certain case studies and related quantitative issues. International Co-operative Publishing House Fairland, Maryland, pp 3–20Google Scholar
  12. Chang-Seok L, Hyon-Je C, Hoonbok Y (2003) Stand dynamics of introduced black locust (Robinia pseudoacacia L.) plantation under different disturbance regimes in Korea. For Ecol Manag 189:281–293CrossRefGoogle Scholar
  13. Clarke GM (1993) Fluctuating asymmetry of invertebrate populations as a biological indicator of environmental quality. Environ Pollut 82:207–211CrossRefGoogle Scholar
  14. Clarke GM (1995) Relationships between developmental stability and fitness—application for conservation biology. Conserv Biol 9:18–24CrossRefGoogle Scholar
  15. Cottingham KL, Carpenter SR (1998) Population, community, and ecosystem variates as ecological indicators: phytoplankton responses to whole-lake enrichment. Ecol Appl 8:508–530CrossRefGoogle Scholar
  16. Cuevas-Reyes P, Gilberti L, González-Rodríguez A, Wilson Fernandes G (2013) Patterns of herbivory and fluctuating asymmetry in Solanum lycocarpum St. Hill (Solanaceae) along an urban gradient in Brazil. Ecol Indic 24:557–561CrossRefGoogle Scholar
  17. Day RW, Quinn P (1989) Comparisons of treatments after analysis of variance in ecology. Ecol Monogr 59:433–463CrossRefGoogle Scholar
  18. DeGomez T, Wagner MR (2001) Culture and use of black locust. HortTechnology 11:279–288Google Scholar
  19. Dimitriou I, Aronsson P, Weih M (2006) Stress tolerance of five willow clones after irrigation with different amounts of landfill leachate. Bioresour Technol 97:150–157CrossRefGoogle Scholar
  20. Forbes VE, Palmqvist A, Bach L (2006) The use and misuse of biomarkers in ecotoxicology. Environ Toxicol Chem 25:272–280CrossRefGoogle Scholar
  21. Freeman DC, Graham JH, Emlen JM (1993) Developmental stability in plants: symmetries, stress and epigenesis. Genetica 89:97–119CrossRefGoogle Scholar
  22. Freeman DC, Graham JH, Tracy M, Emlen JM, Alados CL (1999) Developmental instability as a means of assessing stress in plants: a case study using electromagnetic fields and soybeans. Int J Plant Sci 160:157–166CrossRefGoogle Scholar
  23. Freeman DC, Graham JH, Emlen JM, Tracy M, Hough RA, Alados CL, Escós J (2003) Plant developmental instability: new measures, applications, and regulation. In: Polak M (ed) Developmental instability: causes and consequences. Oxford University Press, New York, pp 367–386Google Scholar
  24. Freeman DC, Brown ML, Duda JJ, Graham JH, Emlen JM, Krzysik AJ, Balbach H, Kovacic DA, Zak JC (2004) Photosynthesis and fluctuating asymmetry as indicators of plant response to soil disturbance in the fall-line Sandhills of Georgia: a case study using Rhus copallinum and Ipomoea pandurata. Int J Plant Sci 165:805–816CrossRefGoogle Scholar
  25. Freeman DC, Brown ML, Duda JJ, Graham JH, Emlen JM, Krzysik AJ, Balbach H, Kovacic DA, Zak JC (2005) Leaf fluctuating asymmetry, soil disturbance and plant stress: a multiple year comparison using two herbs, Ipomoea pandurata and Cnidoscolus stimulosus. Ecol Indic 5:85–95CrossRefGoogle Scholar
  26. Godet JP, Demuynck S, Waterlot C, Lemièreb S, Souty-Grossetc C, Douaya F, Leprêtreb A, Pruvota C (2012) Fluctuating asymmetry analysis on Porcellio scaber (Crustacea, Isopoda) populations living under metals—contaminated woody habitats. Ecol Indic 23:130–139CrossRefGoogle Scholar
  27. Graham JH, Freeman DC, Emlen JM (1993) Developmental stability: a sensitive indicator of populations under stress. In: Landis WG, Hughes JS, Lewis MA (eds) Environmental toxicology and risk assessment STP 1179. American Society for Testing and Materials, Philadelphia, pp 136–158CrossRefGoogle Scholar
  28. Graham JH, Raz S, Hel-Or SH, Nevo E (2010) Fluctuating asymmetry: methods, theory, and applications. Asymmetry 2:466–540CrossRefGoogle Scholar
  29. Graham JH, Duda JJ, Brown ML, Kitchen S, Emlen JM, Malol J, Bankstahl E, Krzysik AJ, Balbach H, Freeman DC (2012) The effects of drought and disturbance on the growth and developmental instability of loblolly pine (Pinus taeda L). Ecol Indic 20:143–150CrossRefGoogle Scholar
  30. Gurevitch J, Hedges LV (1999) Statistical issues in ecological meta-analyses. Ecology 80:1142–1149CrossRefGoogle Scholar
  31. Hammond A, Adriaanse A, Rodenburg E, Bryant D, Woodward R (1995) Environmental indicators: a systematic approach to measuring and reporting on environmental policy performance in the context of sustainable development. World Resources Institute, Washington DCGoogle Scholar
  32. Hoffman AA, Parsons PA (1997) Extreme environmental change and evolution. Cambridge University Press, UKGoogle Scholar
  33. Hoffmann AA, Sgrò CM (2011) Climate change and evolutionary adaptation. Nature 470:479–485CrossRefGoogle Scholar
  34. Hogg ID, Eadie JM, Williams DD, Turner D (2001) Evaluating fluctuating asymmetry in a stream-dwelling insect as an indicator of low-level thermal stress: a large-scale field experiment. J Appl Ecol 38:1326–1339CrossRefGoogle Scholar
  35. Jackson LE, Kurtz JC, Fisher WS (2000) Evaluation guidelines for ecological indicators. Environmental Protection Agency, Washington, Report No EPA/620/ R–99/005Google Scholar
  36. Karvonen E, Merila J, Van Dongen S (2003) Geography of fluctuating asymmetry in the Greenfinch (Carduelis chloris). Oikos 100:507–516CrossRefGoogle Scholar
  37. Komac B, Alados CL (2012) Fluctuating asymmetry and Echinospartum horridum fitness components. Ecol Indic 18:252–258CrossRefGoogle Scholar
  38. Kostić O, Mitrović M, Knezević M, Jarić S, Gajić G, Djurdjević L, Pavlović P (2012) The potential of four woody species for the revegetation of fly ash deposits from the ‘Nikola Tesla-A’ thermoelectric plant (Obrenovac, Serbia). Arch Biol Sci 64:145–158CrossRefGoogle Scholar
  39. Kozlov MV, Niemelä P (1999) Difference in needle length—a new and objective indicator of pollution impact on Scots pine (Pinus sylvestris). Water Air Soil Pollut 116:365–370CrossRefGoogle Scholar
  40. Kozlov MV, Wisley BJ, Koricheva J, Haukioja E (1996) Fluctuating asymmetry of birch leaves increases under pollution impact. J Appl Ecol 33:1489–1495CrossRefGoogle Scholar
  41. Lazić MM, Kaliontzopoulou A, Carretero MA, Crnobrnja-Isailović J (2013) Lizards from urban areas are more asymmetric: using fluctuating asymmetry to evaluate environmental disturbance. PLoS One 8(12):e84190CrossRefGoogle Scholar
  42. Lens L, Van Dongen S, Kark S, Matthysen E (2002) Fluctuating asymmetry as an indicator of fitness: can we bridge the gap between studies? Biol Rev 77:27–38CrossRefGoogle Scholar
  43. Leung B, Knopper L, Mineau P (2003) A critical assessment of the utility of fluctuating asymmetry as a bioindicator of anthropogenic stress. In: Polak M (ed) Developmental instability: causes and consequences. Oxford University Press, New York, pp 415–426Google Scholar
  44. López DR, Brizuela MA, Willems P, Aguiar MR, Siffredi G, Bran D (2013) Linking ecosystem resistance, resilience, and stability in steppes of North Patagonia. Ecol Indic 24:1–11CrossRefGoogle Scholar
  45. Mal TK, Uveges JL, Turk KW (2002) Fluctuating asymmetry as an ecological indicator of heavy metal stress in Lythrum salicaria. Ecol Indic 1:189–195CrossRefGoogle Scholar
  46. Markow TA (1995) Evolutionary ecology and developmental instability. Annu Rev Entomol 40:105–120CrossRefGoogle Scholar
  47. McKenzie JA, O’Farrell K (1993) Modification of developmental instability and fitness: malathion resistance in the Australian sheep blowfly, Lucilia cuprina. In: Markow TA (ed) Developmental stability: Its Origins and Evolutionary Implications. Kluwer, Dordrecht, pp 69–78Google Scholar
  48. Miljković D (2012) Developmental stability of Iris pumila flower traits: a common garden experiment. Arch Biol Sci 64:123–133CrossRefGoogle Scholar
  49. Mittler R (2006) Abiotic stress, the field environment and stress combination. Trends Plant Sci 11:15–19CrossRefGoogle Scholar
  50. Møller AP (1998) Developmental instability of plants and radiation from Chernobyl. Oikos 81:444–448CrossRefGoogle Scholar
  51. Møller AP, Swaddle JP (1997) Asymmetry, developmental stability and evolution. Oxford University Press, OxfordGoogle Scholar
  52. Palmer AR (1994) Fluctuating asymmetry analyses: a primer. In: Markow TA (ed) Developmental stability: Its Origins and Evolutionary Implications. Kluwer, Dordrecht, pp 335–364Google Scholar
  53. Palmer AR (1996) Waltzing with asymmetry. Bioscience 46:518–532CrossRefGoogle Scholar
  54. Palmer AR (1999) Detecting publication bias in meta-analyses: a case study of fluctuating asymmetry and sexual selection. Am Nat 154:220–233CrossRefGoogle Scholar
  55. Palmer AR, Strobeck C (1986) Fluctuating asymmetry: measurement, analysis, patterns. System 17:391–421Google Scholar
  56. Palmer AR, Strobeck C (1992) Fluctuating asymmetry as a measure of developmental stability: implications of non-normal distributions and power of statistical tests. Acta Zool Fenn 191:57–72Google Scholar
  57. Palmer AR, Strobeck C (2003a) Fluctuating asymmetry analysis revisited. In: Polak M (ed) Developmental instability: causes and consequences. Oxford University Press, New York, pp 279–319Google Scholar
  58. Palmer AR, Strobeck C (2003b) Fluctuating asymmetry analysis: a step-by-step example. From: Electronic Appendix V. In: Polak M (ed) Developmental instability: causes and consequences. Oxford University Press, New York, pp 279–319Google Scholar
  59. Parsons PA (1990) Fluctuating asymmetry: an epigenetic measure of stress. Biol Rev 65:131–145CrossRefGoogle Scholar
  60. Parsons PA (1992) Fluctuating asymmetry: a biological monitor of environmental and genomic stress. Heredity 68:361–364CrossRefGoogle Scholar
  61. Parsons PA (2005) Environments and evolution: interactions between stress, resource inadequacy and energetic efficiency. Biol Rev 80:589–610CrossRefGoogle Scholar
  62. Pouyat RV, McDonell MJ, Pickett STA (1997) Litter decomposition and nitrogen mineralization in oak stands along an urban-rural land-use gradient. Urb Ecosyst 1:117–131CrossRefGoogle Scholar
  63. Raz S, Graham JH, Hel-Or H, Pavlicek T, Nevo E (2011) Developmental instability of vascular plants in contrasting microclimates at “Evolution Canyon”. Biol J Linn Soc 102:786–797CrossRefGoogle Scholar
  64. Roach B A (1965) Black locust (Robinia pseudoacacia L). In Fowells HA (ed), Silvics of forest trees of the United States. US Department of Agriculture, Agriculture Handbook 271, Washington, pp 642–648Google Scholar
  65. Rohlf FJ (2010) TpsDIG 2.16. http://life.bio.sunysb.edu/morph/soft-dataacq.html (Accessed 15 December 2013)
  66. Scheffé HA (1953) A method for judging all possible contrasts in the analysis of variance. Biometrika 40:87–104Google Scholar
  67. Sheets HD (2000) TMorphGen6. Department of Physics, Canisius College, Buffalo, NY URL http://www3.canisiuse.du/~sheets/morphsofthtml (Accessed 15 December 2013)
  68. Šilić Č (1990) Ornamental trees and shrubs. “Svjetlost” OOUR Institute for textbooks and teaching aids. Sarajevo—Institute for textbooks and teaching aids, BeogradGoogle Scholar
  69. Smith SA, Donoghue MJ (2008) Rates of molecular evolution are linked to life history in flowering plants. Science 322:86–89CrossRefGoogle Scholar
  70. Smith BH, Garn SM, Cole PE (1982) Problems of sampling and inference in the study of fluctuating dental asymmetry. Am J Phys Anthropol 58:281–289CrossRefGoogle Scholar
  71. Sokal RR, Rohlf FJ (1995) Biometry. Freeman, New YorkGoogle Scholar
  72. Statistical Analysis System Institute, Inc. (2010) The SAS System for Windows, release 9.3., Cary (NC): SAS InstituteGoogle Scholar
  73. Tarasjev A (1995) Relationship between phenotypic plasticity and developmental instability in Iris pumila L. Russ J Genet 31:409–1416Google Scholar
  74. Thornhill R, Møller AP, Gangestad SW (1999) The biological significance of fluctuating asymmetry and sexual selection: a reply to Palmer. Am Nat 154:234–241CrossRefGoogle Scholar
  75. Tracy M, Freeman DC, Duda JJ, Miglia KJ, Graham JH, Hough RA (2003) Developmental instability: an appropriate indicator of plant fitness components? In: Polak M (ed) Developmental instability: causes and consequences. Oxford University Press, New York, pp 517–560Google Scholar
  76. Tucić B, Miljković D (2010) Fluctuating asymmetry of floral organ traits in natural populations of Iris pumila from contrasting light habitats. Plant Species Biol 25:173–184CrossRefGoogle Scholar
  77. 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
  78. Van Dongen S (2006) Fluctuating asymmetry and developmental instability in evolutionary biology: past, present and future. J Evol Biol 19:1727–1743CrossRefGoogle Scholar
  79. Wuytack T, Wuyts K, Van Dongen S, Baeten L, Kardel F, Verheyen K, Samson R (2011) The effect of air pollution and other environmental stressors on leaf fluctuating asymmetry and specific leaf area of Salix alba L. Environ Pollut 159:2405–2411CrossRefGoogle Scholar
  80. Zeleznik JD, Skousen JG (1996) Land reclamation: survival of three tree species on old reclaimed surface mines in Ohio. J Environ Qual 25:1429–1435CrossRefGoogle Scholar
  81. Zvereva EL, Kozlov MV (2001) Effects of pollution induced habitat disturbance on the response of willows to simulated herbivory. J Ecol 89:21–30CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Nataša Barišić Klisarić
    • 1
  • Danijela Miljković
    • 1
  • Stevan Avramov
    • 1
  • Uroš Živković
    • 1
  • Aleksej Tarasjev
    • 1
  1. 1.Department of Evolutionary Biology, Institute for Biological Research “Siniša Stanković”University of BelgradeBelgradeSerbia

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