Skip to main content

Advertisement

SpringerLink
Log in

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

  • Research Article
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • 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 6:1–6

    Article  CAS  Google Scholar 

  • 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)

  • Aksoy A, Sahn U, Duman F (2000) Robinia pseudoacacia L. as a possible biomonitor of heavy metal pollution in Kayseri Turk. J Bot 2:279–284

    Google Scholar 

  • 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 162:67–616

    Article  Google Scholar 

  • Allenbach DM (2010) Fluctuating asymmetry and exogenous stress in fishes: a review. Rev Fish Biol Fish 21:355–376

    Article  Google Scholar 

  • Ambo-Rappe R, Lajus DL, Schreider MJ (2011) Heavy metal impact on growth and leaf asymmetry of seagrass, Halophila ovalis. J Chem Ecotoxicol 3:149–159

    CAS  Google Scholar 

  • Auty RM (1997) Pollution patterns during the industrial transition. 77th. Geogr J 163:206–215

    Article  Google Scholar 

  • 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 278–283

    Google Scholar 

  • 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 30:218–226

    Article  Google Scholar 

  • 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 Jersey

    Google Scholar 

  • 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 3–20

    Google Scholar 

  • 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 189:281–293

    Article  Google Scholar 

  • Clarke GM (1993) Fluctuating asymmetry of invertebrate populations as a biological indicator of environmental quality. Environ Pollut 82:207–211

    Article  CAS  Google Scholar 

  • Clarke GM (1995) Relationships between developmental stability and fitness—application for conservation biology. Conserv Biol 9:18–24

    Article  Google Scholar 

  • Cottingham KL, Carpenter SR (1998) Population, community, and ecosystem variates as ecological indicators: phytoplankton responses to whole-lake enrichment. Ecol Appl 8:508–530

    Article  Google Scholar 

  • 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 24:557–561

    Article  Google Scholar 

  • Day RW, Quinn P (1989) Comparisons of treatments after analysis of variance in ecology. Ecol Monogr 59:433–463

    Article  Google Scholar 

  • DeGomez T, Wagner MR (2001) Culture and use of black locust. HortTechnology 11:279–288

    Google Scholar 

  • Dimitriou I, Aronsson P, Weih M (2006) Stress tolerance of five willow clones after irrigation with different amounts of landfill leachate. Bioresour Technol 97:150–157

    Article  CAS  Google Scholar 

  • Forbes VE, Palmqvist A, Bach L (2006) The use and misuse of biomarkers in ecotoxicology. Environ Toxicol Chem 25:272–280

    Article  CAS  Google Scholar 

  • Freeman DC, Graham JH, Emlen JM (1993) Developmental stability in plants: symmetries, stress and epigenesis. Genetica 89:97–119

    Article  Google Scholar 

  • 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 160:157–166

    Article  Google Scholar 

  • 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 367–386

    Google Scholar 

  • 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 165:805–816

    Article  Google Scholar 

  • 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 5:85–95

    Article  Google Scholar 

  • 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 23:130–139

    Article  CAS  Google Scholar 

  • 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 136–158

    Chapter  Google Scholar 

  • Graham JH, Raz S, Hel-Or SH, Nevo E (2010) Fluctuating asymmetry: methods, theory, and applications. Asymmetry 2:466–540

    Article  Google Scholar 

  • 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 20:143–150

    Article  Google Scholar 

  • Gurevitch J, Hedges LV (1999) Statistical issues in ecological meta-analyses. Ecology 80:1142–1149

    Article  Google Scholar 

  • 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 DC

    Google Scholar 

  • Hoffman AA, Parsons PA (1997) Extreme environmental change and evolution. Cambridge University Press, UK

    Google Scholar 

  • Hoffmann AA, Sgrò CM (2011) Climate change and evolutionary adaptation. Nature 470:479–485

    Article  CAS  Google Scholar 

  • 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 38:1326–1339

    Article  Google Scholar 

  • Jackson LE, Kurtz JC, Fisher WS (2000) Evaluation guidelines for ecological indicators. Environmental Protection Agency, Washington, Report No EPA/620/ R–99/005

    Google Scholar 

  • Karvonen E, Merila J, Van Dongen S (2003) Geography of fluctuating asymmetry in the Greenfinch (Carduelis chloris). Oikos 100:507–516

    Article  Google Scholar 

  • Komac B, Alados CL (2012) Fluctuating asymmetry and Echinospartum horridum fitness components. Ecol Indic 18:252–258

    Article  Google Scholar 

  • 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 64:145–158

    Article  Google Scholar 

  • 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 116:365–370

    Article  CAS  Google Scholar 

  • Kozlov MV, Wisley BJ, Koricheva J, Haukioja E (1996) Fluctuating asymmetry of birch leaves increases under pollution impact. J Appl Ecol 33:1489–1495

    Article  Google Scholar 

  • 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):e84190

    Article  Google Scholar 

  • 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 77:27–38

    Article  Google Scholar 

  • 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 415–426

    Google Scholar 

  • 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 24:1–11

    Article  Google Scholar 

  • Mal TK, Uveges JL, Turk KW (2002) Fluctuating asymmetry as an ecological indicator of heavy metal stress in Lythrum salicaria. Ecol Indic 1:189–195

    Article  CAS  Google Scholar 

  • Markow TA (1995) Evolutionary ecology and developmental instability. Annu Rev Entomol 40:105–120

    Article  CAS  Google Scholar 

  • 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 69–78

    Google Scholar 

  • Miljković D (2012) Developmental stability of Iris pumila flower traits: a common garden experiment. Arch Biol Sci 64:123–133

    Article  Google Scholar 

  • Mittler R (2006) Abiotic stress, the field environment and stress combination. Trends Plant Sci 11:15–19

    Article  CAS  Google Scholar 

  • Møller AP (1998) Developmental instability of plants and radiation from Chernobyl. Oikos 81:444–448

    Article  Google Scholar 

  • Møller AP, Swaddle JP (1997) Asymmetry, developmental stability and evolution. Oxford University Press, Oxford

    Google Scholar 

  • Palmer AR (1994) Fluctuating asymmetry analyses: a primer. In: Markow TA (ed) Developmental stability: Its Origins and Evolutionary Implications. Kluwer, Dordrecht, pp 335–364

    Google Scholar 

  • Palmer AR (1996) Waltzing with asymmetry. Bioscience 46:518–532

    Article  Google Scholar 

  • Palmer AR (1999) Detecting publication bias in meta-analyses: a case study of fluctuating asymmetry and sexual selection. Am Nat 154:220–233

    Article  Google Scholar 

  • Palmer AR, Strobeck C (1986) Fluctuating asymmetry: measurement, analysis, patterns. System 17:391–421

    Google Scholar 

  • 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 191:57–72

    Google Scholar 

  • Palmer AR, Strobeck C (2003a) Fluctuating asymmetry analysis revisited. In: Polak M (ed) Developmental instability: causes and consequences. Oxford University Press, New York, pp 279–319

    Google Scholar 

  • 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 279–319

    Google Scholar 

  • Parsons PA (1990) Fluctuating asymmetry: an epigenetic measure of stress. Biol Rev 65:131–145

    Article  CAS  Google Scholar 

  • Parsons PA (1992) Fluctuating asymmetry: a biological monitor of environmental and genomic stress. Heredity 68:361–364

    Article  Google Scholar 

  • Parsons PA (2005) Environments and evolution: interactions between stress, resource inadequacy and energetic efficiency. Biol Rev 80:589–610

    Article  Google Scholar 

  • Pouyat RV, McDonell MJ, Pickett STA (1997) Litter decomposition and nitrogen mineralization in oak stands along an urban-rural land-use gradient. Urb Ecosyst 1:117–131

    Article  Google Scholar 

  • 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 102:786–797

    Article  Google Scholar 

  • 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 642–648

  • Rohlf FJ (2010) TpsDIG 2.16. http://life.bio.sunysb.edu/morph/soft-dataacq.html (Accessed 15 December 2013)

  • Scheffé HA (1953) A method for judging all possible contrasts in the analysis of variance. Biometrika 40:87–104

    Google Scholar 

  • Sheets HD (2000) TMorphGen6. Department of Physics, Canisius College, Buffalo, NY URL http://www3.canisiuse.du/~sheets/morphsofthtml (Accessed 15 December 2013)

  • Šilić Č (1990) Ornamental trees and shrubs. “Svjetlost” OOUR Institute for textbooks and teaching aids. Sarajevo—Institute for textbooks and teaching aids, Beograd

    Google Scholar 

  • Smith SA, Donoghue MJ (2008) Rates of molecular evolution are linked to life history in flowering plants. Science 322:86–89

    Article  CAS  Google Scholar 

  • Smith BH, Garn SM, Cole PE (1982) Problems of sampling and inference in the study of fluctuating dental asymmetry. Am J Phys Anthropol 58:281–289

    Article  CAS  Google Scholar 

  • Sokal RR, Rohlf FJ (1995) Biometry. Freeman, New York

    Google Scholar 

  • Statistical Analysis System Institute, Inc. (2010) The SAS System for Windows, release 9.3., Cary (NC): SAS Institute

  • Tarasjev A (1995) Relationship between phenotypic plasticity and developmental instability in Iris pumila L. Russ J Genet 31:409–1416

    Google Scholar 

  • Thornhill R, Møller AP, Gangestad SW (1999) The biological significance of fluctuating asymmetry and sexual selection: a reply to Palmer. Am Nat 154:234–241

    Article  Google Scholar 

  • 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 517–560

    Google Scholar 

  • Tucić B, Miljković D (2010) Fluctuating asymmetry of floral organ traits in natural populations of Iris pumila from contrasting light habitats. Plant Species Biol 25:173–184

    Article  Google Scholar 

  • Valkama J, Kozlov MV (2001) Impact of climatic factors on the developmental stability of Mountain birch growing in a contaminated area. J Appl Ecol 38:665–673

    Article  Google Scholar 

  • Van Dongen S (2006) Fluctuating asymmetry and developmental instability in evolutionary biology: past, present and future. J Evol Biol 19:1727–1743

    Article  CAS  Google Scholar 

  • 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 159:2405–2411

    Article  CAS  Google Scholar 

  • Zeleznik JD, Skousen JG (1996) Land reclamation: survival of three tree species on old reclaimed surface mines in Ohio. J Environ Qual 25:1429–1435

    Article  CAS  Google Scholar 

  • Zvereva EL, Kozlov MV (2001) Effects of pollution induced habitat disturbance on the response of willows to simulated herbivory. J Ecol 89:21–30

    Article  Google Scholar 

Download references

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.

Author information

Authors and Affiliations

  1. Department of Evolutionary Biology, Institute for Biological Research “Siniša Stanković”, University of Belgrade, Despota Stefana Blvd. 142, 11000, Belgrade, Serbia

    Nataša Barišić Klisarić, Danijela Miljković, Stevan Avramov, Uroš Živković & Aleksej Tarasjev

Authors
  1. Nataša Barišić Klisarić
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Danijela Miljković
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Stevan Avramov
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Uroš Živković
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Aleksej Tarasjev
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Nataša Barišić Klisarić.

Additional information

Responsible editor: Elena Maestri

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Klisarić, N.B., Miljković, D., Avramov, S. et al. Fluctuating asymmetry in Robinia pseudoacacia leaves—possible in situ biomarker?. Environ Sci Pollut Res 21, 12928–12940 (2014). https://doi.org/10.1007/s11356-014-3211-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-014-3211-2

Keywords

Search

Navigation