• Nataša Barišić Klisarić Institute for Biological Research “Siniša Stanković”, University of Belgrade, Belgrade
  • Danijela Miljković Institute for Biological Research “Siniša Stanković”, University of Belgrade, Belgrade
  • Stevan Avramov Institute for Biological Research “Siniša Stanković”, University of Belgrade, Belgrade
  • Uroš Živković Institute for Biological Research “Siniša Stanković”, University of Belgrade, Belgrade
  • Aleksej Tarasjev Institute for Biological Research “Siniša Stanković”, University of Belgrade, Belgrade


In light of the increasing need for appropriate, cost-effective detection methods of anthropogenic pollution, we evaluated the biomonitoring potential of flower developmental instability (DI) on a widely planted decorative species, Iris germanica, under in situ conditions. DI was measured by fluctuating and radial asymmetries of parts of Iris germanica perianth (810 fall lengths and widths), from clones already growing in two distinct types of habitats with contrasting levels of anthropogenic pollution: in unpolluted (rural) areas, Novi Banovci, Stari Banovci and Belegiš (flowers from 137 clones sampled), and in a polluted (urban) Belgrade metropolitan area (flowers from 133 clones sampled). Our results revealed significantly higher flower radial asymmetry in the polluted habitats compared to unpolluted ones (for three out of four univariate indices, as well as both multivariate ones), but failed to detect a similar effect on fluctuating asymmetry indices. The results of our study therefore demonstrate the potential of DI (when estimated by flower radial asymmetry) in Iris germanica as a cost-effective biomonitoring method for in situ pollution detection based on readily measurable flower parts and moderate sample sizes.

DOI: 10.2298/ABS151229072B

Key words: biomonitoring; Iris germanica; developmental instability; fluctuating asymmetry; radial asymmetry

Received: December 29, 2015; Revised: February 10, 2016; Accepted: February 22, 2016; Published online: August 12, 2016

How to cite this article: Barišić-Klisarić N, Miljković D, Avramov S, Živković U, Tarasjev A. Developmental instability in German Iris flower as a potential biomonitoring method. Arch Biol Sci. 2016;68(4):837-44.


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Auty RM. Pollution Patterns during the Industrial Transition. Geogr J; 1997;163:206-15.

Hoffmann AA, Sgrò CM. Climate change and evolutionary adaptation. Nature. 2011;470(7335):479-85.

Bargagli R. Trace Elements in Terrestrial Plants: An Ecophysiological Approach to Biomonitoring and Biorecovery. Berlin: Springer-Verlag; 1998. 324 p.

Oliva SR, Espinosa AJF. Monitoring of heavy metals in topsoils, atmospheric particles and plant leaves to identify possible contamination sources. Microchem J. 2007;86(1):131-9.

Hammond A, Adriaanse A, Rodenburg E, Bryant D, Woodward R. Environmental indicators: a systematic approach to measuring and reporting on environmental policy performance in the context of sustainable development. Washington: World Resources Institute; 1995. 43 p.

Graham JH, Duda JJ, Brown ML, Kitchen S, Emlen JM, Malol J, Bankstahl E, Krzysik AJ, Balbach H, Freeman DC. The effects of drought and disturbance on the growth and developmental instability of loblolly pine (Pinus taeda L.). Ecol Indic. 2012;20:143-50.

López DR, Brizuela MA, Willems P, Aguiar MR, Siffredi G, Bran D. Linking ecosystem resistance, resilience, and stability in steppes of North Patagonia. Ecol Indic. 2013;24:1-11.

Cairns JrJ. Biological Monitoring: Concept and Scope. In: Cairns J. J, Patil GP, Waters WE, editors. Environmental biomonitoring, assessment, prediction, and management issues. Fairland: International Cooperative Publishing House; 1979. p. 3-20.

Spellerberg IF. Monitoring Ecological Change. Cambridge: Cambridge University Press; 2005. 391 p.

Roff DA. Predicting Body Size with Life History Models. Bioscience. 1986;36(5):316-23.

Kozlov MV, Niemelä P. Difference in needle length − a new and objective indicator of pollution impact on Scots Pine (Pinus sylvestris). Water Air Soil Pollut. 1999;116(1-2):365-70.

Møller AP, Shykoff JA. Morphological developmental stability in plants: Patterns and causes. Int J Plant Sci. 1999;160(S6):S135-S146.

Clarke GM. The genetic basis of developmental stability. V. Inter- and intra-individual character variation. Heredity (Edinb). 1998;80(5):562-7.

Freeman DC, Graham JH, Emlen JM. Developmental stability in plants: Symmetries, stress and epigenesis. Genetica. 1993;89(1-3):97-119.

Graham JH, Raz S, Hel-Or H, Nevo E. Fluctuating Asymmetry: Methods, Theory, and Applications. Symmetry (Basel). 2010;2(2):466-540.

Møller AP, Swaddle JP. Asymmetry, Developmental Stability and Evolution. Oxford: Oxford University Press; 1997. 291 p.

Palmer AR, Strobeck C. Fluctuating asymmetry analysis revisited. In: Polak M, editor. Developmental instability: causes and consequences. New York: Oxford University Press; 2003a. 279-319.

Palmer AR, Strobeck C. Fluctuating asymmetry analysis: A step-by-step example. [Electronic Appendix V]. In: Polak M, editor. Developmental instability: causes and consequences. New York: Oxford University Press; 2003b. 279-319.

Watson PJ, Thornhill R. Fluctuating asymmetry and sexual selection. Trends Ecol Evol. 1994;9(1):21-5.

Krizek BA, Fletcher JC. Molecular mechanisms of flower development: an armchair guide. Nat Rev Genet. 2005;6(9):688-98.

Laitinen RAE, Pöllänen E, Teeri TH, Elomaa P, Kotilainen M. Transcriptional analysis of petal organogenesis in Gerbera hybrida. Planta. 2007;226(2):347-60.

Theissen G, Melzer R. Molecular mechanisms underlying origin and diversification of the angiosperm flower. Ann Bot. 2007;100(3):603-19.

Møller AP, Sorci G. Insect preference for symmetrical artificial flowers. Oecologia. 1998;114(1):37-42.

Galen C. Measuring pollinator-mediated selection on morphometric floral traits: bumblebees and the Alpine sky pilot, Polemonium viscosum. Evol. 1989;43:882-90.

Galen C. Why Do Flowers Vary? Bioscience. 1999;49(8):631-40.

Møller AP, Eriksson M. Patterns of fluctuating asymmetry in flowers: Implications for sexual selection in plants. J Evol Biol. 1994;7(1):97-113.

Møller AP, Eriksson M. Pollinator preference for symmetrical flowers and sexual selection in plants. Oikos. 1995;73(1):15-22.

Conner JK. Floral evolution in wild radish: the roles of pollinators, natural selection, and genetic correlations among traits. Int J plant Sci. 1997;158:108-20.

Møller AP. Developmental stability and pollination. Oecologia. 2000;123(2):149-57.

Damerval C, Nadot S. Evolution of perianth and stamen characteristics with respect to floral symmetry in Ranunculales. Ann Bot. 2007;100(3):631-40.

Whitlock M. The heritability of fluctuating asymmetry and the genetic control of developmental stability. Proc Biol Sci. 1996;263(1372):849-53.

Whitlock M. The repeatability of fluctuating asymmetry: a revision and extension. Proc R Soc B Biol Sci. 1998;265(1404):1429-31.

Dongen S V. How repeatable is the estimation of developmental stability by fluctuating asymmetry? Proc R Soc B Biol Sci. 1998;265(1404):1423-7.

Andalo C, Bazin A, Shykoff JA. Is there a genetic basis for fluctuating asymmetry and does it predict fitness in the plant Lotus corniculatus grown in different environmental conditions? Int J Plant Sci. The 2000;161(2):213-20.

Alados CL, Giner ML, Dehesa L, Escos J, Barroso FG, Emlen JM, Freeman DC. Developmental instability and fitness in Periploca laevigata experiencing grazing disturbance. Int J Plant Sci. 2002;163(6):969-78.

Sherry RA, Lord EM. Developmental stability in flowers of Clarkia tembloriensis (Onagraceae). J Evol Biol. 1996;9(6):911-30.

Roy BA, Stanton ML. Asymmetry of wild mustard, Sinapis arvensis (Brassicaceae), in response to severe physiological stresses. J Evol Biol. 1999;12:440-9.

Rao G-Y, Andersson S, Widén B. Flower and cotyledon asymmetry in Brassica cretica: genetic variation and relationships with fitness. Evolution. 2002;56(4):690-8.

Møller AP. Bumblebee preference for symmetrical flowers. Proc Natl Acad Sci. 1995;92(6):2288-92.

Stebbins GL. Natural selection and differentiation of angiosperm families. Evolution. 1951; 5:299-324.

Bradshaw AD. Evolutionary significance of phenotypic plasticity in plants. Adv Genet. 1965;31:115-55.

Bell G. On the function of flowers. Proc R Soc B Biol Sci. 1985;224(1235):223-65.

Makarevitch I, Golovnina K, Scherbik S, Blinov A. Phylogenetic relationships of the Siberian Iris species inferred from noncoding chloroplast DNA sequences. Int J Plant Sci. 2003;164:229-37.

Mitra J. Karyotype analysis of bearded Iris. Bot Gaz. 1956;4:265-93.

Yu X-F, Zhang H-Q, Yuan M, Zhou Y-H. Karyotype studies on ten Iris species (Iridaceae) from Sichuan, China. Caryologia. 2009;62(3):253-60.

Henderson NC. What is Iris germanica? Bull Amer Iris Soc. 1992;286: 6–11.

Ingersoll HM. The Lilies of France. Monthly Illustrator. 1895;4(12):49-53.

Waddick JW, Zhao YT. Iris of China. Portland: Timber Press; 1992. 192 p.

Jéhan H, Courtois D, Ehret C, Lerch K, Pétiard V. Plant regeneration of Iris pallida Lam. and Iris germanica L. via somatic embryogenesis from leaves, apices and young flowers. Plant Cell Rep. 1994;13(12):671-5.

Wang Y, Jeknic Z, Ernst RC, Chen THH. Improved plant regeneration from suspension-cultured cells of Iris germanica L. ‘Skating Party’. HortScience. 1999;34(7):1271-6.

Neal PR, Dafni A, Giurfa M. Floral symmetry and its role in plant-pollinator systems: terminology, distribution, and hypotheses. Annu Rev Ecol Syst. 1998;29:345-73.

Kalisz S, Ree RH, Sargent RD. Linking floral symmetry genes to breeding system evolution. Trends Plant Sci. 2006;11(12):568-73.

Sawidis T, Breuste J, Mitrovic M, Pavlovic P, Tsigaridas K. Trees as bioindicator of heavy metal pollution in three European cities. Environ Pollut. 2011;159(12):3560-70.

Environmental Protection Agency. Annual report on the state of air quality in the Republic of Serbia in 2014. Belgrade: Ministry of Agriculture and Environmental protection of the Republic of Serbia; 2014.

Environmental Protection Agency. The report on the state of land in the Republic of Serbia for 2013. Ministry of Agriculture and Environmental protection of the Republic of Serbia; 2013.

Unkašević M. Klima Beograda. Beograd: Naučna knjiga; 1994. 122 p.

Palmer AR. Fluctuating asymmetry analyses: a primer. In: Markow TA, editor. Developmental stability, Its Origins and Evolutionary Implications. Dordrecht: Kluwer; 1994. p. 335-64.

Palmer AR, Strobeck C. Fluctuating asymmetry: measurement, analysis, patterns. Annu Rev Ecol Syst Ann Rev. 1986;17(1):391-421.

Palmer AR, Strobeck C. Fluctuating asymmetry as a measure of developmental stability, Implications of non-normal distributions and power of statistical tests. ActaZoolFenn. 1992;191:57-72.

Sokal RR, Rohlf FJ. Biometry. New York: Freeman; 1995.

Scheffe H. A method for judging all contrasts in the analysis of variance. Biometrika. 1953;40(1/2):87-104.

Day RW, Quinn GP. Comparisons of treatments after an analysis of variance in ecology. Ecol Monogr. 1989;59:433-63.

Clarke GM. Relationships between developmental stability and fitness: Application for conservation biology. Conserv Biol. 1995;9(1):18-24.

Alados CL, Navarro T, Escos J, Cabezudo B, Emlen JM. Translational and fluctuating asymmetry as tools to detect stress in stress adapted and nonadapted plants. Int J Plant Sci. 2001;162(3):607-16.

Beasley DAE, Bonisoli-Alquati A, Mousseau TA. The use of fluctuating asymmetry as a measure of environmentally induced developmental instability: A meta-analysis. Ecol Indic. 2013;30:218-26.

Barišić Klisarić N, Miljković D, Avramov S, Zivković U, Tarasjev A. Fluctuating asymmetry in Robinia pseudoacacia leaves − possible in situ biomarker? Environ Sci Pollut Res Int. 2014;21(22):12928-40.

Alados CL, Navarro T, Cabezudo B. Tolerance assessment of Cistus ladanifer to serpentine soils by developmental stability analysis. Plant Ecol. 1999;143(1):51-66.

Barišić Klisarić N. Fluctuating asymmetry as an indicator of developmental stability of selected plant taxa in unpolluted environment and under anthropogenically induced stress. [dissertation]. [Belgrade]: Faculty of Biology, University of Belgrade. 2012. 213p.

Miljković D. Developmental stability of Iris pumila flower traits: A common garden experiment. Arch Biol Sci. 2012;64(1):123-33.

Tucić B, Miljković D. Fluctuating asymmetry of floral organ traits in natural populations of Iris pumila from contrasting light habitats. Plant Species Biol. 2010;25(3):173-84.

Fowler K, Whitlock MC. Fluctuating asymmetry does not increase with moderate inbreeding in Drosophila melanogaster. Heredity (Edinb). 1994;73(4):373-6.

Zhang SW, Srinivasan M V, Horridge GA. Pattern recognition in honeybees: local and global analysis. Proc R Soc B Biol Sci. 1992;248(1321):55-61.

Giurfa M, Dafni A, Neal P. Floral symmetry and its role in plant-pollinator systems. Int J Plant Sci. 1999;160(S6):S41-S50.

Davenport D, Kohanzadeh Y. Orchids, bilateral symmetry and insect perception. J Theor Biol. 1982;94:241-52.

McKenzie JA, O’Farrell K. Modification of developmental instability and fitness: Malathion-resistance in the Australian sheep blowfly, Lucilia cuprina. Genetica. 1993;89(1-3):67-76.

Emlen JM, Freeman DC, Graham JH. Nonlinear growth dynamics and the origin of fluctuating asymmetry. Genetica. 1993;89(1-3):77-96.




How to Cite

Barišić Klisarić N, Miljković D, Avramov S, Živković U, Tarasjev A. DEVELOPMENTAL INSTABILITY IN GERMAN IRIS FLOWER AS A POTENTIAL BIOMONITORING METHOD. Arch Biol Sci [Internet]. 2016Nov.25 [cited 2023Jun.10];68(4):837-44. Available from: