SMALL-SCALE VARIATIONS IN LEAF SHAPE UNDER ANTHROPOGENIC DISTURBANCE IN DIOECIOUS FOREST FORB MERCURIALIS PERENNIS: A GEOMETRIC MORPHOMETRIC EXAMINATION
Keywords:leaf morphology, geometric morphometrics, anthropogenic stress, trampling, sexual dimorphism
Plants are exposed to increasing levels of diverse human activities that have profound effects on their overall morphology and, specifically, on leaf morphology. Anthropogenic disturbances in urban and suburban forest recreational sites are attracting growing research interest. To explore the persisting recreational impact on leaf shape and size, we conducted a field study on the dioecious forb Mercurialis perennis L. (Euphorbiaceae), typical for undisturbed understory communities. We selected adjacent sites in a suburban forest, which experience contrasting regimes of disturbance by human trampling under otherwise concordant natural conditions. Patterns of leaf shape and size variation and putative sex-specific response to disturbance were analyzed using a geometric morphometric approach. In addition to leaf-level data, plant height, internode and leaf number were analyzed to explore the same response at the whole-plant level. The results show significant variations associated with disturbance at both levels: plants growing under a heavy disturbance regime had shorter stems with a greater number of wider and shorter leaves. Significant differences between sites were also found for leaf size, with larger leaves observed in an undisturbed site. The effects of sex and sex x site interaction on leaf size and shape were nonsignificant, pointing to the absence of sexual dimorphism and sex-specific response to disturbance. Contrary to leaf shape and size, all three analyzed shoot traits showed highly significant sexual dimorphism, with male plants being higher and having higher leaf and internode count.
Received: November 11, 2015; Revised: December 16, 2015; Accepted: December 16, 2015; Published online: January 21, 2016
How to cite this article: Vujić V, Rubinjoni L, Selaković S, Cvetković D. Small-scale variations in leaf shape under anthropogenic disturbance in dioecious forest forb mercurialis perennis: A geometric morphometric examination. Arch Biol Sci. 2016;68(4):705:13.
Honour SL, Bell JNB, Ashenden TW, Cape JN, Power SA. Responses of herbaceous plants to urban air pollution: effects on growth, phenology and leaf surface characteristics. Environ Pollut. 2009;157:1279-86.
Vujić V, Avramov S, Tarasjev A, Barišić Klisarić N, Živković U, Miljković D. The effects of traffic-related air pollution on the flower morphology of Iris pumila -comparison of a polluted city area and the unpolluted Deliblato Sands (nature reserve). Appl Ecol Env. 2015;13:405-15.
Guirado M, Pino J, Rodà F. Understorey plant species richness and composition in metropolitan forest archipelagos: effects of forest size, adjacent land use and distance to the edge. Global Ecol Biogeogr. 2006;15:50e62.
Kutiel P, Zhevelev Y. Recreational use impact on soil and vegetation at picnic sites in Aleppo pine forests on Mount Carmel, Israel. Isr J Plant Sci. 2001;49:49-56.
Amrein D, Rusterholz HP, Baur B. Disturbance of suburban Fagus forests by recreational activities: effects on soil characteristics, above-ground vegetation and seed bank. Appl Veg Sci. 2005;8:175-82.
Bernhardt-Römermann M, Gray A, Vanbergen AJ, Berges L, Bohner A, Brooker RW, De Bruyn L, De Cinti B, Dirnböck T, Grandin U, Hester AJ, Kanka R, Klotz S, Loucougaray G, Lundin L, Matteucci G, Mészáros I, Oláh V, Preda E, Prévosto B, Pykälä J, Schmidt W, Taylor ME, Vadineanu A, Waldmann T, Stadler J. Functional traits and local environment predict vegetation responses to disturbance: a pan-European multi-site experiment. J Ecol. 2011;99:777-87.
Pescott OL, Stewart GB. Assessing the impact of human trampling on vegetation: a systematic review and metaanalysis of experimental evidence. PeerJ. 2014;2:e360. DOI:10.7717/peerj.360.
Kissling M, Hegetschweiler KT, Rusterholz HP, Baur B. Short-term and long-term effects of human trampling on above-ground vegetation, soil density, soil organic matter and soil microbial processes in suburban beech forests. Appl Soil Ecol. 2009;42:303-14.
Hamberg L, Malmivaara-Lämsä M, Lehvävirta S, O’Hara RB, Kotze DJ. Quantifying the effects of trampling and habitat edges on forest understory vegetation - a field experiment. J Environ Manage. 2010;91:1811-20.
Malmivaara-Lämsä M, Hamberg L, Löfström I, Vanha- Majamaa I, Niemelä J. Trampling tolerance of understorey vegetation in different hemiboreal urban forest site types in Finland. Urban Ecosyst. 2008;11:1-16.
Rusterholz HP, Kissling M, Baur B. Disturbances by human trampling alter the performance, sexual reproduction and genetic diversity in a clonal woodland herb. Perspect Plant Ecol. 2009;11:17-29.
Oral D, Ozcan M, Gökbulak F, Efe A, Hizal A. Response of understory vegetation to exclosure in a heavily compacted forest recreational site. J Environ Biol. 2013;34:811-7.
Yorks TJ, West NE, Mueller RJ, Warren SD. Toleration of traffic by vegetation: life form conclusions and summary extracts from a comprehensive data base. Environ Manage. 1997;21:121-31.
Hill R, Pickering C. Differences in resistance of three subtropical vegetation types to experimental trampling. J Environ Manage. 2009;90:1305-12.
Liddle MJ. Recreation Ecology. London, UK: Chapman & Hall;1997.
Cole DN. Impacts of hiking and camping on soils and vegetation: a review. In: Buckley R, editor. Environmental Impacts of Ecotourism. Wallingford, UK: CABI Publishing; 2004. p. 41-60.
Klingenberg CP. Evolution and development of shape: integrating quantitative approaches. Nat Rev Genet. 2010;11:623-35.
Viscosi V, Cardini A. Leaf Morphology, Taxonomy and Geometric Morphometrics: A Simplified Protocol for Beginners. PloS One. 2011;6:e25630.
Klingenberg CP, Barluenga M, Meyer A. Shape analysis of symmetric structures: quantifying variation among individuals and asymmetry. Evolution. 2002;56:1909-20.
Jojić V, Nenadović J, Blagojević J, Paunović M, Cvetković D, Vujošević M. Phenetic relationships among four Apodemus species (Rodentia, Muridae) inferred from skull variation. Zool Anz. 2012;251:26-37.
Viscosi V, Fortini P, Slice DE, Loy A, Blasi C. Geometric morphometric analyzes of leaf variation in four oak species of the subgenus Quercus (Fagaceae). Plant Biosyst. 2009;143:575-87.
Klingenberg CP, Duttke S, Whelan S, Kim M. Developmental plasticity, morphological variation and evolvability: a multilevel analysis of morphometric integration in the shape of compound leaves. J Evol Biol. 2012;25:115-29.
Jefferson GR. Biological Flora of the British Isles: Mercurialis perennis L. J Ecol. 2008;96:386-412.
Wade KM. Experimental studies on the distribution of the sexes of Mercurialis perennis L. III. Transplanted populations under light screens. New Phytol. 1981;87:447-55.
Cvetković D, Jovanović V. Altitudinal variation of the sex ratio and segregation by gender in the dioecious plant Mercurialis perennis L. (Euphorbiaceae) in Serbia. Arch Biol Sci. 2007;59:193-8.
Vandepitte K, Honnay O, De Meyer T, Jacquemyn H, Roldán-Ruiz I. Patterns of sex ratio variation and genetic diversity in the dioecious forest perennial Mercurialis perennis. Plant Ecol. 2010;206:105-14.
Vandepitte K, Roldán-Ruiz I, Leus L, Jacquemyn H, Honnay O. Canopy closure shapes clonal diversity and fine-scale genetic structure in the dioecious understorey perennial Mercurialis perennis. J Ecol. 2009;97:404-14.
Sánchez-Vilas J, Pannell JR. Differential niche modification by males and females of a dioecious herb: extending the Jack Sprat effect. J Evol Biol. 2010;23:2262-6.
Barrett SC, Hough J. Sexual dimorphism in flowering plants. J ExpBot. 2013;64:67-82.
Cornelissen T, Stiling P. Sex-biased herbivory: a meta-analysis of the effects of gender on plant-herbivore interactions. Oikos. 2005;111:488-500.
Glišić M, Lakušić D, Šinžar-Sekulić J, Jovanović S. GIS analysis of spatial distribution of invasive tree species in the protected natural area of Mt. Avala (Serbia). Bot Serb. 2014;38:131-8.
Jovović N, editor. Predeo izuzetnih odlika „Avala“ - predlog za zaštitu. (Landscape of exceptional characteristics “Avala” - a proposal for protection). Belgrade, Serbia: Institute for nature conservation of Serbia; 2004. p. 14-6.
Sheets HD. IMP - Integrated Morphometrics Package. Buffalo, USA: Department of Physics, Canisius College; 2003. Available: http://www3.canisius.edu/~sheets/morphsoft.html
Zelditch ML, Swiderski DL, Sheets HD, Fink WL. Geometric morphometrics for biologists: a primer. New York, USA: Elsevier; 2004.
Rohlf FJ. TpsDig, Version 2.12. Department of Ecology and Evolution. New York, USA: SUNY at Stony Brook; 2008. Available: http://life.bio.sunysb.edu/morph/
Klingenberg CP. MORPHOJ: an integrated software package for geometric morphometrics. Mol Ecol Resour. 2011;11:353-7.
Dryden IL, Mardia KV. Statistical Shape Analysis. New York, USA: John Wiley and Sons; 1998.
Rohlf FJ. Shape statistics: Procrustes superimpositions and tangent spaces. J Class. 1999;16:197-223.
Monteiro LR. Multivariate regression models and geometric morphometrics: the search for causal factors in the analysis of shape. Syst Biol. 1999;48:192-9.
Good P. Permutation tests: a practical guide to resampling methods for testing hypotheses. New York, USA: Springer; 2000.
R Core Team. “R: a language and environment for statistical computing.” Vienna, Austria: R Foundation for Statistical Computing; 2013. Available: http://www.R-project.org
Sun D, Liddle MJ. Plant morphological characteristics and resistance to simulated trampling. Environ Manage. 1993;17:511-21.
Meerts P, Vekemans R. Phenotypic plasticity as related to trampling within a natural population of Polygonum aviculare subsp. aequale. Acta Oecol. 1991;12:203-12.
Sunohara Y, Ikeda H. Effects of trampling and ethephon on leaf morphology in trampling-tolerant Plantago asiatica and Eleusine indica. Weed Res. 2003;43:155-62.
Grabherr G. Damage to vegetation by recreation in the Austrian and German Alps. In: Bayfield N, Barrow GC, editors. The Ecological Impact of Outdoor Recreation on Mountain Areas in Europe and North America. Ashford, UK: Wye College; 1985. p. 74-91.
Kobayashi T, Ikeda H, Hori Y. Growth analysis and reproductive allocation of Japanese forbs and grasses in relation to organ toughness under trampling. Plant Biol. 1999;1:445-52.
Roovers P, Verheyen K, Hermy M, Gulinck H. Experimental trampling and vegetation recovery in some forest and heathland communities. Appl Veg Sci. 2004;7:111-8.
Braam J. In touch: plant responses to mechanical stimuli. New Phytol. 2005;165:373-89.
Potters G, Pasternak TP, Guisez Y, Palme KJ, Jansen MAK. Stress-induced morphogenic responses: growing out of trouble? Trends Plant Sci. 2007;12:98-105.
Sunohara Y, Ikeda H, Tsukagoshi S, Murata Y, Sakurai N, Noma Y. Effects of trampling on morphology and ethylene production in Asiatic plantain. Weed Sci. 2002; 50:479-84.
Scott SL, Aarssen LW. Within-species leaf size-number tradeoffs in herbaceous angiosperms. Botany. 2012;90:223-35.
Lloyd GD, Webb CJ. Secondary sex characters in plants. Bot Rev. 1977;43:177-216.
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