Plant morpho-physiological variation under distinct environmental extremes in restinga vegetation

Scarano, Fabio Rubio; Barros, Cláudia Franca; Loh, Roberta Kuan Tchuen; Mattos, Eduardo Arcoverde de; Wendt, Tânia

doi:10.1590/2175-7860200960113

ABSTRACT

This paper is a synthesis of over ten years of research on inter- and intra-population variation in morphophysiology of six plant species at the Jacarepiá restinga: the shrubs Alchornea triplinervia, Andira legalis, Clusia fluminensis and Myrsine parvifolia, the bromeliad Aechmea maasii (formerly identified as Aechmea bromeliifolia, now recognized as a species only found in Central Brazil) and the geophyte palm Allagoptera arenaria. Individual shape, stature and growth, leaf anatomy, photoinhibition, and carbon, nitrogen and water use were the main parameters studied. The isolated study of intra-specific variation in one or a few of the above-mentioned traits often does not allow a distinction between acclimation and stress symptoms. Thus, we used an approach that integrated morphology, anatomy, physiology and also population parameters. Variation in morphological, anatomical and physiological traits was found for the majority of these species, and often indicated great acclimation capacity to distinct environmental extremes. This acclimation capacity may be partly responsible for the broad colonization success of extreme habitats in restingas, by species often originating in mesic forest environments. This phenomenon is an additional element to be accounted for as an important component of the high biodiversity of the Atlantic forest complex. Finally, we discuss implications for biodiversity conservation of intra-specific variation at the population level.

Key words:
acclimation; clonal growth; intraspecific variation; leaf anatomy; photoinhibition; restinga

RESUMO

Este trabalho é uma síntese das informações obtidas em mais de dez anos de pesquisas sobre variação morfofisiológica entre populações e dentre indivíduos de uma mesma população para seis espécies da restinga de Jacarepiá: os arbustos Alchornea triplinervia, Andira legalis, Clusia fluminensis e Myrsine parvifolia, a bromélia Aechmea maasii (anteriormente identificada como Aechmea bromeliifolia, que agora é como são denominadas plantas ocorrentes no Brasil central) e a palmeira geófita Allagoptera arenaria. Forma, porte e crescimento de indivíduos, anatomia foliar, fotoinibição da fotossíntese e uso de carbono, nitrogênio e água foram os principais parâmetros estudados. Com freqüência, a análise isolada da variação de um desses parâmetros não permite distinguir aclimatação de sintoma de injúria. Logo, os estudos aqui revisados apresentam uma abordagem que integra os diferentes parâmetros auto-ecológicos mencionados, assim como estes a parâmetros populacionais. Variação em caracteres morfológicos, anatômicos e fisiológicos foi detectada para a maioria destas espécies e, em geral, apontou para uma grande capacidade de aclimatação das mesmas a distintas circunstâncias ambientais. Tal capacidade de ajuste deve ter sido essencial para que várias destas espécies, na maioria oriundas de ambientes florestais, pudessem vir a colonizar um ambiente extremo como as restingas. Esta mesma capacidade é um elemento a mais a ser contabilizado como componente da grande biodiversidade existente no complexo vegetacional atlântico. Por fim, discutimos as implicações para conservação da biodiversidade da variação intra-específica encontrada ao nível populacional.

Palavras-chave:
aclimatação; anatomia foliar; crescimento clonal; fotoinibição; restinga; variação intra-específica

Full text available only in PDF format.

ACKNOWLEDGEMENTS

We thank D.S.D. Araujo and C.F.C. Sá for introducing us to this beautiful vegetation and for providing guidance and logistic support at the earlier steps of the series of studies reviewed here; G. Ganade for critical reading of an earlier version of the manuscript; Fundação O Boticário, PRONEX/ FINEP, PROBRAL (CAPES-DAAD), and Volkswagen Foundation for providing financial support to various studies reviewed here; CNPq, CAPES, FAPERJ, Fundação Botânica Margaret Mee and Petrobras for research grants; and in particular to all those who took part in field studies or in the papers published regarding Jacarepiá Reserve: E.F. Amado, S.M.B. Barreto, P. Cirne, H.M. Duarte, T. Fontoura, A.C. Franco, A. Geβler, H.R.P. Lima, L.S. López, U. Lüttge, A. Mantovani, D.C. Pereira, P. Peres-Neto, F. Reinert, H. Rennenberg, K.T. Ribeiro, G. Rôças, and H.L.T. Zaluar.

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Publication Dates

Publication in this collection
Jan-Mar 2009

History

Received
May 2008
Accepted
Feb 2009

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[1] Agosta, S. J. & Klemens, J. A. 2008. Ecological fitting by phenotypically flexible genotypes: implications for species associations, community assembly and evolution. Ecology Letters 11: 1123-1134.

[2] Araujo, D. S. D. 1997. Cabo Frio region, southeastern Brazil. In: Davis, S. D.; Heywood,V. H.; Herrera-Macbryde, O.; Villa-Lobos, J. & Hamilton, A. C. (eds.). Centres of plant diversity: a guide and strategy for their conservation 3. The Americas. WWF/IUCN, Washington. Pp. 373-375.

[3] Araujo, D. S. D. 2000. Análise florística e fitogeográfica das restingas do estado do Rio de Janeiro. D.Sc. Thesis. Universidade Federal do Rio de Janeiro, 169p.

[4] Araujo, D. S. D. & Peixoto, A. L. 1977. Renovação da comunidade vegetal de restinga após uma queimada. Trabalhos do XXVI Congresso Nacional de Botânica. Academia Brasileira de Ciências, Rio de Janeiro. Pp.1-17.

[5] Araujo, D. S. D.; Sá, C. F. C.; Fontella-Pereira, J.; Garcia, D. S.; Ferreira, M. V.; Paixão, R. J.; Schneider, S. M. & Fonseca-Kruel, V. S. 2009 Área de Proteção Ambiental de Massambaba, Rio de Janeiro: caracterização fitofisionômica e florística. Rodriguésia 60(1): 67-96.

[6] Barbará, T.; Martinelli, G.; Fay, M. F.; Mayo, S. J. & Lexer, C. 2007. Population differentiation and species cohesion in two closely related plants adapted to neotropical high-altitude "inselbergs", Alcantarea imperialis and Alcantarea geniculata (Bromeliaceae). Molecular Ecology 16: 1981-1992.

[7] Barros, C. F. 1998. Estudo da epiderme foliar de espécies tropicais. D.Sc. Thesis. Universidade Federal do Rio de Janeiro, 176p.

[8] Björkman, O. & Demmig, B. 1987. Photon yield of O2-evolution and chlorophyll fluorescence characteristics at 77K among vascular plants of diverse origins. Planta 170: 489-504.

[9] Broadmeadow, M. S. J.; Griffiths, H.; Maxwell, C. & Borland A. 1992. The carbon isotope ratio of plant organic material reflects temporal and spatial variations in CO2 within tropical forest formation in Trinidad. Oecologia 89: 435-441.

[10] Brooks, J. R.; Sprugel, D. G. & Hinckley, T. M. 1996. The effects of light acclimation during and after foliage expansion on photosynthesis of Abies amabilis foliage within the canopy. Oecologia 107: 21-32.

[11] Chazdon, R. L. & Kaufmann, S. 1993. Plasticity of leaf anatomy of two rain forest shrubs in relation to photosynthetic light acclimation. Functional Ecology 7: 385-394.

[12] Cirne, P. & Scarano, F. R. 2001. Resprouting and growth dynamics after fire of the clonal shrub Andira legalis (Leguminosae) in a sandy coastal plain in southeastern Brazil. Journal of Ecology 89: 351-357.

[13] Cirne, P.; Zaluar, H. L. T. & Scarano, F. R. 2003. Plant diversity, interspecific associations and postfire resprouting on a sandy spit in a Brazilian coastal plain. Ecotropica 9: 33-38.

[14] Crawford, R. M. M. 2008. Plants at the margin: ecological limits and climate change. Cambridge University Press, Cambridge, 478p.

[15] Demmig-Adams, B. & Adams, W. W. 2006. Photoprotection in an ecological context: the remarkable complexity of thermal energy dissipation. New Phytologist 172: 11-21.

[16] Duarte, H. M.; Geβler, A.; Scarano, F. R.; Franco, A. C.; Mattos, E. A.; Nahm, M.; Rennenberg, H.; Rodrigues, P. J. F. P.; Zaluar, H. L. T. & Lüttge, U. 2005. Ecophysiology of six selected shrub species in different plant communities at the periphery of the Atlantic Forest of SE-Brazil. Flora 200: 456-476.

[17] Eriksson, O. 1993. Dynamics of genets in clonal plants. Trends in Ecology and Evolution 9: 313-316.

[18] Faria, A. P. G. 2006. Revisão taxonômica e filogenia de Aechmea Ruiz & Pav. Subg. Macrochordion (de Vriese) Baker, Bromelioideae-Bromeliaceae. D.Sc. Thesis. Universidade Federal do Rio de Janeiro, Rio de Janeiro, 199p.

[19] Fuller, T. 2003. The integrative biology of phenotypic plasticity. Biology and Philosophy 18: 381-389.

[20] Geβler, A.; Duarte, H. M.; Franco, A. C.; Lüttge, U.; Mattos, E. A.; Nahm, M.; Scarano, F. R.; Zaluar, H. L. T. & Rennenberg, H. 2005. Ecophysiology of selected tree species in different plant communities at the periphery of the Atlantic Forest of SE- Brazil. II. Spatial and ontogenetic dynamics in deciduous Andira legalis Trees Structure and Function 19: 510-522.

[21] Griffiths, H.; Ong, B. L.; Avadhani, P. N. & Goh, C. J. 1989. Recycling of respiratory CO during crassulacean acid metabolism: 2 alleviation of photoinhibition in Pyrrosia piloselloides Planta 179: 115-122.

[22] Hansen, T. F.; Pélabon, C.; Ambruster, W. S. & Carlson, M. L. 2003. Evolvability and genetic constraint in Dalechampia blossoms: components of variance and measures of evolvability. Journal of Evolutionary Biology 16: 754-766.

[23] Harrison, S. 1991. Local extinction in a metapopulation context: an empirical evaluation. Biological Journal of the Linnean Society 42: 73-88.

[24] Högberg, P. 1997. ¹⁵N natural abundance in soil-plant systems. New Phytologist 137: 179-203.

[25] Hubbell, S. P. 2001. The unified neutral theory of biodiversity and biogeography. Princeton University Press, Princeton, 375p.

[26] Hulme, P. E. 2008. Phenotypic plasticity and plant invasions: is it all Jack? Functional Ecology 22: 3-7.

[27] Hutchings, M. J. & Kroon, H. 1994. Foraging in plants: the role of morphological plasticity in resource acquisition. Advances in Ecological Research 25: 159-238.

[28] Jain, S. K. 1979. Adaptive strategies: polymorphism, plasticity and homeostasis. : Solbrig, O. T.; Jain, S.; Johnson, G. B. & Raven P. H. (eds.). Topics in Plant Population Biology. Columbia University Press, New York. Pp. 160-187.

[29] Juniper, B. E. & Jeffree, C. E. 1983. Plant Surfaces. Edward Arnold, London. 93p.

[30] Kroon, H. & Hutchings, M. J. 1995. Morphological plasticity in clonal plants: the foraging concepts reconsidered. Journal of Ecology 83: 143-152.

[31] Kruger, L. M.; Midgley, J. J. & Cowling, R. M. 1997. Resprouters vs reseeders in South African forests trees; a model based on forest canopy height. Functional Ecology 11: 101-105.

[32] Lüttge, U. & Scarano, F. R. 2007. Synecological comparisons sustained by ecophysiological fingerprinting of intrinsic photosynthetic capacity of plants as assessed by measurements of light response curves. Revista Brasileira de Botânica 30: 355-364.

[33] Mace, G. M. & Kershaw, M. 1997. Extinction risk and rarity on an ecological timescale. : Kunin, W. E. & Gaston, K. J. (eds.). The biology of rarity: causes and consequences of rare-common differences. Chapman & Hall, London. Pp. 130-149.

[34] Macek, P. & Lepš, J. 2003. The effect of environmental heterogeneity on clonal behaviour of Prunella vulgaris L. Plant Ecology 168: 31-43.

[35] Martin, C. E. 1994. Physiological ecology of the Bromeliaceae. Botanical Review 60: 1-82.

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