RESPOSTAS MORFOLÓGICAS DE Ludwigia helminthorrhiza (MART.) H.HARA (ONAGRACEAE) À SAZONALIDADE HÍDRICA DO PANTANAL
DOI:
https://doi.org/10.4257/oeco.2019.2304.12Palavras-chave:
aquatic macrophyte, ecological anatomy, lombrigueira.Resumo
Em planícies de inundação, espécies de macrófitas respondem à sazonalidade hídrica por meio de alteração morfológica. Órgãos vegetativos de Ludwigia helminthorrhiza (Myrtales, Onagraceae) podem desenvolver-se em ambiente aquático e em solo livre de inundação. Acreditamos que órgãos vegetativos de plantas do segundo ambiente não apresentem adaptações típicas (e.g., aerênquima, redução de lignificação, desenvolvimento de raízes adventícias) de ambientes aquáticos. Mediu-se o comprimento, largura e espessura do limbo; espessura do caule; comprimento dos entrenós; e comprimento das raízes de indivíduos dos dois ambientes. Analisou-se a anatomia das porções medianas dos órgãos e quantificou-se os estômatos. Órgãos vegetativos foram maiores nas plantas desenvolvidas na água; densidade de estômatos semelhante nas faces do limbo nos dois ambientes, entretanto maior no solo seco. Tecidos de adaptação à anoxia, como aerênquima, expresso em maior quantidade nas plantas d’água, facilitando o transporte de gases, reduzindo fitotoxinas e suportando a planta. Há anatomia similar nos indivíduos dos dois ambientes, contudo ausência ou redução do aerênquima nos órgãos aéreos das plantas de solo seco, com presença apenas de raiz adventícia “principal” e laterais pilíferas. Nas plantas d’água observou-se quatro tipos de raízes adventícias (pneumatóforos e raiz com acréscimo de aerênquima). Evidenciamos plasticidade morfológica, importante para o sucesso no estabelecimento e sobrevivência da espécie no Pantanal.
MORPHOLOGICAL RESPONSES OF Ludwigia helminthorrhiza (MART.) H.HARA (ONAGRACEAE) TO PANTANAL WATER SEASONALITY. In floodplains, species of macrophytes respond to water seasonality through morphological alteration. Vegetative organs of Ludwigia helminthorrhiza (Myrtales, Onagraceae) can develop in aquatic environment and in soil free of flood. We believe that vegetative organs of plants of the second environment do not present typical adaptations (e.g. aerenchyma, lignification reduction, adventitious root development) of aquatic environments. The limb length, width and thickness; stem thickness; length of internodes; and roots length of individuals in the two environments were measured. The anatomy of the medial portions of the organs was analyzed and the stomata quantified. Vegetative organs were larger in plants developed in water; density of stomata similar to the limb faces in both environments, but higher in the dry soil. Adapting tissues to anoxia, as aerenchyma, expressed in greater quantity in water plants, facilitating the gases transport, reducing phytotoxins and giving plant support. There is similar anatomy in the individuals of both environments, however absence or reduction of aerenchyma in the aerial organs of dry soil plants, with presence of only “principal” adventitious root and lateral piliferous. In the water plants four types of adventitious roots (pneumatophores and root with addition of aerenchyma) were observed. We demonstrate morphological plasticity, important for success in establishing and surviving the species in the Pantanal.
Referências
Angeles, G. 1992. The periderm of flooded and non-flooded Ludwigia octovalvis (Onagraceae). IAWA Journal, 13(2), 195-200. DOI: 10.1163/22941932-90001268
Arber, A. R. 1920. Water plants: a study of aquatic angiosperms. Cambridge: Cambridge University Press: p. 468.
Armstrong, W. 1979. Aeration in higher plants. In: H. W. Woolhouse (Ed.), Advances in botanical research. pp. 225—332. London: Academic Press.
Armstrong, W., Justin, S., Beckett, P., & Lythe, S. 1991. Root adaptation to soil waterlogging. Aquatic Botany, 39, 57-73. DOI: 10.1016/0304-3770(91)90022-W
Baas, P. 1973. The wood anatomical range in Illex (Aquifoliaceae) and its ecological and phylogenetic significance. Blumea, 21, 193-258.
Baas, P., Werker, E., & Fahn, A. 1983. Some ecological trends in vessel characters. Iawa Journal, 4(2), 141-159. DOI: 10.1163/22941932-90000407
Barrett, S. C. H., Eckert, C. G., & Husband, B. C. 1993. Evolutionary processes in aquatic plant populations. Aquatic Botany, 44, 105-145. DOI: 10.1016/0304-3770(93)90068-8
Bedoya, A. M., & Madriñán, S. 2014. Evolution of the aquatic habit in Ludwigia (Onagraceae): Morpho-anatomical adaptive strategies in the Neotropics. Aquatic Botany, 120, 352-362. DOI: 10.1016/j.aquabot.2014.10.005
Blom, C. W. P. M. 1999. Adaptations to flooding stress: from plant community to molecule. Plant Biology, 1(3), 261-273. DOI: 10.1111/j.1438-8677.1999.tb00252.x
Boeger, M. R. T., & Wisniewski, C. 2003. Comparação da morfologia foliar de espécies arbóreas de três estádios sucessionais distintos de Floresta Ombrófila Densa (Floresta Atlântica) no sul do Brasil. Revista Brasileira de Botânica, 26(1), 61-72. DOI: 10.1590/S0100-84042003000100007
Boschilia, S. M., Thomaz, S. M., & Piana, P. A. 2006. Plasticidade morfológica de Salvinia herzogii (de La Sota) em resposta à densidade populacional. Acta Scientiarum Biological Sciences, 28(1), 35-39. DOI: 10.4025/actascibiolsci.v28i1.1056
Bridle, P., & Timberlake, C. F. 1997. Anthocyanins as natural food colours – selected aspects. Food Chemistry, 58(1-2), 103-109. DOI: 10.1016/s0308-8146(96)00222-1
Camargo, M. A. B., & Marenco, R. A. 2011. Density, size and distribution of stomata in 35 rainforest tree species in Central Amazonia. Acta Amazonica, 41(2), 205-212. DOI: 10.1590/S0044-59672011000200004
Carlquist, S. 1987. Wood anatomy of noteworthy species of Ludwigia (Onagraceae) with relation to ecology and systematics. Annals of the Missouri Botanical Garden, 74, 889-896. DOI: 10.2307/2399455
Castro, E. M., Pereira, F. J., & Paiva, R. 2009. Histologia vegetal: Estrutura e função de órgãos vegetativos. Lavras: Universidade Federal de Lavras: p. 234.
Catian, G., & Scremin-Dias, E. 2015. Phenotypic variations in leaf anatomy of Nymphaea gardneriana (Nymphaeaceae) demonstrate its adaptive plasticity. The Journal of the Torrey Botanical Society, 142(1), 18-26. DOI: 10.3159/TORREY-D-14-00038.1
Cook, R. E. 1979. Asexual reproduction: a further consideration. American Naturalist, 113(5), 769-772.
Crawford, R. M. M., Sduger, C., & Studer, K. 1989. Deprivation indifference as a survival strategy in competition: advantages and disadvantages of anoxia tolerance in wetland vegetation. Flora, 182(3-4), 189-201. DOI: 10.1016/S0367-2530(17)30409-7
Cutter, E. G. 1978. Plant anatomy. Massachusetts: Addison-Wesley: p. 314.
Ellmore, G. S. 1981. Root dimorphism in Ludwigia peploides (Onagraceae): development of two root types from similar primordia. Botanical Gazette, 142(4), 525-533. DOI: 10.1086/337255
Evans, J. R. 1999. Leaf anatomy enables more equal access to light and CO2 between chloroplasts. New Phytologist, 143(1), 93-104. DOI: 10.1046/j.1469-8137.1999.00440.x
Evert, R. F., Eichhorn, S. E., & Raven, P. H. 2012. Biology of plants. New York: W. H. Freeman.
Fahn, A. 1979. Secretory tissues in plants. London: Academic Press: p. 302.
Fahn, A. 1982. Plant anatomy. Oxford: Pergamon.
Feldman, L. P. 1984. Regulation of root development. Annual Review of Plant Physiology, 35, 223-242. DOI: 10.1146/annurev.pp.35.060184.001255
Folorunso, A. E., Adelalu, K. F., & Oziegbe, M. 2014. Use of foliar and stem anatomical characters in the identification of Ludwigia (Linn.) species in Nigeria. The International Journal of Biological and Chemical Sciences, 8(5), 2232-2243. DOI: 10.4314/ijbcs.v8i5.26
Gonçalves, E. G., & Lorenzi, H. 2007. Morfologia vegetal: organografia e dicionário ilustrado de morfologia das plantas vasculares, Nova Odessa: Plantarum: p. 416.
Gould, K. S., Kuhn, D. N., Lee, D. W., & Oberbauer, S. F. 1995. Why leaves are sometimes red. Nature, 378, 241-242. DOI: 10.1038/378241b0
Hamilton, S. K., Sippel, S. J., & Melack, J. M. 1996. Inundation patterns in the Pantanal wetland of South America determined from passive microwave remote sensing. Archives of Hydrobiology, 137, 1-23.
Heinrich, G. 1973. Die Feinstruktur der Trichom-Hydathoden von Monarda fistulosa. Protoplasma, 77(2), 271-278. DOI: 10.1007/BF01276763
Holdaway-Clarke, T. L., Weddle, N. M., Kim, S., Robi, A., Parris, C., Kunkel, J. G., & Hepler, P. K. 2003. Effect of extracellular calcium, pH and borate on growth oscillations in Lilium formosanum pollen tubes. Journal of Experimental Botany, 54(380), 65-72. DOI: 10.1093/jxb/erg004
Hook, D. D., & Scholtens, J. R. 1978. Adaptations and flood tolerance of tree species. In: D. D. Hook, & R. M. M. Crawford (Eds.), Plant life in anaerobic environments. pp. 299-331. Michigan: Ann Arbor.
Idestam-Almqvist, J., & Kautsky, L. 1995. Plastic responses in morphology of Potamogeton pectinatus L. to sediment and above-sediment conditions at two sites in the northern Baltic proper. Aquatic Botany, 52(3), 205-216. DOI: 10.1016/0304-3770(95)00499-8
Jackson, M. B., & Armstrong, W. 1999. Formation of aerenchyma and the processes of plant ventilation in relation to soil flooding and submergence. Plant Biology, 1(3), 274-287. DOI: 10.1111/j.1438-8677.1999.tb00253.x
Jackson, M. B., & Colmer, T. D. 2005. Response and adaptation by plants to flooding stress. Annals of Botany, 96(4), 501-505. DOI: 10.1093/aob/mci205
Jackson, M. B., & Drew, M. C. 1984. Effects of flooding on growth and metabolism of herbaceous plants. In: T. T. Kozlowski (Ed.), Flooding and plant growth. pp. 47-111. London: Academic Press.
Junk, W. J., & Piedade, M. T. F. 1997. Plant life in the floodplain with special reference to herbaceous plants. In: W. J. Junk (Ed.), The Central Amazon floodplain: ecological studies. pp. 147-185. Berlin: Springer.
Junk, W. J., Bayley, P. B., & Sparks, R. E. 1989. The flood pulse concept in river-floodplain systems. Canadian Journal of Fishers and Aquatic, 106, 110-127.
Justin, S. H. F. W., & Armstrong, W. 1987. The anatomical characteristics of roots and plant response to soil flooding. New Phytologist, 106(3), 465-495. DOI: 10.1111/j.1469-8137.1987.tb00153.x
Kaplan, Z. 2002. Phenotypic plasticity in Potamogeton (Potamogetonaceae). Folia Geobotanica, 37(2), 141-170. DOI: 10.1007/BF02804229
Kawase, M. 1981. Anatomical and morphological adaptation of plants to waterlogging. Horticultural Science, 16, 30-34.
Keating, R. 1982. The evolution and systematics of Onagraceae: leaf anatomy. Annals of the Missouri Botanical Gardener, 69(4), 770-803. DOI: 10.2307/2398996
Kolb, R. M., Medri, M. E., Bianchini, E., Pimenta, J. A., Giloni, P. C., & Correa, G. T. 1998. Anatomia ecológica de Sebastiania commersoniana (Baillon) Smith & Downs (Euphorbiaceae) submetida ao alagamento. Revista Brasileira de Botânica, 21(3), 305-312. DOI: 10.1590/S0100-84041998000300010
Kraus, J. E., & Arduim, M. 1997. Manual Básico de Métodos em Morfologia Vegetal. Seropédica: Editora da Universidade Federal Rural do Rio de Janeiro: p. 198.
Lake, J. A., Quick, W. P., Beerling, D. J., & Woodward, E. I. 2001. Signals from mature to 388 new leaves. Nature, 411(6834), 154-154. DOI: 10.1038/35075660
Leroux, O. 2012. Collenchyma: a versatile mechanical tissue with dynamic cell wall. Annals of Botany, 110(6), 1083-1098. DOI: 10.1093/aob/mcs186
Lersten, N. R., & Curtis, J. D. 1985. Distribution and anatomy of hydathodes in Asteraceae. Botanical Gazette, 146(1), 106-114. DOI: 10.1086/337504
Lillie, R. D. 1965. Histopathologic technic and practical histochemistry. New York: McGraw-Hill.
Lovett Doust, L. 1981. Population dynamics and local specialization in a clonal perennial (Ranunculus repens). I The dynamics of ramets in contrasting habitats. Journal of Ecology, 69(3), 743-755. DOI: 10.2307/2259633
Lytle, S. T. 2003. Adaptation and acclimation of populations of Ludwigia repens to growth in high-and lower-CO2 springs. Doctoral thesis. Botany Department at the University of Florida. p. 146.
Macedo, N. A. 1997. Manual de técnicas em histologia vegetal. Feira de Santana: Universidade Estadual Feira de Santana: p. 96.
Metcalfe, C. R., & Chalk, L. 1972. Anatomy of the dicotyledons. Oxford: Clarenton Press: p. 1500.
Metcalfe, C. R., & Chalk, L. 1979. Anatomy of the Dicotyledons. Oxford: Clarendon Press: p. 276.
Montefusco, A. R. G. 2005 Anatomia ecológica do lenho de Stryphnodendron adstringens (Mart.) Coville (Leguminosae), Barbatimão, no Parque Estadual de Cerrado, Jaguariaíva-PR. Master thesis. Setor de Ciências Agrárias da Universidade Federal do Paraná. p. 105.
Morretes, B. L., & Ferri, M. G. 1959. Contribuição ao estudo da anatomia das folhas de plantas do Cerrado I. Boletim da Faculdade de Filosofia, Ciências e Letras da USP, 16, 7-70. DOI: 10.11606/issn.2318-5988.v16i0p7-70
Moysset, L., & Simon, E. 1991. Secondary pulvinus of Robinia pseudoacacia (Leguminosae) – structural and ultrastructural features. American Journal of Botany, 78(11), 1467-1486. DOI: 10.1002/j.1537-2197.1991.tb11426.x
Niklas, K. J. 2009. Functional adaptation and phenotypic plasticity at the cellular and whole plant level. Journal of Biosciences, 34(4), 613-620. DOI: 10.1007/s12038-009-0079-2
Paiva, E. A. S., & Machado, S. R. 2003. Collenchyma in Panicum maximum (Poaceae): localisation and possible role. Australian Journal of Botany, 51, 69-73. DOI: 10.1071/BT02046
Peel, M. C., Finlayson, B. L., & McMahon, T. A. 2007. Updated world map of the Köppen-Geiger climate classification. Hydrology and Earth System Sciences, 11(5), 1633-1644. DOI: 10.5194/hess-11-1633-2007
Pilon, J., & Santamaría, L. 2002. Clonal variation in morphological and physiological responses to irradiance and photoperiod for the aquatic angiosperm Potamogeton pectinatus. Journal of Ecology, 90(5), 859-870. DOI: 10.1046/j.1365-2745.2002.00716.x
Pott, A., & Pott, V. J. 1994. Plantas do Pantanal. Brasília: Embrapa: p. 320.
Pott, V. J., & Pott, A. 2000. Plantas aquáticas do Pantanal. Corumbá: Embrapa: p. 404.
Pozer, C. G., & Nogueira, F. 2004. Pastagens nativas inundáveis da região norte do Pantanal de Mato Grosso: variações de biomassa e de produtividade primária. Brazilian Journal of Biology, 64(4), 859-866. DOI: 10.1590/S1519-69842004000500016.
Raven, P. H. 2001. Biologia vegetal. Guanabara Koogan: Rio de Janeiro: p. 906.
Rich, S. M., Ludwig, M., & Colmer, T. D. 2012. Aquatic adventitious root development in partially and completely submerged wetland plants Cotula coronopifolia and Meionectes brownii. Annals of Botany, 110(2), 405-414. DOI: 10.1093/aob/mcs051
Ridge, I. 1987. Ethilene and growth control in amphibious plants. In: R. M. M. Crawford (Ed.), Plant life in aquatic and amphibious habitats. pp. 53-76. Oxford: Blackwell Scientific Publications.
Rizzini, C. T. 1997. Tratado de fitogeografia do Brasil: aspectos ecológicos, sociológicos e florísticos. Rio de Janeiro: Âmbito Cultural Edições.
Rodrigues, R. S., & Irgang, B. E. 2001. Potamogetonaceae Dumort. no Rio Grande do Sul, Brasil. Iheringia, Serie Botânica, 56, 3-49. DOI: 10.1590/2175-7860201768117
Rodrigues, S., Scremin-Dias, E., Medeiros, H. C. S., & Souza, M. C. 2007. Alterações estruturais do caule e da folha de Ludwigia inclinata (L.F.) M. Gómez, desenvolvidos emersos e submersos. Revista Brasileira de Biociências, 5(1), 174-176.
Rutishauser, R. 1997. Structural and developmental diversity in Podostemaceae (river-weeds). Aquattic Botany, 57(1-4), 29-70. DOI: 10.1016/S0304-3770(96)01120-5
Santamaría, L. 2002. Why are most aquatic plants widely distributed? Dispersal, clonal growth and small-scale heterogeneity in a stressful environment. Acta Oecologica, 23(3), 137-154. DOI: 10.1016/S1146-609X(02)01146-3
Santamaría, L., Figuerola, J., Pilon J. J., Mjelde, M., Green, A. J., Boer, T., King, R. A., & Gornall, R. J. 2003. Plant performance across latitude: the role of plasticity and local adaptation in an aquatic plant. Ecology, 84(9), 2454-2461. DOI: 10.1890/02-0431
Scremin-Dias, E. 1999. O retorno à origem aquática. In: E. Scremin-Dias, V. J. Pott, R. C. Hora, & P. R. Souza (Orgs.), Nos jardins submersos da Bodoquena. pp. 25-42. Campo Grande: Universidade Federal de Mato Grosso do Sul.
Scremin-Dias, E. 1992. Morfoanatomia dos órgãos vegetativos de Ludwigia sedoides (Humb. & Bonpl.) Hara (Onagraceae) ocorrente no Pantanal Sul-Mato-Grossense. Master thesis. Setor de Ciências biológicas da Universidade Federal do Paraná.
Scremin-Dias, E., Lorenz-Lemke, A. P., & Oliveira, A. K. M. 2011. The floristic heterogeneity of Pantanal and the occurrence of species with different adaptive strategies to water stress. Brazilian Journal of Biology, 71(1), 275-282. DOI: 10.1590/S1519-69842011000200006
Scremin-Dias, E., Pott, V. J., Hora, R. C., & Souza, P. R. 1999. Nos jardins submersos da Bodoquena: guia para identificação das plantas aquáticas de Bonito e região. Campo Grande: Ed. UFMS p. 160.
Sculthorpe, C. D. 1967. The Biology of aquatic vascular plants. Londres: Eduard Arnold Publ: p. 620.
Sculthorpe, C. D. 1985. The biology of aquatic vascular plants. Königstein: Koeltz Scientifc Books: p. 610.
Seago, J. L., & Fernando, D. D. 2013. Anatomical aspects of angiosperm root evolution. Annals of Botany, 112, 223-238.
Seago, J. L., Marsh, L. C., Stevens, K. J., Soukup, A., Votrubova, O., & Enstone, D. E. 2005. A re-examination of the root cortex in wetland flowering plants with respect to aerenchyma. Annals of Botany, 96(4), 565-579. DOI: 10.1093/aob/mci211
Shimamura, S., Yamamoto, R., Nakamura, T., Shimada, S., & Komatsu, S. 2010. Stem hypertrophic lenticels and secondary aerenchyma enable oxygen transport to roots of soybean in flooded soil. Annals of Botany, 106(2), 277-284. DOI: 10.1093/aob/mcq123
Silva, J. S. V., & Abdon, M. M. 1998. Delimitação do Pantanal Brasileiro e suas sub-regiões. Pesquisa Agropecuária Brasileira, 33, 1703-1711.
Somavilla, N. S., & Graciano-Ribeiro, D. 2012. Ontogeny and characterization of aerenchymatous tissues of Melastomataceae in the flooded and well-drained soils of a Neotropical Savanna. Flora, 207(3), 212-222. DOI: 10.1016/j.flora.2012.01.007
Soriano, B. M. A., Clarke, R. T., & Catella, A. C. 2001. Evolução da erosividade das cheias na bacia do rio Taquari. Corumbá: Embrapa Pantanal. Boletim de Pesquisa: p. 18.
Spencer, D. F. 1986. Early growth of Potamogeton pectinatus L. in response to temperature and irradiance: morphology and pigment composition. Aquatic Botany, 26, 1-8.
Spencer, W. E., & Bowes, G. 1990. Ecophysiology of the world’s most troublesome aquatic weeds. In: A. H. Pieterse, & K. J. Murphy (Eds.), Aquatic weeds: the ecology and management of nuisance aquatic vegetation. pp. 39-73. Oxford: Oxford University Press.
Thomaz, S. M., & Bini, L. M. 2003. Ecologia e manejo de macrófitas aquáticas. Maringá: Universidade Estadual de Maringá: p. 341.
Via, S., Gomulkiewicz, R., Jong, G., Schlichting, C. D., & Van Tienderen, P. H. 1995. Adaptative phenotypic plasticity: consensus and controversy. Trends in Ecology & Evolution, 10(5), 212-217. DOI: 10.1016/S0169-5347(00)89061-8
West-Eberhard, M. J. 2003. Developmental plasticity and evolution. Oxford: Oxford University Press: p. 816.
Yamamoto, F., Sakata, T., & Terazawa, K. 1995. Growth, morphology, stem anatomy, and ethylene production in flooded Alnus japonica seedlings. IAWA Journal, 16 (1), 47-59. DOI: 10.1163/22941932-90001388
Zar, J. H. 1999. Biostatistical analysis. New Jersey: Prentice Hall.
