Factores ambientales que modulan la fenología foliar de árboles del Bosque Atlántico

  • Débora di Francescantonio Laboratorio de Ecología Forestal y Ecofisiología, Instituto de Biología Subtropical, Universidad Nacional de Misiones, CONICET. Asociación Civil Centro de Investigaciones del Bosque Atlántico (CeIBA). http://orcid.org/0000-0002-1495-9955
  • Mariana Villagra Laboratorio de Ecología Forestal y Ecofisiología, Instituto de Biología Subtropical, Universidad Nacional de Misiones, CONICET. Asociación Civil Centro de Investigaciones del Bosque Atlántico (CeIBA).
  • Guillermo Goldstein Laboratorio de Ecología Funcional, Instituto de Ecología, Genética y Evolución de Buenos Aires, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, CONICET.
  • Paula I. Campanello Laboratorio de Ecología Forestal y Ecofisiología, Instituto de Biología Subtropical, Universidad Nacional de Misiones, CONICET. Centro de Estudios Ambientales Integrados, Facultad de Ingeniería, Universidad Nacional de la Patagonia San Juan Bosco, CONICET.
Palabras clave: bosque subtropical, fotoperíodo, hábito foliar

Resumen

La fenología foliar responde de manera sensible a distintas señales ambientales. La coordinación entre las fases fenológicas y estas señales le permite a las especies ajustar el momento óptimo para expandir sus hojas y crecer, así como para evitar los posibles daños que causan las condiciones ambientales desfavorables. Por otro lado, en las especies deciduas, la altura de los árboles es otro factor clave, ya que los eventos de expansión y caída de las hojas de los individuos del dosel determinan la disponibilidad de luz para los de menor altura. El objetivo de nuestro trabajo fue conocer de qué manera los factores ambientales interactúan con la fenología foliar en especies arbóreas de diferente hábito foliar que coexisten en el extremo sur del Bosque Atlántico semideciduo. Para esto se monitoreó la fenología foliar de 10 especies arbóreas típicas del dosel del Bosque Atlántico semideciduo en la provincia de Misiones. En las especies deciduas y brevideciduas se identificaron patrones estacionales en las fases de expansión y caída de hojas, vinculados con las variaciones en las temperaturas y el fotoperíodo. En las siempreverdes, en cambio, no se encontró una asociación clara. Los árboles deciduos no dominantes adelantaron la expansión de hojas en comparación con los dominantes. Esto implicaría una estrategia para optimizar la captura de luz y la ganancia de carbono al inicio de la primavera extendiendo la estación de crecimiento. La fenología de las especies deciduas se acopló de forma estrecha a las variables ambientales, lo cual podría generar, en estas especies, mayor vulnerabilidad ante eventos extremos de estrés ambiental, como las bajas temperaturas y el déficit hídrico.

Citas

Aguirre, L., E. Anderson, B. Gunnar, S. Herzog, and P. Jørgensen. 2012. Fenología y relaciones ecológicas interespecíficas de la biota andina frente al cambio climático. Cambio Climático y Biodiversidad en los Andes Tropicales. Pp. 428.

Augspurger, C. K., J. M. Cheeseman, and C. F. Salk. 2005. Light gains and physiological capacity of understorey woody plants during phenological avoidance of canopy shade. Functional Ecology 19:537-546. https://doi.org/10.1111/j.1365-2435.2005.01027.x.

Badeck, F. W., A. Bondeau, K. Böttcher, D. Doktor, W. Lucht, J. Schaber, and S. Sitch. 2004. Responses of spring phenology to climate change. New Phytologist 162:295-309. https://doi.org/10.1111/j.1469-8137.2004.01059.x.

Banda-R, K., A. Delgado-Salinas, K. G. Dexter, R. Linares-Palomino, Oliveira-Filho, P. Ary, M. Pullan, C. Quintana, and R. Ricarda. 2016. Plant diversity patterns in neotropical dry forests and their conservation implications. Science 353:1383-1388. https://doi.org/10.1126/science.aaf5080.

Bianchini, E., J. M. Emmerick, A. V. L. Messetti, and J. A. Pimenta. 2015. Phenology of two Ficus species in seasonal semi-deciduous forest in Southern Brazil. Brazilian Journal of Biology 75:206-214. https://doi.org/10.1590/1519-6984.10614.

Blundo, C., N. I. Gasparri, A. Malizia, M. Clark, G. Gatti, P. I. Campanello, H. R. Grau, L. Paolini, L. R. Malizia, S. E. Chediack, P. Macdonagh, and G. Goldstein. 2018. Relationships among phenology, climate and biomass across subtropical forests in Argentina. Journal of Tropical Ecology 34:93-107. https://doi.org/10.1017/S026646741800010X.

Borchert, R., Z. Calle, A. H. Strahler, A. Baertschi, R. E. Magill, J. Broadhead, J. Kamau, J. Njoroge, and C. Muthuri. 2014. Insolation and photoperiodic control of tree development near the equator. New Phytologist 205:7-13. https://doi.org/10.1111/nph.12981.

Borchert, R., and G. Rivera. 2001. Photoperiodic control of seasonal development and dormancy in tropical stem-succulent trees. Tree Physiology 21:213-221. https://doi.org/10.1093/treephys/21.4.213.

Borchert, R., G. Rivera, and W. Hagnauer. 2002. Modification of Vegetative Phenology in a Tropical Semi-deciduous Forest by Abnormal Drought and Rain1. Biotropica 34:27-39. https://doi.org/10.1646/0006-3606(2002)034[0027:MOVPIA]2.0.CO;2. https://doi.org/10.1111/j.1744-7429.2002.tb00239.x.

Borchert, R., K. Robertson, M. D. Schwartz, and G. Williams-Linera. 2005. Phenology of temperate trees in tropical climates. International Journal of Biometeorology 50:57-65. https://doi.org/10.1007/s00484-005-0261-7.

Campanello, P. I., P. Mac Donagh, and G. Goldstein. 2009. Reduced-impact logging and post-harvest mamagement in the atlantic forest of Argentina: alternative approaches to enhance regeneration and growth of canopy trees. Pp. 39-59 in S. P. Rossberg (ed.). Forest Management. Nova Science, New York, USA.

Campanello, P. I., J. F. Garibaldi, M. G. Gatti, and G. Goldstein. 2007a. Lianas in a subtropical Atlantic Forest: Host preference and tree growth. Forest Ecology and Management 242:250-259. https://doi.org/10.1016/j.foreco.2007.01.040.

Campanello, P. I., M. Genoveva Gatti, A. Ares, L. Montti, and G. Goldstein. 2007b. Tree regeneration and microclimate in a liana and bamboo-dominated semideciduous Atlantic Forest. Forest Ecology and Management 252:108-117. https://doi.org/10.1016/j.foreco.2007.06.032.

Chuine, I., and E. G. Beaubien. 2001. Phenology is a major determinant of tree species range. Ecology Letters 4:500-510. https://doi.org/10.1046/j.1461-0248.2001.00261.x.

Chuine, I., and J. Régnière. 2017. Process-Based Models of Phenology for Plants and Animals. Annual Review of Ecology, Evolution, and Systematics 48:159-182. https://doi.org/10.1146/annurev-ecolsys-110316-022706.

Cristiano, P., N. Madanes, P. Campanello, D. di Francescantonio, S. Rodríguez, Y.-J. Zhang, L. Carrasco, and G. Goldstein. 2014. High NDVI and Potential Canopy Photosynthesis of South American Subtropical Forests despite Seasonal Changes in Leaf Area Index and Air Temperature. Forests 5:287-308. https://doi.org/10.3390/f5020287.

Davies, T. J., E. M. Wolkovich, N. J. B. Kraft, N. Salamin, A. M., T. R. Ault, J. L. Betancourt, K. Bolmgren, E. E. Cleland, B. I. Cook, and T. M. Crimmins. 2013. Phylogenetic conservatism in plant phenology. Journal of Ecology 101:1520-1530. https://doi.org/10.1111/1365-2745.12154.

Denny, E. G., K. L. Gerst, A. J. Miller-Rushing, G. L. Tierney, T. M. Crimmins, C. A. F. Enquist, P. Guertin, A. H. Rosemartin, M. D. Schwartz, K. A. Thomas, and J. F. Weltzin. 2014. Standardized phenology monitoring methods to track plant and animal activity for science and resource management applications. International Journal of Biometeorology 58:591-601. https://doi.org/10.1007/s00484-014-0789-5.

Deslauriers, A., S. Rossi, and T. Anfodillo. 2007. Dendrometer and intra-annual tree growth : What kind of information can be inferred? Dendrochronologia 25:113-124. https://doi.org/10.1016/j.dendro.2007.05.003.

Forrest, J., and A. J. Miller-Rushing. 2010. Toward a synthetic understanding of the role of phenology in ecology and evolution. Philosophical Transactions of the Royal Society B: Biological Sciences 365:3101-3112. https://doi.org/10.1098/rstb.2010.0145.

di Francescantonio, D., M. Villagra, G. Goldstein, and P. I. Campanello. 2018. Leaf phenology and water-use patterns of canopy trees in Northern Argentinean subtropical forests. Tree Physiology 38:1841-1854. https://doi.org/10.1093/treephys/tpy072.

Franco, A. M. S. 2008. Estrutura, diversidade e aspectos ecológicos do componente arbustivo e arbóreo em uma floresta estacional, Parque Estadual do Turvo, sul do Brasil. Universidad Federal do Rio Grande Do Sul.

Fu, Y. H., X. Zhang, S. Piao, F. Hao, X. Geng, Y. Vitasse, C. Zohner, J. Peñuelas, and I. A. Janssens. 2019. Daylength helps temperate deciduous trees to leaf-out at the optimal time. Global Change Biology 25:2410-2418. https://doi.org/10.1111/gcb.14633.

Gatti, M. G., P. I. Campanello, L. F. Montti, and G. Goldstein. 2008. Frost resistance in the tropical palm Euterpe edulis and its pattern of distribution in the Atlantic Forest of Argentina. Forest Ecology and Management 256:633-640. https://doi.org/10.1016/j.foreco.2008.05.012.

Hijmans, R. J. 2016. geosphere: spherical trigonometry R package. URL: https://tinyurl.com/ydhhw6sn.

Hódar, J. A., R. Zamora, and J. Peñuelas. 2004. El efecto del Cambio Global en las interacciones planta- animal. Pp. 461-478 in F. Valladares (ed.). Ecología del bosque mediterráneo en un mundo cambiante. Madrid.

IBGE. 2012. Manual Técnico da Vegetação Brasileira. Série Manuais Técnicos em Geociências 1. 2nd edition. IBGE-Instituto Brasileiro de Geografia e Estatística, Rio de Janeiro, Brasil.

Jardim Botânico do Rio de Janeiro. 2018. Flora do Brasil 2020. Under construction.

Kikuzawa, K., and M. J. Lechowicz. 2011. Ecology of Leaf Longevity. Springer Tokyo, Tokyo. https://doi.org/10.1007/978-4-431-53918-6.

Kikuzawa, K., Y. Onoda, I. J. Wright, and P. B. Reich. 2013. Mechanisms underlying global temperature-related patterns in leaf longevity. Global Ecology and Biogeography 22:982-993. https://doi.org/10.1111/geb.12042.

Köcher, P., V. Horna, and C. Leuschner. 2013. Stem water storage in five coexisting temperate broad-leaved tree species: Significance, temporal dynamics and dependence on tree functional traits. Tree Physiology 33:817-832. https://doi.org/10.1093/treephys/tpt055.

Kramer, K., B. Degen, J. Buschbom, T. Hickler, W. Thuiller, M. T. Sykes, and W. de Winter. 2010. Modelling exploration of the future of European beech (Fagus sylvatica L.) under climate change-Range, abundance, genetic diversity and adaptive response. Forest Ecology and Management 259:2213-2222. https://doi.org/10.1016/j.foreco.2009.12.023.

Lasky, J. R., M. Uriarte, and R. Muscarella. 2016. Synchrony, compensatory dynamics, and the functional trait basis of phenological diversity in a tropical dry forest tree community: effects of rainfall seasonality. Environmental Research Letters 11:115003. https://doi.org/10.1088/1748-9326/11/11/115003.

Lund, U., C. Agostinelli, and M. C. Agostinelli. 2017. Package ‘circular.’ CRAN Repository.

Marques, M. C. M., J. J. Roper, and A. P. Baggio Salvalaggio. 2004. Phenological patterns among plant life-forms in a subtropical forest in southern Brazil. Plant Ecology 173:203-213. https://doi.org/10.1023/B:VEGE.0000029325.85031.90.

Morellato, L. P. C., B. Alberton, S. T. Alvarado, B. Borges, E. Buisson, M. G. G. Camargo, L. F. Cancian, D. W. Carstensen, D. F. E. Escobar, P. T. P. Leite, I. Mendoza, N. M. W. B. Rocha, N. C. Soares, T. S. F. Silva, V. G. Staggemeier, A. S. Streher, B. C. Vargas, and C. A. Peres. 2016. Linking plant phenology to conservation biology. Biological Conservation 195:60-72. https://doi.org/10.1016/j.biocon.2015.12.033.

Morellato, P., L. F. Alberti, and I. Hudson. 2010. Applications of Circular Statistics in Plant Phenology: a Case Studies Approach. Pages 339-359 in I. L. Hudson and M. Keatley (eds.). Phenological Research: Methods for Environmental and Climate Change Analysis. Springer, Dordrecht. https://doi.org/10.1007/978-90-481-3335-2_16.

Morellato, P., D. Talora, A. Takahasi, C. Bencke, E. Romera, and V. Zipparro. 2000. Phenology of Atlantic Rain Forest Trees: A Comparative Study 1. Biotropica 32:811-823. https://doi.org/10.1646/0006-3606(2000)032[0811:POARFT]2.0.CO;2. https://doi.org/10.1111/j.1744-7429.2000.tb00620.x.

Oliveira-Filho, A. T., J. C. Budke, J. A. Jarenkow, P. V. Eisenlohr, and D. R. M. Neves. 2015. Delving into the variations in tree species composition and richness across South American subtropical Atlantic and Pampean forests. Journal of Plant Ecology 8:242-260. https://doi.org/10.1093/jpe/rtt058.

Oliveira-Filho, A. T., and M. A. Fontes. 2000. Patterns of Floristic Differentiation among Atlantic Forests in Southeastern Brazil and the Influence of Climate. Biotropica 32:793-810. https://doi.org/10.1646/0006-3606(2000)032[0793:POFDAA]2.0.CO;2. https://doi.org/10.1111/j.1744-7429.2000.tb00619.x.

Osada, N., and T. Hiura. 2019. Intraspecific differences in spring leaf phenology in relation to tree size in temperate deciduous trees. Tree Physiology 39:782-791. https://doi.org/10.1093/treephys/tpz011.

Oyazabal, M., J. Clavijo, L. Oakley, F. Biganzoli, P. Tognetti, I. Barberis, H. Maturo, R. Aragón, P. I. Campanello, D. Prado, M. Oesterheld, and R. J. C. León. 2018. Unidades de vegetación de la Argentina. Ecologia Austral 28:40-63. https://doi.org/10.25260/EA.18.28.1.0.399.

Panchen, Z. A., R. B. Primack, B. Nordt, E. R. Ellwood, A. D. Stevens, S. S. Renner, C. G. Willis, R. Fahey, A. Whittemore, Y. Du, and C. C. Davis. 2014. Leaf out times of temperate woody plants are related to phylogeny, deciduousness, growth habit and wood anatomy. New Phytologist 203:1208-1219. https://doi.org/10.1111/nph.12892.

Pennington, R. T., M. Lavin, and A. Oliveira. 2009. Woody Plant Diversity, Evolution, and Ecology in the Tropics: Perspectives from Seasonally Dry Tropical Forests. Annual Review of Ecology Evolution and Systematics 40:437-457. https://doi.org/10.1146/annurev.ecolsys.110308.120327.

Pewsey, A., M. Neuhauser, and G. Ruxton. 2013. Circular statistics in R. Oxford University Press, Oxford, United Kingdom.

Di Rienzo, J. A., F. Casanoves, M. G. Balzarini, L. Gonzalez, M. Tablada, and C. W. Robledo. 2017. InfoStat versión (2017). Grupo InfoStat, FCA, Universidad Nacional de Córdoba, Argentina.

Rossi, S., and J. Bousquet. 2014. The bud break process and its variation among local populations of boreal black spruce. Frontiers in Plant Science 5:1-9. https://doi.org/10.3389/fpls.2014.00574.

van Schaik, C. P., J. W. Terborgh, and S. J. Wright. 1993. The Phenology of Tropical Forests: Adaptive Significance and Consequences for Primary Consumers. Annual Review of Ecology and Systematics 24:353-377. https://doi.org/10.1146/annurev.es.24.110193.002033.

Seki, M., T. Yoshida, and T. Takada. 2015. A general method for calculating the optimal leaf longevity from the viewpoint of carbon economy. Journal of Mathematical Biology 71:669-690. https://doi.org/10.1007/s00285-014-0830-7.

Shimamoto, C. Y., P. C. Botosso, E. Amano, and M. C. M. Marques. 2016. Stem growth rhythms in trees of a tropical rainforest in Southern Brazil. Trees-Structure and Function 30:99-111. https://doi.org/10.1007/s00468-015-1279-z.

Singh, R. K., T. Svystun, B. AlDahmash, A. M. Jönsson, and R. P. Bhalerao. 2017. Photoperiod- and temperature-mediated control of phenology in trees - a molecular perspective. New Phytologist 213:511-524. https://doi.org/10.1111/nph.14346.

Srur, M., F. Gatti, V. Benesovsky, J. Herrera, R. Melzew, and M. Camposano. 2007. Identificación, caracterización y mapeo de los ambientes del Parque Nacional Iguazú. Puerto Iguazú.

Veloso, H. P., A. L. R. Rangel-Filho, and J. C. A. Lima. 1991. Classificação da vegetação brasileira, adaptada a um sistema universal. Page (I. B. de G. e Estatística, Ed.). Rio de Janeiro, Brasil.

Vitasse, Y. 2013. Ontogenic changes rather than difference in temperature cause understory trees to leaf out earlier. New Phytologist 198:149-155.

Vitasse, Y., A. Lenz, and C. Körner. 2014. The interaction between freezing tolerance and phenology in temperate deciduous trees. Frontiers in Plant Science 5:1-12. https://doi.org/10.1111/nph.12130.

Werneck, F. P. 2011. The diversification of eastern South American open vegetation biomes: Historical biogeography and perspectives. Quaternary Science Reviews 30:1630-1648. https://doi.org/10.1016/j.quascirev.2011.03.009.

Zar, J. H. 1999. Biostatistical Analysis. Prentice-Hall Inc., New Jersey.

Zhang, Y.-J., P. M. Cristiano, Y.-P. Zhang, K.-F. Cao, and G. H. Goldstein. 2016. Carbon Economy of Subtropical Forests. Page in G. Goldstein and L. S. Santiago (eds.). Tropical Tree Physiology. Springer. https://doi.org/10.1007/978-3-319-27422-5_16.

Zuloaga, F., O. Morrone, and M. Belgrano. 2008. Catálogo de plantas vasculares del Cono Sur. Missouri Botanical Garden Press.

Factores ambientales que modulan la fenología foliar de árboles del Bosque Atlántico
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2020-10-23
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