Rita de Cássia Quitete Portela, Verônica Marques Feliciano da Silva, Eduardo Teles Barbosa Mendes, Thales Moreira de Lima, Maria Isabel Guedes Braz, Adilson Martins Pintor, Pheterson Godinho de Oliveira, Eduardo Arcoverde de Mattos


Temporal variation in rainfall and temperature, which is likely to increase in frequency due to climate change, may cause changes not only in the endogenous rhythms of organisms, but also in their phenology. This is of great concern, because ecological mismatches caused by phenological shifts may affect not only individuals but entire communities, via disruption and cascade effects in diverse ecological processes. Here, we tested the sensitivity of the phenology of Euterpe edulis Mart. to a period of extreme drought, using phenological data for three populations occurring from 0 to 1,200 m a.s.l.. Euterpe edulis is a Neotropical palm that is ecologically important because of its abundance and diverse frugivorous interactions. Three phenophases (flowers, unripe fruit, and ripe fruit) were recorded monthly from June 2014 to May 2017. Additionally, seeds were collected in 2014 and 2015 to assess wet and dry mass variation. The intensity of the drought varied with altitude. The main differences between populations were earlier flowering, a longer fruit maturation period, and larger seeds at higher altitudes. In the year of the severe drought, there were marked decreases in the synchrony of flowering and unripe fruits in the high-altitude populations. All populations exhibited decreases in seed water content, but only the high-altitude populations had decreases in seed dry mass, probably due to the drought. Despite differences in the total annual rainfall, there was relatively similar exposure to the intense drought across the altitudinal range. Populations did however differ in their sensitivity to drought, and the high-altitude populations were not able to maintain synchrony in the flowering and unripe fruit phases. Extreme events in which both climatic and biotic responses were observed were thus related to distinct population thresholds to rainfall shifts in an endangered tropical keystone palm species.


Arecaceae; Atlantic rainforest; drought; long-term ecological research; phenology; southeastern Brazil

Full Text:



Allen, C.D., Macalady A.K., Chenchoun H., Bachelet D., McDowell N., Vennetier M., Kitzberger T., Rigling A., Breshears D.D., Hogg E.H. (Ted), Gonzalez P., Fensham R., Zhang Z., Castro J., Demidova N., Lim J., Allard G., Running S.W., Semerci A., Cobb N. 2010. A Global Overview of Drought and Heat-Induced Tree Mortality Reveals Emerging Climate Change Risks for Forests. Forest Ecology and Management, 259 (4): 660–684. https://doi.org/10.1016/j.foreco.2009.09.001.

Anderson, J.T., Inouye D.W.I., McKinney A.M., Colautti R.I., Mitchell-Olds T. 2012. Phenotypic Plasticity and Adaptive Evolution Contribute to Advancing Flowering Phenology in Response to Climate Change. Proceedings of the Royal Society B: Biological Sciences, 279 (1743), 3843–3852. https://doi.org/10.1098/rspb.2012.1051.

Andrade, A.C.S. 2001. The Effect of Moisture Content and Temperature on the Longevity of Heart of Palm Seeds (Euterpe Edulis). Seed Science and Technology, 29 (1), 171–82.

Bencke, C.C. & Morellato, L.P.C. 2002. Estudo Comparativo Da Fenologia de Nove Espécies Arbóreas Em Três Tipos de Floresta Atlântica no Sudeste Do Brasil. Revista Brasileira de Botânica, 25 (2), 237–248. https://doi.org/10.1590/s0100-84042002000200012.

Bradley, N.L., Leopold A.C., Ross J., Huffaker W. 1999. Phenological Changes Reflect Climate Change in Wisconsin. Proceedings of the National Academy of Sciences of the United States of America 96 (17): 9701–4. https://doi.org/10.1073/pnas.96.17.9701.

Braz, M.I.G., Portela, R.D.C.Q., Cosme, L.H.M., Marques, V.G.C., de Mattos, E.A. 2014. Germination niche breadth differs in two co-occurring palms of the Atlantic Rainforest. Natureza & Conservação, 12(2), 124-128.https://doi.org/10.1016/j.ncon.2014.09.003.

Bruno, M.M.A., Massi, K.G., Vidal, M.M., Hay, J.V. 2019. Reproductive Phenology of Three Syagrus Species (Arecaceae) in a Tropical Savanna in Brazil. Flora: Morphology, Distribution, Functional Ecology of Plants, 252, 18–25. https://doi.org/10.1016/j.flora.2019.02.002.

Cardoso, S.R.S., Eloy, N.B., Provan, J., Cardoso, M.A., Ferreira P.C.G. 2000. Genetic Differentiation of Euterpe Edulis Mart. Populations Estimated by AFLP Analysis. Molecular Ecology, 9(11), 1753–1760. https://doi.org/10.1046/j.1365-294X.2000.01056.x.

Castro, E.R., Galetti, M., Morellato, L. P.C. 2007. Reproductive Phenology of Euterpe Edulis (Arecaceae) along a Gradient in the Atlantic Rainforest of Brazil. Australian Journal of Botany, 55 (7), 725–735. https://doi.org/10.1071/BT07029.

Chambers, J.M., Cleveland, W.S., Kleiner, B., Tukey, P.A. 1983. Graphical Methods for Data Analysis. Wadsworth & Brooks/Cole. Pacific Grove.

Chuine, I., Beaubien E.G. 2001. Phenology Is a Major Determinant of Tree Species Range. Ecology Letters, 4 (5), 500–510. https://doi.org/10.1046/j.1461-0248.2001.00261.x.

Chuine, I., Cambon G., Comtois P. 2000. Scaling Phenology from the Local to the Regional Level: Advances from Species-Specific Phenological Models. Global Change Biology, 6 (8), 943–952. https://doi.org/10.1046/j.1365-2486.2000.00368.x.

Cleland, E.E., Chuine I., Menzel A., Mooney H. A., Schwartz M.D. 2007. Shifting Plant Phenology in Response to Global Change. Trends in Ecology and Evolution, 22 (7), 357–365. https://doi.org/10.1016/j.tree.2007.04.003.

Colwell, R.K., Brehm G., Cardelús, C.L., Gilman, A.C., Longino, J.T. 2008. Global Warming, Elevational RangeShifts, and Lowland Biotic Attrition in the Wet Tropics. Science, 322, 258–261. https://doi.org/10.1126/science.1162547.

De Steven, Diane, Donald M. Windsor, Francis E. Putz, and Bonifacio de Leon. 1987. Vegetative and Reproductive Phenologies of a Palm Assemblage in Panama. Biotropica, 19 (4), 342–356. https://doi.org/10.2307/2388632.

Duputié, A, Rutschmann, A., Ronce, O., Chuine, I. 2015. Phenological Plasticity Will Not Help All Species Adapt to Climate Change. Global Change Biology, 21 (8), 3062–3073. https://doi.org/10.1111/gcb.12914.

Elzinga, J.A., Atlan, A., Biere A., Gigord L., Weis, A.E., Bernasconi, G. 2007. Time after Time: Flowering Phenology and Biotic Interactions. Trends in Ecology and Evolution, 22 (8), 432–439. https://doi.org/10.1016/j.tree.2007.05.006.

Fantini, A.C., Guries, R.P. 2007. Forest Structure and Productivity of Palmiteiro (Euterpe Edulis Martius) in the Brazilian Mata Atlântica. Forest Ecology and Management, 242 (2–3), 185–194. https://doi.org/10.1016/j.foreco.2007.01.005.

Favreto, R. 2010. Aspectos Etnoecológicos e Ecofisiológicos de Euterpe Edulis Mart. (Arecaceae). Tese de doutorado. Instituto de Biociência do Programa de Pós-Graduação em Botânica da Universidade Federal do Rio Grande do Sul. p.143.

Fisch, S.T.V., Nogureira Jr., L.R., Mantovani, W. 2000. Fenologia Reprodutiva de Euterpe Edulis Mart. Na Mata Atlântica (Reserva Ecológica Do Trabiju, Pindamonhangaba – SP). Revista de Biociência, 6 (2), 31–37. https://doi.org/10.1590/S1676-06032006000300008.

Foden, W.B., Young, B. E., Akçakaya, H.R., Garcia R.A., Hoffmann, A.A., Stein B.A., Thomas, C.D., Wheatley, C.J., Bickford, D., Carr, J.A., Hole, D.G., Martin, T.G., Pacific, M., Pearce-Higgins, J.W., Platts, P.J., Visconti, P., Watson, J.E.M. 2019. Climate Change Vulnerability Assessment of Species. Wiley Interdisciplinary Reviews: Climate Change, 10 (1), 1–36. https://doi.org/10.1002/wcc.551.

Forrest, J.R.K. 2016. Complex Responses of Insect Phenology to Climate Change. Current Opinion in Insect Science 17, 49–54. https://doi.org/10.1016/j.cois.2016.07.002.

Galetti, M., Aleixo, A. 1998. Effects of Palm Heart Harvesting on Avian Frugivores in the Atlantic Rain Forest of Brazil. Journal of Applied Ecology, 35 (2), 286–293. https://doi.org/10.1046/j.1365-2664.1998.00294.x.

Galetti, M., Fernandez, J.C. 1998. Palm Heart Harvesting in the Brazilian Atlantic Forest: Changes in Industry Structure and the Illegal Trade. Journal of Applied Ecology, 35 (2), 294–301. https://doi.org/10.1046/j.1365-2664.1998.00295.x.

Genini, Julieta, Galetti M., Morellato L.P.C. 2009. Fruiting Phenology of Palms and Trees in an Atlantic Rainforest Land-Bridge Island. Flora: Morphology, Distribution, Functional Ecology of Plants, 204 (2), 131–145. https://doi.org/10.1016/j.flora.2008.01.002.

Grubb, P.J. 1977. The Maintenance of Species-Richness in Plant Communities: The Importance of the Regeneration Niche. Biological Reviews, 52 (1), 107–145. https://doi.org/10.1111/j.1469-185X.1977.tb01347.x.

Harrison, R. D. 2000. Repercussions of El Nino: drought causes extinction and the breakdown of mutualism in Borneo. Proceedings of the Royal Society of London. Series B: Biological Sciences, 267 (1446), 911-915. https://doi.org/10.1098/rspb.2000.1089.

Hart, Robbie, Salick, J. 2018. Vulnerability of Phenological Progressions over Season and Elevation to Climate Change: Rhododendrons of Mt. Yulong. Perspectives in Plant Ecology, Evolution and Systematics 34, 129–139. https://doi.org/10.1016/j.ppees.2018.09.001.

Henderson, A., Galeano, G., Bernal, R. 1995. Field guide to the palms of the Americas. New Jersey: Princeton University Press. p. 502.

Instituto Nacional de Meteorologia (INMET). Retrieved on August 21, 2019, from http://www.inmet.gov.br.

IPCC, 2014. Climate Change. 2014: Synthesis Report. Contribution of Working Groups I, II and III to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change [Core Writing Team, R.K. Pachauri and L.A. Meyer (eds.)]. IPCC, Geneva, Switzerland. p.151.

Jentsch, A., Kreyling, J., Beierkuhnlein, C. A new generation of climate‐change experiments: events, not trends. 2007. Frontiers in Ecology and Environment, 5(7), 365-374

Llorens, L., Peñuelas, J. 2005. Experimental Evidence of Future Drier and Warmer Conditions Affecting Flowering of Two Co-Occurring Mediterranean Shrubs. International Journal of Plant Sciences, 166 (2), 235–245. https://doi.org/10.1086/427480.

Lorenzi, H., Noblick, L.R., Kahn F., Ferreira E. 2010. Flora Brasileira: Arecaceae (Palmeiras). Instituto Plantarum, São Paulo. Nova Odessa: p.368.

Malhi, Y., Girardin, C.A.J., Goldsmith, G.R., Doughty, C.E., Salinas, N., Metcalfe D.B., Huasco,W.H., Silva-Espejo, J.E., De Aguilla-Pasquell, J., Amézquita, F.F., Aragão, L.E.O.C., Guerrieri, R., Ishida, F.Y., Bahar, N.H.A., Farfan-Rios, W., Phillips, O.L. Meir, P., Silman, Miles. 2017. The Variation of Productivity and Its Allocation along a Tropical Elevation Gradient: A Whole Carbon Budget Perspective. New Phytologist, 214 (3), 1019–1032. https://doi.org/10.1111/nph.14189.

Martinelli, G., Moraes, M. A. 2013. Livro Vermelho da Flora Brasileira. Andrea Jakobson Estúdio. Instituto de Pesquisas Jardim Botânico do Rio de Janeiro, Rio de Janeiro. p.1100.

Moles, A.T., Westoby, M. 2004. Seed mass and seedling establishment after fire in Ku-ring-gai Chase National Park, Sydney, Australia. Austral Ecology, 29 (4), 383–390. https://doi.org10.1111/j.1442-9993.2004.01374.x

Morellato, L.P.C., Alberton, B., Alvarado, S.T., Borges, B., Buisson, E., Camargo, M.G.G., Cancian, L.F., Carstensen, D.W., Escobar, D.F.E., Leite, P.T.P., Mendoza, I., Rocha, N.M.W.B., Soares,. N.C., Silva, T.S.F., Staggemeier, V.G., Streher, A.S., Vargas, B.C., Peres, C.A. 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.C., Talora, D.C., Takahasi, A., Bencke, C.C., Romera, E.C., Zipparro, V.B. 2000. Phenology of Atlantic Rain Forest Trees: A Comparative Study1. Biotropica, 32 (4), 811–823. https://doi.org/10.1646/0006-3606(2000)032[0811:poarft]2.0.co;2.

Nicotra, A.B., Atkin, O.K., Bonser, S.P., Davidson, A.M., Finnegan, E.J., Mathesius, U., Poot, P. Purugganan, M.D., Richards, C.L., Valladares, F., van Kleunen, M. 2010. Plant Phenotypic Plasticity in a Changing Climate. Trends in Plant Science 15 (12). Elsevier: 684–692. https://doi.org/10.1016/j.tplants.2010.09.008.

Olejniczak, P., Czarnoleski, M., Delimat, A., Majcher, B.M., Szczepka, K. 2018. Seed Size in Mountain Herbaceous Plants Changes with Elevation in a Species-Specific Manner. PLoS ONE, 13 (6), 1–14. https://doi.org/10.1371/journal.pone.0199224.

Peñuelas, J., Gordon C., Llorens L., Nielsen, T., Tietema, A., Beier, C., Bruna p., Emmett, B., Estiarte, M., and Gorissen A. 2004. Nonintrusive Field Experiments Show Different Plant Responses to Warming and Drought among Sites, Seasons, and Species in a North-South European Gradient. Ecosystems, 7 (6), 598–612. https://doi.org/10.1007/s10021-004-0179-7.

Pessoa S. V. A.; Oliveira R. R. 2006. Análise estrutural da vegetação arbórea em três fragmentos florestais na reserva biológica de Poço das Antas, Rio de Janeiro, Brasil. Rodriguésia, 57(3), 391–411. http://dx.doi.org/10.1590/2175-7860200657302.

Primack, Richard B. 1987. Relationships among flowers, fruits, and seeds. Annual Review of Ecology and Systematics, 18, 409–430

Qi, W., Bu, H., Cornelissen, J.H.C., Zhang, C., Guo S., Wang, J., Zhou, X., Li, W., Du, G. 2015. Untangling Interacting Mechanisms of Seed Mass Variation with Elevation: Insights from the Comparison of Inter-Specific and Intra-Specific Studies on Eastern Tibetan Angiosperm Species. Plant Ecology, 216 (2), 283–292. https://doi.org/10.1007/s11258-014-0435-7.

Quitete, R.C.P., Bruna, E.M., Santos, F.A.M. 2010. Demography of Palm Species in Brazil’s Atlantic Forest: A Comparison of Harvested and Unharvested Species Using Matrix Models. Biodiversity and Conservation, 19 (8), 2389–2403. https://doi.org/10.1007/s10531-010-9846-5.

R Development Core Team. 2015. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0, URL http://www.R-project.org/

Rathcke, B., Lacey, E.P. 1985. Phenological Patterns of Terrestrial Plants. Annual Review of Ecology and Systematics, 16, 179–214.

Sakai, S., Kitajima, K. 2019. Tropical Phenology: Recent Advances and Perspectives. Ecological Research, 34 (1), 50–54. https://doi.org/10.1111/1440-1703.1131.

Sakurai, A., Takahashi, K. 2017. Flowering Phenology and Reproduction of the Solidago Virgaurea L. Complex along an Elevational Gradient on Mt Norikura, Central Japan. Plant Species Biology, 32 (4), 270–278. https://doi.org/10.1111/1442-1984.12153.

Sattler, D., Lindner, A., Morawetz, W. 2007. A função da sazonalidade no levantamento estrutural de uma floresta montana tropical no Rio de Janeiro. Brasil. In: Cronemberger C. & De Castro EBV (Eds.). Ciência e conservação Serra dos Órgãos. 1st ed. pp.105–116. Vegetação e Flora. IBAMA, Brasilia

Schwartz, N.B., Budsock, A.M., Uriarte M. 2019. Fragmentation, Forest Structure, and Topography Modulate Impacts of Drought in a Tropical Forest Landscape. Ecology, 100 (6), e02677. https://doi.org/10.1002/ecy.2677.

Silva Matos, D.M., Freckleton P.R., Watkinson A.R.. 1999. The Role of Density Dependence in the Population Dynamics of a Tropical Palm. Ecology, 80 (8), 2635–2650. https://doi.org/10.1890/0012-9658(1999)080[2635:TRODDI]2.0.CO;2.

Smith, M.D. 2011. An Ecological Perspective on Extreme Climatic Events: A Synthetic Definition and Framework to Guide Future Research. Journal of Ecology, 99 (3), 656–663. https://doi.org/10.1111/j.1365-2745.2011.01798.x.

Staggemeier, V.G., Morellato L.P.C. 2011. Reproductive Phenology of Coastal Plain Atlantic Forest Vegetation: Comparisons from Seashore to Foothills. International Journal of Biometeorology, 55 (6), 843–854. https://doi.org/10.1007/s00484-011-0482-x.

Tanner, E.V.J., Vltousek, P.M., Cuevas. E. 1998. Experimental Investigation of Nutrient Limitation of Forest Growth on Wet Tropical Mountains. Ecology, 79 (1), 10–22. https://doi.org/10.1890/0012-9658(1998)079[0010:EIONLO]2.0.CO;2.

Terborgh, J. 1986. Keystone Plant Resources in the Tropical Forest. In: Soulé, I. & Michael, E. (Eds.). Conservation Biology, pp. 330–344. Sinauer, Sunderland.

The United States Naval Observatory (USNO). Retrieved on August 15, 2019, from https://aa.usno.navy.mil/data/docs/Dur_OneYear.php.

van Schaik, C.P., Terborgh J.W., Wright S.J. 1993 The phenology of tropical forests: adaptive significance and consequences for primary consumers. Annual Review of ecology and Systematics, 24.1, 353–377.

Walther, G., Post, E., Convey, P., Menzel, A., Parmesan, C., Beebee, T. J. C., Fromentin, J., Hoegh-Guldberg, O., Bairlein., F. 2002. Ecological responses to recent climate change. Nature 416, 389–395.

Westoby, M., Leishman, M., & Lord, J. (1996). Comparative ecology of seed size and dispersal. Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences ,351(1345), 1309–1318. https://doi.org/10.1098/rstb.1996.0114.

Wolfe, L.M., Burns J.L. 2001. A Rare Continual Flowering Strategy and Its Influence on Offspring Quality in a Gynodioecious Plant. American Journal of Botany, 88 (8), 1419–1423. https://doi.org/10.2307/3558448.

Wolkovich, E..M, Davies, T.J., Schaefer, H., Cleland, E.E., Cook, B.I., Travers, S.E., Willis, C.G., Davis, C.C. 2013. Temperature-Dependent Shifts in Phenology Contribute to the Success of Exotic Species with Climate Change. American Journal of Botany, 100 (7), 1407–1421. https://doi.org/10.3732/ajb.1200478.

Zar, J. H. 1996. Biostatistical analysis. Prentice-Hall, Upper Saddle River, New Jersey. p. 662.

DOI: https://doi.org/10.4257/oeco.2020.2402.11


  • There are currently no refbacks.