Anderson da Rocha Gripp, Luísa Alícida Fernandes Tavares, Letícia da Silva Brito, Adriano Caliman, André Tavares Corrêa Dias, Eduardo Arcoverde de Mattos, Dora Villela, Ana Paula Silva, Francisco de Assis Esteves, Rodrigo Lemes Martins


Climate is an important driver of litterfall along different ecosystems. However, little is known about how climate affects litter production in plant communities of Restinga. The aim of this study is to characterize the temporal variation in leaf litter production in an Open Clusia Formation in Restinga de Jurubatiba National Park, from 2001 to 2018, and assess how local variability in litter production reflects the local climatic conditions and its variability. We tested the hypothesis that monthly leaf litterfall increases in dry months and in drier and warmer than average months; we also evaluated if annual leaf litterfall increases in wetter and warmer years following leaf production patterns, that increases in these conditions. We found that litterfall peaks in the drier months. This pattern is consistent for many tropical ecosystems, even evergreen ecosystems, and may have evolved as a strategy that result in reduced water stress by plants, during drier and warmer periods, or may simply be a stress symptom. However, we also found that decreases in monthly rainfall and increases in monthly ∆Temperature (temperature observed minus estimated based on 1970-2000 interval) stimulate leaf litter production. Hot and warmer than average years also seem to stimulate leaf litterfall. It suggests that annual leaf litterfall and leaf production are less affected by precipitation regimes than variations in temperature (or radiation, which is directly related to temperature). It may result from the fact that Clusia hilariana, the dominant species in this ecosystem which accounts to 80 % of leaf litterfall, is a CAM photosynthesis species, a characteristic commonly associated with avoidance of water stress by plants. Although leaf litterfall seems to be predominantly driven by climate at annual scale, only 15 % of its variation was associated to climate at seasonal scale, suggesting that local factors control litterfall at lower temporal scales in Open Clusia Formation.


Climatic variability; coastal sand dune vegetation; litter production; open Clusia formation.


Alvares, C. A., Stape, J. L., Sentelhas, P. C., de Moraes, G., Leonardo, J., & Sparovek, G. 2013. Köppen's climate classification map for Brazil. Meteorologische Zeitschrift, 22(6), 711–728. DOI:10.1127/0941-2948/2013/0507

Araujo, D. d., & Henriques, R. P. 1984. Análise florística das restingas do Estado do Rio de Janeiro. In: Lacerda, L.D., Araújo, D.S.D., Cerqueira, R. & Turcq, B. (Eds.). Restingas: origem, estrutura e processos. pp. 159–193. Anais do Simpósio de Restingas Brasileiras. Niterói: CEUFF.

Araújo, V., Barbosa, M., Araújo, J., & Vasconcellos, A. 2019. Spatial-temporal variation in litterfall in seasonally dry tropical forests in Northeastern Brazil. Brazilian Journal of Biology, 1–12. DOI: 10.1590/1519-6984.192113

Barnes, B. V., Zak, D. R., Denton, S. R., & Spurr, S. H. 1998. Forest Ecology. New York: John Wiley & Sons. p. 774.

Berg, B., & Laskowski, R. 2005. Litter fall. Advances in Ecological Research, 38, 19–71. DOI:10.1016/S0065-2504(05)38002-0

Borchert, R., Calle, Z., Strahler, A. H., Baertschi, A., Magill, R. E., Broadhead, J. S., Kamau, J., Njoroge, J., Muthuri, C. 2015. Insolation and photoperiodic control of tree development near the equator. New Phytologist, 205(1), 7–13. DOI:10.1111/nph.12981

Brietz, R. M. D. 1994. Ciclagem de nutrientes minerais em duas florestas da planície litorânea da Ilha do Mel, Paranaguá, PR. Dissertação de Mestrado. Universidade Federal do Paraná, Curitiba. p. 256.

Brito, L. S. 2015. Avaliação do aporte e decomposição da serapilheira e lixiviação de nutrientes em duas fitofisionomias de uma restinga do Norte Fluminense. Dissertação de Mestrado, Universidade Federal do Rio de Janeiro - Campus UFRJ-Macaé Professor Aloisio Teixeira, Macaé. p. 83.

Brito, L. S., Irmler, U., Forte, B. V. G., Xavier, T. P., & Martins, R. L. 2018. Matter turnover in the oligotrophic restinga ecosystem and the importance of the key species Clusia hilariana. Biota Neotropica, 18(4), 1–10. DOI:10.1590/1676-0611-bn-2018-0552

Camara, R., Pereira, M. G., Menezes, L. F. T., Segall, A. B., & Castro, J. S. R. 2018. Litter Dynamics in a Forest Dune at Restinga da Marambaia, RJ, Brazil. Floresta e Ambiente, 25(2). 1–10. DOI:10.1590/2179-8087.004616

Caris, E. A. P., Kurtz, B. C., Cruz, C. B. M., & Scarano, F. R. 2013. Vegetation cover and land use of a protected coastal area and its surroundings, southeast Brazil. Rodriguésia, 64(4), 747–755. DOI:10.1590/S2175-78602013000400006

Carvalho, D. C. d., Pereira, M. G., & de Menezes, L. F. T. 2014. Aporte de biomassa e nutrientes por Allagoptera arenaria na Restinga da Marambaia, Rio de Janeiro, RJ. Floresta, 44(3), 349–358. DOI:10.5380/rf.v44i3.28142

Cebrian, J. 1999. Patterns in the fate of production in plant communities. The American Naturalist, 154(4), 449–468. DOI:10.1086/303244

Chave, J., Navarrete, D., Almeida, S., Alvarez, E., Aragao, L., Bonal, D., Chatelet, P., Silva-Espejo, J. E., Goret, J.-Y., von Hildebrand, P., Jimenez, E., Patino, S., Penuela, M. C., Phillips, O. L., Stevenson, P. & Malhi, Y. 2010. Regional and seasonal patterns of litterfall in tropical South America. Biogeosciences, 7, 43–55. DOI:10.5194/bg-7-43-2010

Chen, H. Y., Brant, A. N., Seedre, M., Brassard, B. W., & Taylor, A. R. 2017. The contribution of litterfall to net primary production during secondary succession in the boreal forest. Ecosystems, 20(4), 830–844. DOI:10.1007/s10021-016-0063-2

Clark, D. A., Brown, S., Kicklighter, D. W., Chambers, J. Q., Thomlinson, J. R., & Ni, J. 2001. Measuring net primary production in forests: concepts and field methods. Ecological applications, 11(2), 356–370. DOI:10.1890/1051-0761(2001)011[0356:MNPPIF]2.0.CO;2

DeForest, J. L., Chen, J., & McNulty, S. G. 2009. Leaf litter is an important mediator of soil respiration in an oak-dominated forest. International journal of biometeorology, 53(2), 127–134. DOI:10.1007/s00484-008-0195-y

Dias, A. T., de Mattos, E. A., Vieira, S. A., Azeredo, J. V., & Scarano, F. R. 2006. Aboveground biomass stock of native woodland on a Brazilian sandy coastal plain: estimates based on the dominant tree species. Forest Ecology & Management, 226(1-3), 364–367. DOI:10.1016/j.foreco.2006.01.020

Dias, A. T. C., & Scarano, F. R. 2007. Clusia as nurse plant. In: Lüttge, U. (Ed.). Clusia: a woody neotropical genus with remarkable plasticity and diversity. pp. 55–71. Springer.

Duffy, P. B., Brando, P., Asner, G. P., & Field, C. B. 2015. Projections of future meteorological drought and wet periods in the Amazon. Proceedings of the National Academy of Sciences, 112(43), 13172–13177. DOI:10.1073/pnas.1421010112

Fauset, S., Freitas, H. C., Galbraith, D. R., Sullivan, M. J., Aidar, M. P., Joly, C. A., Phillips, O. L., Vieira, S. A. & Gloor, M. U. 2018. Differences in leaf thermoregulation and water use strategies between three co‐occurring Atlantic forest tree species. Plant, Cell & Environment, 41(7), 1618–1631. DOI:10.1111/pce.13208

Ferreira, M. L., Silva, J. L., Pereira, E. E., & Lamano-Ferreira, A. P. N. 2014. Litter fall production and decomposition in a fragment of secondary Atlantic Forest of São Paulo, SP, southeastern Brazil. Revista Árvore, 38(4), 591–600. DOI:10.1590/S0100-67622014000400002

Finotti, R., Freitas, S. R., Cerqueira, R., & Vieira, M. V. (2003). A Method to Determine the Minimum Number of Litter Traps in Litterfall Studies. Biotropica, 35(3), 419–421. DOI:10.1111/j.1744-7429.2003.tb00595.x

Franco, A. C., Haag-Kerwer, A., Herzog, B., Grams, T. E., Ball, E., de Mattos, E. A., Scarano, F. R., Barreto, S., Garcia, M. A., & Mantovani, A. 1996. The effect of light levels on daily patterns of chlorophyll fluorescence and organic acid accumulation in the tropical CAM tree Clusia hilariana. Trees, 10(6), 359–365. DOI:10.1007/BF02185639

Fu, R., Yin, L., Li, W., Arias, P. A., Dickinson, R. E., Huang, L., Chakraborty, S., Fernandes, K., Liebmann, B., & Fisher, R. (2013). Increased dry-season length over southern Amazonia in recent decades and its implication for future climate projection. Proceedings of the National Academy of Sciences, 110(45), 18110–18115. DOI:10.1073/pnas.1302584110

Girardin, C. A., Malhi, Y., Doughty, C. E., Metcalfe, D. B., Meir, P., del Aguila‐Pasquel, J., Araujo‐Murakami, A., da Costa, A. C. L., Silva‐Espejo, J. E., & Farfan Amezquita, F. 2016. Seasonal trends of Amazonian rainforest phenology, net primary productivity, and carbon allocation. Global Biogeochemical Cycles, 30(5), 700–715. DOI:10.1002/2015GB005270

Guan, K., Wood, E. F., Medvigy, D., Kimball, J., Pan, M., Caylor, K. K., Sheffield, J., Xu, X., & Jones, M. O. 2014. Terrestrial hydrological controls on land surface phenology of African savannas and woodlands. Journal of Geophysical Research: Biogeosciences, 119(8), 1652–1669. DOI:10.1002/2013JG002572

Guerreiro, Q., Oliveira Junior, R., Ruivo, M., Silva, K., Beldini, T., Guedes, M., Mota, A. F. L., Moraes, B. L. T., Santos, P. R. B., & Duin, I. (2018). Litter production in a natural stand of Brazil nut trees (Bertholletia excelsa Bonpl.). African Journal of Agricultural Research, 13(5), 228–238. DOI:10.5897/AJAR2017.12856

Hay, J. D., & Lacerda, L. D. 1984. Ciclagem de Nutrientes no Ecossistema de Restinga. In: L. D. Lacerda, Araújo, D.S.D., Cerqueira, R. & Turq, B. (Ed.), Restingas: Origem, Estrutura, Processos. pp. 459–473. Niterói: CEUFF.

Hobbie, S. J. 2015. Plant species effects on nutrient cycling: revisiting litter feedbacks. Trends in Ecology and Evolution, 30(6), 357–363. DOI:10.1016/j.tree.2015.03.015

Jackson, J. F. 1978. Seasonality of flowering and leaf-fall in a Brazilian subtropical lower montane moist forest. Biotropica, 38–42. DOI:10.2307/2388103

Lawrence, D. 2005. Regional‐Scale Variation in Litter Production and Seasonality in Tropical Dry Forests of Southern Mexico. Biotropica, 37(4), 561–570. DOI:10.1111/j.1744-7429.2005.00073.x

Malhi, Y., Doughty, C., & Galbraith, D. 2011. The allocation of ecosystem net primary productivity in tropical forests. Philosophical Transactions of the Royal Society B: Biological Sciences, 366(1582), 3225–3245. DOI:10.1098/rstb.2011.0062

Marques, M. C., & Oliveira, P. 2004. Fenologia de espécies do dossel e do sub-bosque de duas Florestas de Restinga na Ilha do Mel, sul do Brasil. Revista Brasileira de Botânica, 27(4), 713–723.

Martinelli, L. A., Lins, S. R., & dos Santos-Silva, J. C. 2017. Fine litterfall in the Brazilian Atlantic forest. Biotropica, 49(4), 443–451. DOI:10.1111/btp.12448

Monteiro, M. M., Giaretta, A., Pereira, O. J., & Menezes, L. F. T. 2014. Composição e estrutura de uma restinga arbustiva aberta no norte do Espírito Santo e relações florísticas com formações similares no Sudeste do Brasil. Rodriguésia, 65(1), 61–72. DOI:10.1590/S2175-78602014000100005

Moraes, R., Delitti, W. B. C., & Struffaldi-de Vuono, Y. 1999. Litterfall and litter nutrient content in two Brazilian Tropical Forests. Brazilian Journal of Botany, 22(1), 09–16. DOI:10.1590/S0100-84041999000100002

Morellato, L. P. C., Talora, D. C., Takahasi, A., Bencke, C. C., Romera, E. C., & Zipparro, V. B. 2000. Phenology of Atlantic rain forest trees: a comparative study. Biotropica, 32(4b), 811–823. DOI:10.1111/j.1744-7429.2000.tb00620.x

Nepstad, D., Moutinho, P., Dias‐Filho, M., Davidson, E., Cardinot, G., Markewitz, D., Figueiredo, R., Vianna, N., Chambers, J., & Ray, D. 2002. The effects of partial throughfall exclusion on canopy processes, aboveground production, and biogeochemistry of an Amazon forest. Journal of Geophysical Research: Atmospheres, 107(D20), LBA 53 - 1–18. DOI:10.1029/2001JD000360

Niinemets, Ü. 2001. Global‐scale climatic controls of leaf dry mass per area, density, and thickness in trees and shrubs. Ecology, 82(2), 453–469. DOI:10.1890/0012-9658(2001)082[0453:GSCCOL]2.0.CO;2

Oliveira-Galvão, A., Galvão, W., & Carvalho, V. 1990. Monitoramento da cobertura vegetal da restinga de Carapebus-Macaé (RJ), a partir de imagens orbitais. In: S. Watanabe (Ed.), II Simpósio de Ecossistemas da Costa Sul e Sudeste Brasileira: Estrutura, função e manejo. pp. 442–454. São Paulo: ACIESP.

Parsons, S., Valdez-Ramirez, V., Congdon, R., & Williams, S. 2014. Contrasting patterns of litterfall seasonality and seasonal changes in litter decomposability in a tropical rainforest region. Biogeosciences, 11(18), 5047–5056. DOI:10.5194/bg-11-5047-2014

Paula, R. R., Pereira, M. G., & Menezes, L. F. T. 2009. Aporte de nutrientes e decomposição da serapilheira em três fragmentos florestais periodicamente inundados na Ilha da Marambaia, RJ. Ciência Florestal, 19(2), 139–148. DOI:10.5902/19805098405

Pereira, M. G., Silva, A. N., Paula, R. R., & Menezes, L. F. T. 2012. Aporte e decomposição de serapilheira em floresta periodicamente inundável na restinga da Marambaia, RJ. Ciência Florestal, 22(1), 59–67.

Pimentel, M. 2002. Variação espacial na estrutura de comunidades vegetais da formação aberta de Clusia no Parque Nacional da Restinga de Jurubatiba, RJ. Doctoral Thesis. Universidade Federal do Rio de Janeiro, Rio de Janeiro, Brazil, Rio de Janeiro.

Pimentel, M. C., Barros, M. J., Cirne, P., Mattos, E. A. d., Oliveira, R. C., Pereira, M. C., Scarano, F. R., Zaluar, H. L. T., & Araujo, D. S. 2007. Spatial variation in the structure and floristic composition of" restinga" vegetation in southeastern Brazil. Brazilian Journal of Botany, 30(3), 543–551. DOI:10.1590/S0100-84042007000300018

Pires, L. A., Britez, R. M. d., Martel, G., & Pagano, S. N. 2006. Produção, acúmulo e decomposição da serapilheira em uma restinga da Ilha do Mel, Paranaguá, PR, Brasil. Acta Botânica Brasílica, 173–184.

Proctor, J., Anderson, J., Fogden, S., & Vallack, H. 1983. Ecological studies in four contrasting lowland rain forests in Gunung Mulu National Park, Sarawak. II. Litterfall, litter standing crop and preliminary observations on herbivory. Journal of Ecology, 71(1), 261–283.

Rapp, M., Santa Regina, I., Rico, M., & Gallego, H. A. 1999. Biomass, nutrient content, litterfall and nutrient return to the soil in Mediterranean oak forests. Forest Ecology & Management, 119(1-3), 39–49. DOI:10.1016/S0378-1127(98)00508-8

Rodarte, A. 2008. Caracterização espacial, temporal e biologia floral das espécies de restinga, com ênfase nos recursos florais. Doctoral Thesis, Universidade Federal do Rio de Janeiro - Museu Nacional, Rio de Janeiro.

Rodrigues, R. F. C. 2014. Estudo da Variação dos Caracteres Estruturais, Anatômicos e Fisiológicos da Folha de Clusia hilariana Schltdl. (Clusiaceae) Relacionados à Sazonalidade no PARNA Restinga de Jurubatiba. Master Thesis, Universidade Federal do Rio de Janeiro - Campus UFRJ-Macaé Professor Aloisio Teixeira, Macaé. p. 68.

Rosado, B. H. P. 2006. A importância da inclusão de diferentes dimensões de variação de características morfo-fisiológicas e de crescimento para o entendimento dos padrões de dominância de plantas de restinga. Master Thesis, Universidade Federal do Rio de Janeiro, Rio de Janeiro. p. 100.

Rosado, B. H. P., & de Mattos, E. A. 2007. Variação temporal de características morfológicas de folhas em dez espécies do Parque Nacional da Restinga de Jurubatiba, Macaé, RJ, Brasil. Acta Botânica Brasílica, 21(3), 741–752.

Rosado, B. H. P., & de Mattos, E. A. 2010. Interspecific variation of functional traits in a CAM‐tree dominated sandy coastal plain. Journal of Vegetation Science, 21(1), 43–54. DOI:10.1111/j.1654-1103.2009.01119.x

Rowland, L., da Costa, A. C., Oliveira, A. A., Almeida, S. S., Ferreira, L. V., Malhi, Y., Metcalfe, D. B., Mencuccini, M., Grace, J., & Meir, P. 2018. Shock and stabilisation following long‐term drought in tropical forest from 15 years of litterfall dynamics. Journal of Ecology, 106(4), 1673–1682. DOI:10.1111/1365-2745.12931

Rowland, L., Malhi, Y., Silva-Espejo, J. E., Farfán-Amézquita, F., Halladay, K., Doughty, C., Meir, P., & Phillips, O. L. 2014. The sensitivity of wood production to seasonal and interannual variations in climate in a lowland Amazonian rainforest. Oecologia, 174(1), 295–306. DOI:10.1007/s00442-013-2766-9

Sayer, E. J. 2006. Using experimental manipulation to assess the roles of leaf litter in the functioning of forest ecosystems. Biological Reviews, 81(1), 1–31. DOI:10.1017/S1464793105006846

Scarano, F. R. 2002. Structure, function and floristic relationships of plant communities in stressful habitats marginal to the Brazilian Atlantic rainforest. Annals of Botany, 90(4), 517–524. DOI:10.1093/aob/mcf189

Silva, A. 2003. Solos e produção de serrapilheira em moitas no Parque Nacional da Restinga de Jurubatiba, RJ. Master Thesis, Universidade Estadual do Norte Fluminense, Campos dos Goytacazes. p. 78.

Talora, D. C., & Morellato, L. P. C. 2000. Fenologia de espécies arbóreas em floresta de planície litorânea do sudeste do Brasil. Brazilian Journal of Botany, 13–26.

R Core Team. 2018. R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing. Retrieved from

Villela, D., de Mattos, E., Pinto, A., Vieira, S., & Martinelli, L. 2012. Carbon and nitrogen stock and fluxes in coastal Atlantic Forest of southeast Brazil: potential impacts of climate change on biogeochemical functioning. Brazilian Journal of Biology, 72(3), 633–642. DOI:10.1590/S1519-69842012000400003

Villela, D. M., Silva, A. P., Bonadiman, G. S. L., Silva, A., & Souza, R. 2020. Clusia hilariana a key species on nutrient cycling in sand dune vegetation thickets. Oecologia australis, in press.

Vitousek, P. M. 1984. Litterfall, nutrient cycling, and nutrient limitation in tropical forests. Ecology, 65(1), 285–298. DOI:10.2307/1939481

Wagner, F. H., Hérault, B., Bonal, D., Stahl, C., Anderson, L. O., Baker, T. R., Becker, G. S., Beeckman, H., Souza, D. B., Botosso, P. C., Bowman, D. M. J. S., Bräuning, A., Brede, B., Brown, F. I., Camarero, J. J., Camargo, P. B., Cardoso, F. C. G., Carvalho, F. A., Castro, W., Chagas, R. K., Chave, J., Chidumayo, E. N., Clark, D. A., Costa, F. R. C., Couralet, C., Mauricio, P. H. S., Dalitz, H., Castro, V. R., Milani, J. E. F., Oliveira, E. C. O., Arruda, L. S., Devineau, J.-L., Drew, D. M., Dünisch, O., Durigan, G., Elifuraha, E., Fedele, M., Fedele, L. F., Filho, A. F., Finger, C. A. G., Franco, A. C., Júnior, J. L. F., Galvão, F., Gebrekirstos, A., Gliniars, R., Graça, P. M. L. A., Griffiths, A. D., Grogan, J., Guan, K., Homeier, J., Kanieski, M. R., Kho, L. K., Koenig, J., Kohler, S. V., Krepkowski, J., Lemos-Filho, J. P., Lieberman, D., Lieberman, M. E., Lisi, C. S., Santos, T. L., Ayala, J. L. L., Maeda, E. E., Malhi, Y., Maria, V. R. B., Marques, M. C. M., Marques, R., Chamba, H. M., Mbwambo, L., Melgaço, K. L. L., Mendivelso, H. A., Murphy, B. P., O’Brien, J. J., Oberbauer, S. F., Okada, Pélissier, R., Prior, L. D., Roig, F. A., Ross, M., Rossatto, D. R., Rossi, V., Rowland, L., Rutishauser, E., Santana, H., Schulze, M., Selhorst, D., Silva, W. R., Silveira, M., Spannl, S., Swaine, M. D., Toledo, J. J., Toledo, M. M., Toledo, M., Toma, T., Filho, M. T., Hernández, J. I. V., Verbesselt, J., Vieira, S. A., Vincent, G., Castilho, C. V., Volland, F., Worbes, M., Zanon, M. L. B., & Aragão, L. E. O. C. 2016. Climate seasonality limits leaf carbon assimilation and wood productivity in tropical forests. Biogeosciences, 13(8). DOI:10.5194/bg-13-2537-2016

Wagner, F., Rossi, V., Stahl, C., Bonal, D., & Herault, B. 2012. Water availability is the main climate driver of neotropical tree growth. PloS one, 7(4), e34074. DOI:10.1371/journal.pone.0034074

Wei, X., & Davidson, G. 1998. Impacts of large-scale timber harvesting on the hydrology of the Bowron River Watershed. Paper presented at the Proceedings of the CWRA 51th annual conference: mountain to sea: human interaction with the hydrologic cycle. Canadian Water Resource Association, Victoria, British Columbia.

Wright, S. J., & Cornejo, F. H. 1990. Seasonal drought and leaf fall in a tropical forest. Ecology, 71(3), 1165–1175. DOI:10.2307/1937384

Zhang, H., Yuan, W., Dong, W., & Liu, S. 2014. Seasonal patterns of litterfall in forest ecosystem worldwide. Ecological Complexity, 20, 240–247. DOI:10.1016/j.ecocom.2014.01.003


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