Reproductive phenology of Euterpe edulis (Arecaceae) along a gradient in the Atlantic rainforest of Brazil
E. R. Castro A , M. Galetti B and L. P. C. Morellato A CA Universidade Estadual Paulista, IB, Departamento de Botânica, Grupo de Fenologia de Plantas e Dispersão de Sementes, Rio Claro, SP, Brazil.
B Universidade Estadual Paulista, IB, Departamento de Ecologia, Laboratório de Biologia da Conservação, CP 199, CEP 13506-900, Rio Claro, SP, Brazil.
C Corresponding author. Email: pmorella@rc.unesp.br
Australian Journal of Botany 55(7) 725-735 https://doi.org/10.1071/BT07029
Submitted: 17 February 2007 Accepted: 28 June 2007 Published: 15 November 2007
Abstract
The palm Euterpe edulis Mart. is one of the dominant tree species in the Atlantic rainforest and considered a key resource for many frugivorous birds. We compared the reproductive phenology of E. edulis in three types of Atlantic rainforest (two lowland forests, restinga and coastal-plain, and a premontane forest) on Cardoso Island (Cananéia, São Paulo, Brazil), aiming to answer the following questions: (i) whether the reproduction of E. edulis is annual and seasonal across the years in the three forest types studied; (ii) what are the environmental factors influencing the reproductive phenology of E. edulis; and (iii) how does the timing of fruiting and fruit production of E. edulis vary among the three forest types? We evaluated the presence of flowers and fruits (immature, unripe and ripe) from August 2001 to July 2004 in 150 individuals (50 per forest), and estimated the number of infructescences with ripe fruits and the production of fruits and seeds by collecting them on the forest floor in the three forest types. Flowering and fruiting of E. edulis were annual and significantly seasonal in the three forest types, with a high synchrony of flowering and medium to low synchrony of fruiting. Flowering peaked in November and December, and immature and unripe fruits peaked in January and March, all during the rainy season. Immature and unripe fruit phases were correlated with the daylength, precipitation and temperature, important factors for fruits development. Ripe fruits peaked in April and May, in the less rainy season, with significant differences in the mean dates among forests. The number of infructescences with ripe fruits and the biomass of fruits and seeds collected on the ground also differed significantly among the forest types, being greater in the restinga and coastal-plain forests, respectively. Differences in productivity were related to palm density in each area and the soil fertility. The complementary fruiting pattern of E. edulis in the forests studied may affect the distribution and abundance of certain frugivorous bird species that feed on their fruits.
Acknowledgements
The authors thank D. Levey and an anonymous reviewer for their comments on the manuscript, Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP, processo no. 01/10300-4) for financial support, Idea Wild for donation of equipment, Instituto Florestal for permission to conduct research in Ilha do Cardoso State Park, Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) for the doctoral fellowship to E. R. Castro, and research productivity fellowship and grant to L. P. C. Morellato and M. Galetti.
Alencar JC
(1994) Fenologia de cinco espécies arbóreas tropicais de Sapotaceae correlacionada a variáveis climáticas na Reserva Ducke, Manaus—AM. Acta Amazonica 24, 161–182.
Barros F,
Melo MMRF,
Chiea SAC,
Kirizawa M,
Wanderley MGL, Jung-Mendaçolli SL
(1991) Flora Fanerogâmica de Ilha do Cardoso. Boletim do Instituto de Botânica 1, 1–184.
Bencke CSC, Morellato LPC
(2002) Estudo comparativo da fenologia de nove espécies arbóreas em três tipos de floresta atlântica no sudeste do Brasil. Revista Brasileira de Botânica 25, 237–248.
Bernardi JVE,
Landim PMB,
Barreto CL, Monteiro RC
(2005) Estudo espacial do gradiente de vegetação do Parque Estadual da Ilha do Cardoso, SP, Brasil. Holos Environment 5, 1–22.
Berry EJ, Gorchov DL
(2004) Reproductive biology of the dioecious understorey palm Chamaedorea radicalis in a Mexican cloud forest: pollination vector, flowering phenology and female fecundity. Journal of Tropical Ecology 20, 369–376.
| Crossref | GoogleScholarGoogle Scholar |
Calderón MEP
(2002) Patrones de caída de frutos en Mauritia flexuosa L.f. y fauna involucrada en los procesos de remoción de semillas. Acta Botanica Venezuelica 25, 1–22.
Callazos ME, Mejía M
(1988) Fenología y poscosecha de milpesos Jessenia bataua (Mart.) Burret. Acta Agronomica 38, 53–63.
Chapman CA,
Chapman LJ,
Struhsaker TT,
Zanne AE,
Clark CJ, Poulsen JR
(2005) A long-term evaluation of fruiting phenology: importance of climate change. Journal of Tropical Ecology 21, 31–45.
| Crossref | GoogleScholarGoogle Scholar |
Charles-Dominique P,
Atramentowicz M,
Charles-Dominique M,
Gerald H,
Hladick A,
Hladick CM, Prevost MF
(1981) Les mammiféres frugivores arboricoles nocturnes d’une forêt guyanaise: inter-relations plantes-animaux. Revue d’Ecologie: La Terre et la Vie 35, 341–435.
Curran LM, Leighton M
(2000) Vertebrate responses to spatio-temporal variation in seed production of mast-fruiting Dipterocarpaceae. Ecological Monographs 70, 101–128.
De Steven D,
Windsor DM,
Putz FE, de León B
(1987) Vegetative and reproductive phenologies of palm assemblage in Panama. Biotropica 19, 342–356.
| Crossref | GoogleScholarGoogle Scholar |
Fisch STV,
Nogueira LR, Mantovani W
(2000) Fenologia reprodutiva de Euterpe edulis Mart. na mata atlântica (Reserva Ecológica do Trabiju, Pindamonhangaba—SP). Revista Biociências 6, 31–37.
Galetti M, Aleixo A
(1998) Effects of the palm heart harvesting on avian frugivores in the Atlantic forest of Brazil. Journal of Applied Ecology 35, 286–293.
| Crossref | GoogleScholarGoogle Scholar |
Galetti M, Fernandez JC
(1998) Palm heart harvesting in the Brazilian Atlantic forest: changes in industry structure and the illegal trade. Journal of Applied Ecology 35, 294–301.
| Crossref | GoogleScholarGoogle Scholar |
Galetti M,
Zipparro V, Morellato LP
(1999) Fruit phenology and frugivory on the palm Euterpe edulis in a lowland atlantic forest of Brazil. Ecotropica 5, 115–122.
Galetti M,
Keuroghlian A,
Hanada I, Morato MI
(2001) Frugivory and seed dispersal by the lowland tapir (Tapirus terrestris) in southeast Brazil. Biotropica 33, 723–726.
Galetti M,
Donatti CI,
Pires AS,
Guimarães PR, Jordano P
(2006) Seed survival and dispersal of an endemic Atlantic forest palm: the combined effects of defaunation and forest fragmentation. Botanical Journal of the Linnean Society 151, 141–149.
| Crossref | GoogleScholarGoogle Scholar |
Ghazoul J,
Liston KA, Boyle TJB
(1998) Disturbance-induced density-dependent seed set in Shorea siamensis (Dipterocarpaceae), a tropical forest tree. Journal of Ecology 86, 462–473.
| Crossref | GoogleScholarGoogle Scholar |
Guilherme FAG,
Morellato LPC, Assis MA
(2004) Horizontal and vertical tree community structure in a Atlantic rain forest, southeastern Brazil. Revista Brasileira de Botânica 27, 725–737.
Henderson A,
Fisher B,
Scariot A,
Whitaker Pacheco MA, Pardini R
(2000) Flowering phenology of a palm community in a Central Amazon. Brittonia 52, 149–159.
| Crossref | GoogleScholarGoogle Scholar |
Janzen DH
(1974) Tropical blackwater rivers, animals and mast fruiting by the Dipterocarpaceae. Biotropica 6, 69–103.
| Crossref | GoogleScholarGoogle Scholar |
Küchmeister H,
Silberbauer-Gottsberger I, Gottsbergerger G
(1997) Flowering, pollination, nectar standing crop, and nectaries of Euterpe precatoria (Arecaceae), an Amazonian rain forest palm. Plant Systematics and Evolution 206, 71–97.
| Crossref | GoogleScholarGoogle Scholar |
Loiselle BA, Blake JG
(1991) Temporal variation in birds and fruits along on elevational gradient in Costa Rica. Ecology 72, 180–193.
| Crossref | GoogleScholarGoogle Scholar |
Lugo AE, Frangi JL
(1993) Fruit fall in the Luquillo Experimental Forest. Puerto Rico. Biotropica 25, 73–84.
| Crossref | GoogleScholarGoogle Scholar |
Malizia LR
(2001) Seasonal fluctuations of birds, fruits, and flowers in a subtropical forest of Argentina. The Condor 103, 45–61.
| Crossref | GoogleScholarGoogle Scholar |
Martén S, Quesada M
(2001) Phenology, sexual expression, and reproductive success of the rare neotropical palm Geonoma epetiolata. Biotropica 33, 596–605.
Melo MMRF, Mantovani W
(1994) Composição florística e estrutura do trecho de mata atlântica de encosta, na Ilha do Cardoso (Cananéia, SP, Brazil). Boletim do Instituto de Botânica 9, 107–157.
Mikich SB, Silva SM
(2001) Composição florística e fenologia das espécies zoocóricas de remanescentes de floresta estacional semidecidual no centro-oeste do Paraná, Brazil. Acta Botânica Brasílica 15, 89–113.
| Crossref | GoogleScholarGoogle Scholar |
Miller C
(2002) Fruit production of the ungurahua palm (Oenocarpus bataua subsp. bataua, Arecaceae) in an indigenous managed reserve. Economic Botany 56, 165–176.
| Crossref | GoogleScholarGoogle Scholar |
Morellato LPC,
Talora DC,
Takahasi A,
Bencke CC,
Romera EC, Zipparro VB
(2000) Phenology of Atlantic rain forest trees: a comparative study. Biotropica 32, 811–823.
| Crossref | GoogleScholarGoogle Scholar |
Otero-Arnaiz A, Oyama K
(2001) Reproductive phenology, seed set and pollination in Chamaedorea alternans, an understorey dioecious palm in a rain forest in Mexico. Journal of Tropical Ecology 17, 745–754.
Peres CA
(1994) Composition, density and fruiting phenology of arborescent palms in a Amazonian Terra Firme Forest. Biotropica 26, 285–294.
| Crossref | GoogleScholarGoogle Scholar |
Peres CA
(2000) Identifying keystone plant resources in tropical forests: the case of gums from Parkia pods. Journal of Tropical Ecology 16, 287–317.
| Crossref | GoogleScholarGoogle Scholar |
Pizo MA, Simão I
(2001) Seed deposition patterns and the survival of seeds and seedlings of the palm Euterpe edulis. Acta Oecologica 22, 229–233.
| Crossref | GoogleScholarGoogle Scholar |
Pizo MA,
Von Allmen C, Morellato LPC
(2006) Seed size variation in the palm Euterpe edulis and the effects of seed predators on germination and seedling survival. Acta Oecologica 29, 311–315.
| Crossref | GoogleScholarGoogle Scholar |
Rathcke B, Lacey EP
(1985) Phenological patterns of terrestrial plants. Annual Review of Ecology and Systematics 16, 179–214.
| Crossref | GoogleScholarGoogle Scholar |
Ratsirarson J, Silander JA
(1996) Reproductive biology of the threatened Madagascar triangle palm: Neodypsis decaryi Jumelle. Biotropica 28, 737–745.
| Crossref | GoogleScholarGoogle Scholar |
Rodriguez M,
Olmos F, Galetti M
(1993) Seed dispersal by tapir in southeastern Brazil. Mammalia 57, 460–461.
Rosa L,
Castellani TT, Reis A
(1998) Biologia reprodutiva de Butia capitata (Martius) Beccari var. odorata (Palmae) na região de restinga do município de Laguna, SC. Revista Brasileira de Botânica 21, 131–142.
Ruiz RR, Alencar JC
(2004) Comportamento fenológico da palmeira patauá (Oenocarpus bataua) na reserva florestal Adolpho Ducke, Manaus, Amazonas, Brasil. Acta Amazonica 34, 553–558.
| Crossref | GoogleScholarGoogle Scholar |
Sakai S,
Momose K,
Yumoto T,
Nagamisu T,
Nagamisu H,
Hamid AA, Nakashizuka T
(1999) Plant reproductive phenology over four years including an episode of general flowering in a lowland Dipterocarp forest, Sarawak, Malaysia. American Journal of Botany 86, 1414–1436.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Scariot AO, Lleras E
(1991) Reproductive biology of the palm Acrocomia aculeata in central Brazil. Biotropica 23, 12–22.
| Crossref | GoogleScholarGoogle Scholar |
Scariot AO, Lleras E
(1995) Flowering and fruiting phenologies of the palm Acrocomia aculeata. Patterns and consequences. Biotropica 27, 168–173.
| Crossref | GoogleScholarGoogle Scholar |
Sist P
(1989) Peuplement et phénologie dês palmier em forêt guyanaise (Pist et Saint Elle). Revue d’Écologie (La Terre et La Vie) 44, 113–151.
Somanathan H, Borges RM
(2000) Influence of exploitation on population structure, spatial distribution and reproductive success of dioecious species in a fragment cloud forest in India. Biological Conservation 94, 243–256.
| Crossref | GoogleScholarGoogle Scholar |
Souza AF, Martins FR
(2004) Population structure and dynamics of a neotropical palm in fire-impacted fragments of the Brazilian Atlantic forest. Biodiversity and Conservation 13, 1611–1632.
| Crossref | GoogleScholarGoogle Scholar |
Stevenson PR
(2004) Phenological patterns of woody vegetation at Tinigua Park, Colombia: methodological comparisons with emphasis on fruit production. Caldasia 26, 125–150.
Sugyama M
(1998) Estudo de florestas da restinga da Ilha do Cardoso, Cananéia, São Paulo, Brazil. Boletim do Instituto de Botânica 11, 119–159.
Tabarelli M,
Silva MJC, Gascon C
(2004) Forest fragmentation, synergisms and the impoverishment of neotropical forest. Biodiversity and Conservation 13, 1419–1425.
| Crossref | GoogleScholarGoogle Scholar |
Talora DC, Morellato LPC
(2000) Fenologia de espécies arbóreas em floresta de planície litorânea do sudeste do Brazil. Revista Brasileira de Botânica 23, 13–26.
van Schaik CP,
Terborgh JW, Wright SJ
(1993) The phenology of tropical forest: adaptive significance and consequences for primary consumers. Annual Review of Ecology and Systematics 24, 353–377.
Voeks RA
(2002) Reproductive ecology of the piassava palm (Attalea funifera) of Bahia, Brazil. Journal of Tropical Ecology 18, 121–136.
Von Allmen C,
Morellato LPC, Pizo MA
(2004) Seed predation under high seed density condition: the palm Euterpe edulis in the Brazilian Atlantic forest. Journal of Tropical Ecology 20, 471–474.
| Crossref | GoogleScholarGoogle Scholar |
Wheelwright NT, Orians GH
(1982) Seed dispersal by animals: contrasts with pollen dispersal, problems of terminology, and constraints on evolution. American Naturalist 119, 402–413.
| Crossref | GoogleScholarGoogle Scholar |
Wright SJ, van Schaik CP
(1994) Light and the phenology of tropical trees. American Naturalist 143, 192–199.
| Crossref | GoogleScholarGoogle Scholar |
Zhang S, Wang L
(1995) Comparison of three fruit census methods in French Guiana. Journal of Tropical Ecology 11, 281–294.