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Bird Frugivory and the Fate of Seeds of Cryptocarya Alba (Lauraceae) in the Chilean Matorral

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Bird Frugivory and the Fate of Seeds of Cryptocarya Alba (Lauraceae) in the Chilean Matorral Revista Chilena de Historia Natural 69: 357-363, 1996 Bird frugivory and the fate of seeds of Cryptocarya alba (Lauraceae) in the Chilean matorral Frugivorfa por aves y el destino de !as semillas de Cryptocarya alba (Lauraceae) en el matorral chileno RAMIRO 0. BUSTAMANTE1, ALAN WALKOWIAK2, CAROLINA A. HENRIQUEZ1 and ITALO SEREY1 1Departamento de Ciencias Ecologicas, Facultad de Ciencias,Universidad de Chile, Casilla 653, Santiago. Chile. E-mail:[email protected] 2Empresa Electrica Pangue S.A., Avda. Suecia 488, Providencia, Santiago ABSTRACT We evaluated the effect of frugivorous birds on the germination and establishment of Cryptocarya alba, a common tree of the Chilean matorral. Although the removal of the pericarp of fruits increased germination rate. bird-dispersed seeds loose germination capacity at a higher rate than those dispersed by gravity alone. Seeds dispersed toward dense habitats survived, germinated and established at a higher proportion than those dispersed in sparse habitats. However, the survival of established seedlings was null at the end of summer, in both types of habitat. We conclude that seedling germination and establishment is more likely when dispersal is coupled with the rain season and it occurs in dense habitats. We discuss the implications of these effects of frugivores in the context of the regeneration processes of this species in the Chilean matorral. Key words: dispersal, germination, regeneration, seedling establishment, seed predation. RESUMEN Nosotros evaluamos el efecto de !as aves frugfvoras en la germinacion y cstablccimiento de Cr)ptocarya alba, un árbol común del matorral chileno. Aunque la remocion del pericarpo de Ios frutos incremento !as tasas de germinacion, !as semillas dispersadas por aves perdieron la capacidad de germinacion a una tasa mayor que !as dispersadas por gravedad solamente. Las semillas dispersadas a habitats densos sobrevivieron, germinaron y se establecieron en una mayor proporcion que !as dispersa- das a habitats ralos. Sin embargo, la sobrevivencia de plantulas establecidas fue nula al finalizar el verano en ambos tipos de habitats. Nosotros concluimos que la gcrminacion de semillas y establecimiento de plantulas es más posible cuando la dispersion se encuentra asociada a la época de lluvias y ocurre en parches densos de vegetacion del matorral chileno. Finalmente, discutimos !as implicancias de Ios efectos de !as aves frugfvoras en el contexto de la regeneracion de esta especie en el matorral chileno. Palabras clave: deprcdacion de semillas. dispersion. establecimiento de plantulas, germinacion, regeneracion. INTRODUCTION I 985, Loiselle 1990, Jordano 1992, Stiles 1992, Hen·era et al. 1994). Recent evidences Seed dispersal is a crucial process through- show that the study of the ecological factors out the life cycle of plants (Solbrig I 980). It which mediate plant-frugivorous bird inter- allows an increase of germination and estab- action poses a more complex picture about lishment away parent plants (Howe & the nature of this biotic interaction. For Smallwood 1982), and subsequently the example, clumps of seeds deposited in faeces colonization of plants to unoccupied habitats and regurgitates may attract predators which (Harper I 977, Jordano 1992). Among the reduces seed survival (Janzen 1982). The diverse set of dispersal agents, the effects of passage of seeds through the animal guts frugivores (birds, mammals) on plant popula- may kill insect predators, compensating seed tion structure and demography have received survival (Janzen et al 1985, Hauser 1994, a particular attention (Herrera & Jordano Miller 1994). Additionally, seeds may be 1981, Pratt & Stiles 1983, J ohnson et al. deposited in microsites where germination (Received 24 January 1996; accepted 16 May 1996; managed by Francisco Bozinovic) 358 BUSTAMANTE ET AL. and establishment are unlikely, reducing nal Park (32° 57' S, 71° 08' W), located in recruitment (Bustamante et al. 1992). Clearly, the mediterranean ecosystem of central frugivory is a complex interaction whose ef- Chile. The vegetation in this zone is sclero- fects on seed and seedling demography will phyllous forest (Villaseiior & Serey 1980/81) be dependent of the ecological context where where it is possible to recognize two con- it takes place (Thompson 1982, Greenwood trasting habitats: sparse habitats (42% cover; 1985). Here, we show an example where the Maldonado 1990), dominated by Baccharis outcome of frugivores on plant recruitment is linearis (R.et P.) and Muehlenbeckia has- conditioned by the biotic and abiotic context tulata (J.E.Sm.) Johnst. and dense habitats where it takes place. The study system is the (95% of cover; Maldonado 1990) with Cryp- tree Cryptocarya alba (Mol.) Looser (Laura- tocarya alba and Peumus boldus as dominant ceae) and the frugivorous birds which dis- trees. perse its seeds in the Chilean matorral. Spe- cifically, we evaluated how fruit consump- Germination tests tion by birds affect seed germination. Moreover, we monitored the fate of bird- During April 1992, we collected propagules dispersed seeds in open versus closed previously dispersed by birds (without habitats. Finally, we discussed to what extent pericarp) and by gravity (ripe fruits and with the effect of birds on germination is reflected the intact pericarp). We took special care that in seed and seedling demography. all the selected propagules were not damaged by physical and/or biotic causes. METHODS Propagules were stored in mesh bags and maintained in the laboratory under controlled Cryptocarya alba is a sclerophyllous tree temperature (20° C) and relative air humidity distributed through the south-facing slopes (40-50%). We performed six experiments, and humid ravines of the Chilean matorral once a month, between April and September, (Armesto & Martfnez 1978). Its fruits are by taking random samples of seeds from the red, one-seeded drupes (1-2 cm long) with a mesh bags. We compared germination be- thin pericarp that disperse from March to tween bird-dispersed versus gravity-fallen July. Dispersal agents are foxes (Pseuda- propagules by disposing them in Petri dishes lopex sp.; Jaksic et al. 1980, Armesto et al. with filter paper, in dark conditions, 15° C 1987) and birds (Calumba araucana Lesson, and water ad libitum. We used 10 Petri Mimus thenca (Molina), Pyrope pyrope dishes per treatment and 10 seeds per Petri (Kittlitz), Turdus falklandii Quoy et Gay- dish. We recorded the number of germination nard; Bustamante 1992). Many fruits fall each 2 days, from the first day after initiated passively beneath parent plants as well the experiment. Observations were perform- (Bustamante 1992). Bird-dispersed seeds are ed for 65 days. After this time, no evidence easily identified in the field because they of further germination was detected. are regurgitated in clumps, intact and without pericarp under perch trees (Bustamante et al. Fate of seeds and seedlings 1993 ). Cryptocarya alba is considered a late- successional species (Armesto & Pickett In order to evaluate the fate of seeds and 1985), that germinates and establishes under seedlings, we focused only on bird-dispersed the canopy of the sclerophyllous forests. The seeds because they are distributed in both seeds are considered recalcitrant because closed and sparse habitats; fallen-gravity they lose viability and die up during the fifth propagules were never found in sparse or sixth months after dispersal (Bustamante habitats. During June 1992, we distributed et al. 1992). 600 seeds dispersed by birds in 30 groups, 20 seeds per groups, randomly disposed on Study area the ground. This density is appropriate for experiments as birds generate dense patches Experiments were performed between April of seeds under perch trees (R.O. Bustamante, 1992 to March 1993 at La Campana Natio- obs. pers.). This procedure was repeated both BIRD FRUGIVORY IN CRYPTOCARYA ALBA 359 in sparse and dense habitats. The total area important in sparse habitats ( 69% of con- we used for the experiments was about 0.5 sumption; Figure 1). Seeds germinated in ha. per habitat-type. In January I 993, we higher proportion in dense habitats than in counted the number of seeds removed or sparse habitats (proportion test, Z = 3.6, P = destroyed by fungus, the number of 0.0006; Figure 1). The proportion of seeds germinated seeds, the number of seeds that which established as seedling, P(R), was germinated and died, and the number of higher in sparse habitats (proportion test Z seeds that were established as seedlings. We = 1.78, P = 0.03; Fig. 1). The proportion of assumed that the responsible agents of seed seeds that germinated and established as removal were birds and rodents (see also seedling, P(G and R), was similar in both V asquez et al. 1995 for a detailed study of habitat-types (proportion test, Z = -0.85, P = seed predation by birds and rodents). By the 0.27; Fig. 1). A global comparison, that is end of the summer (March 1993), we count- P(So and G and R) detected a significant ed the number of surviving seedlings. This difference in the dense habitats in relation information was analyzed by using fate to sparse habitat (proportion test, Z = -6.80, diagrams (sensu Price & Jenkins 1986). This P < 0.0001, Figure 1). Finally, the 100% of ): method enabled the estimation of: (i) P(S 0 seedlings died by dessication and herbivory the probability of a seed to survive predation; at the end of the summer in both habitat- (ii) P(G): the probability of a seed to ger- types (Figure 1). ): minate; (iii) P(S 1 the probability of a seed that failed to germinate survives; (iv) P(R): the probability that a seed recruit to seedling DISCUSSION stage; and (v) P(S?): the probability of sur- vival of a seedling at the end of the Summer. Birds and seed germination Birds affected the germination of Cryptoca- RESULTS rya alba seeds in a subtle way. The removal of pericarp increases germination sig- Germination tests Bird-dispersed seeds germinated at a higher TABLE I proportion than gravity-dispersed seeds Germination percentage (mean± 1 se) for (Wilcoxon, Z = 3.8, P << 0,001; Z = 3.4, P gravity-dispersed and bird-dispersed seeds in << 0.001; Z = 2,2, P < 0.05 for April, May Cryptocarya alba.
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