Revista Chilena de Historia Natural 69: 357-363, 1996 Bird frugivory and the fate of seeds of alba () in the Chilean matorral

Frugivorfa por aves y el destino de !as semillas de (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 of the Chilean matorral. Although the removal of the pericarp of 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 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 is a crucial process through- show that the study of the ecological factors out the life cycle of (Solbrig I 980). It which mediate -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, ) 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- . perse its seeds in the Chilean matorral. Spe- cifically, we evaluated how 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. Experiments were performed and June, respectively). In July 1992, no from April to September 1992 under lab differences between treatments were detected conditions. Ten seeds per replicate, number of (Wilcoxon, Z = 0.9, P = 0.16; Table 1). replicates n = 10. The asterisc (*) indicates the During August and September 1992, ger- slope of the regresion curve estimated along the mination was zero in both treatments (Table time for each treatment 1). Overall, bird-dispersed seeds tended to Porcentaje de germinaci6n (promedio ± I ee) loose germination capacity at a higher rate para semillas dispersadas por aves y por gravedad en CrJplocarya alba. Los experimentos fueron realizados desde than gravity-dispersed seeds (slope compari- abril a septiembre 1992 bajo condiciones de laboratorio. son test, t = - 5.34, d.f. = 76, P < 0.005, Diez semillas por replica. numero de replicas n = 10. El Table 1). asterisco indica la pendiente de la curva de regresi6n a lo largo del tiempo para cad a tratamiento

Fate of seeds and seedlings Months Gravity-dispersed seeds Bird-disrersed seeds

April 56.0 ± 4.7 100.0 ± 0.0 Seed predation was significantly lower in May 55.5 ± 5.2 81.0 ± 2.3 the dense habitat compared to sparse habitats June 8.0 ± 2.0 20.0± 2.6 (proportion tests, Z 8.6, P < 0.0004; Fig- July 7.0 ± 2.6 3.0 ± 1.5 = - August 0.0 0.0 ure 1). Fungi were the most conspicuous September 0.0 0.0 seed consumers in dense habitats (82% of consumption); birds and rodents were most * Slope -1.9 ± 0.2 -3.5 ± 0.1 360 BUSTAMANTEET AL.

a) Dense habitat

P(G}=0.68 P ( S n G} 0. 15 0 =

P(G n R} =0.11 p (SI } =I

P( Son G.A R)~0.05

b) Sparse habitat

P(S0 nG}=0.03

P (G n R}= 0.09

P(S0 nGnR} = 0.02

Fig. 1: Fate diagrams from bird-dispersed seeds of Cryptocarya alba in a) dense habitats and b) sparse habitats, Chilean matorral. The initial number of seeds disposed

) in the field for both treatments was 600. P(S 0 = the probability of a seed to survive predation, P(G) = the probability of a seed to germinate, P(R) = the probability that a seed recruit to seedling stage, P(S 1) = probability that a seed that failed to germinate survives, P(S 2) =the probability a seedling to survive at the end of the Summer. Diagrarnas de destino para semillas de Cryptocarya alba en a) habitat denso y b) habitat ralo, matorral ) = chileno. El numero inicial de sernillas dispuestas en el campo para ambos tratamientos fue de 600. P(S 0 probabilidad de una semillas de sobrevivir a la depredaci6n, P(G) = probabilidad de una semilla de gerrninar, P(R) = probabilidad de una semilla de reclutar al estado de plantula, P(S 1) = probabilidad que una semilla que no germin6, sobreviva, P(S 2) = probabilidad de una plantula de sobrevivir hasta fines del verano. nificantly during the first months but later, desiccation. It is possible that exposed seeds this effect decreases to become zero (Figure lose water in such a way that they in turn 1). This results may be explained presumably lose germination capacity faster than those by the protection of the pericarp against seeds with the intact pericarp. That is, if BIRD FRUGJVORY IN CRYPTOCARYA ALBA 36I bird-dispersed seeds are transported when potential for recolonization to such habitats water conditions for germination are critical, (Fuentes et al. I 983, Fuentes et al. 1984, the potential positive effect on germination, Fuentes et al. 1986). The death of the 100% may become irrelevant lately. In the Chilean of Cryptocarya alba seedlings in sparse matorral, the duration of the rainy season is habitats (Figure I b), corroborates this as- highly variable among years (Di Castri & sertion. However, the death of the 100% of Hajek 1976, Espinoza et al. I 988). More- seedlings in dense habitats (Figure I a), over, the duration of the dispersal phase of shows that the regeneration process inside Cryptocarya alba is variable among years the remnants forests is severely precluded as well (R.O. Bustamante pers. obs.). This as well. Regeneration studies in the matorral may result, in a temporal disacoupling be- suggest that this process is an episodic event tween dispersal of seeds and rains: the frac- that occurs during extremely rainy years tion of seeds dispersed by birds before (Fuentes et al. 1986). As during I 992 precip- precipitations will die by desiccation, itations were abundant, the lack of regenera- irrespective of an initial potential beneficial tion both in dense and sparse habitat suggests effect of birds on seed germination. They additional constraints for regeneration of will affect seed germination positively only Cryptocarya alba and other shade-tolerant to the fraction of seeds that are dispersed species in the chilean matorral. The after the occurrence of precipitations. This anthropogenic activities have changed the hypothesis is amenable to be tested by field matorral from a continuous cover of native experiments. vegetation to a discontinuous and isolated fragments of native vegetation, surrounded Fate of seeds and seedlings by a seminatural matrix (Fuentes & Hajek 1979, Fuentes I994). We suggest a strong Birds disperse seeds both in the dense and edge effect (sensu Murcia I 995), which is in the sparse habitats. Once seeds arrive to expressed in (i) modifications of the abiotic sparse habitats, they have a lower survival conditions inside the remnant fragments and and germination probability (Figure I) due to (ii) the intrusion of herbivores (rabbits, cows factors such as seeds predators and water and horses). This changes induced by the stress. Interestingly, P(R), the probability that fragmentation of the matorral should reduce a seed recruit to seedling stage, was higher in the potential for regeneration of Cryptocarya sparse habitats (Fig. I). It is possible that the alba and other similar species even during conditions of higher luminosity, typical of rany years. Further rearch is needed to sparse habitats in the Chilean matorral Del evaluate the magnitud of the edge effect Pozo et al. 1989) increased seedling recruit- during wet and dry years in the matorral and ment initially, in a similar way as docu- to elucidate its importance for the regenera- mented for some shade-tolerant tree species tion of this species. growing in large gaps in forests (Becker & An alternative mode of regeneration Wong 1985, Murray 1988). P(G and R) were seems to be the vegetative reproduction from similar in both dense and sparse habitat lignotubers (Montenegro et al. 1983). In fact, (Figure I), reflecting a compensatory effect vegetative reproduction has been considered in demographic processes that is, higher an important source of plant regeneration P(G) but lower P(R) in dense habitats in once human disturbances remove the cover contrast to a lower P(G) but a higher P(R) in of the matorral (Araya & Avila 1981, Mon- sparse habitat. Overall, the lower P(S and G tenegro et al. 1983). This reproductive mode and R) observed in the sparse habitat (Fig. may be efficient for rapid regrowth (Mon- I), suggest that seed predation in sparse tenegro et al. 1983). However, it may be habitat is so intense that is able to reduce deleterious for the plant populations in the seedling recruitment even in presence of the long term, because genetic variability may be compensatory effect detected in this study. severely eroded. Seedling survival in sparse habitats is In summary, the effect of frugivores birds constrained by severe mortality attributable on Cryptocarya alba seeds will depend on to desiccation and herbivory, thus precluding when and where they disperse the seeds. 362 BUSTAMANTEET AL.

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