Massive Seed Predation of Pseudobombax Grandiflorum (Bombacaceae) by Parakeets Brotogeris Versicolurus (Psittacidae) in a Forest Fragment in Brazil’

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BlOTROPlCA 34(4): 613-615 2002

Massive Seed Predation of Pseudobombax grandiflorum (Bombacaceae) by Parakeets Brotogeris versicolurus (Psittacidae) in a Forest Fragment in Brazil’

ABSTRACT Here we report massive seed predation of Pseudobombax grandzfirum (Bombacaceae) by Botogeris versicolurus (Psitta- cidae) in a forest fragment in Brazil. The intensity of seed predation was very high when compared to other studies in continuous forest, perhaps resulting from a scarcity of resources in such areas. This scarcity may limit the range of parrot’s diet to a few plant species. It suggests that studies of Psittacidae seed predation may be important for conservation of some plants in fragments.

Kq word: Atlantic Forest; Brazil; Brotogeris versicolurus; firest papentation; Pseudobombax grandiflorum; Psitta- riake; seed preaktion.

A SUBSTANTIAL PORTION OF SEED CROP is lost to predators in every fruiting event Uanzen 1972, 1981; Howe 1980; Schupp 1988) and because of this extensive mortality, seed predation is one of the major ecological and evolutionary forces affecting individual plants, populations, and communities (Schupp 1988). Psittacids (parrots, macaws, and parakeets) have been recognized as important pre-dispersal seed predators in the Neotropics Uanzen 1972, Higgins 1979, Howe 1980, Janzen 1981, Galetti & Rodrigues 1992, Coates-Estrada et al. 1993). The diet of most species consists of fruits, seeds, and flowers, which are taken in treetops or on the ground (Forshaw 1981, Roth 1984, Galetti 1993); however, despite their potential impacts on plant recruitment, very few data are available on the intensity of seed predation by parrots, especially in fragmented forests (Higgins 1979, Galetti & Rodrigues 1992). The Canary-winged Parakeet Brotogeris uersicolurw is a small, long-tailed psittacid that is widely distributed in South America. It inhabits cerrado, gallery forests, parts of the Atlantic forest (Sick 1997), and disturbed areas (Paranhos 1995) in eastern and southern Brazil from Cead, Maranh50, southern Par& to south Rio de Janeiro, western S~OPaulo, Mato Grosso, and northern and eastern Bolivia, Paraguay, and northern Argentina (Forshaw 1981). It is a generalist species and its diet is composed of a wide variety of pulp, seeds, flowers, and some insects. Paranhos (1995) observed Canary-winged Par- akeets feeding on different items of 45 plant species from 16 families. Bombacaceae plants are common items in the diets of most Brazilian psittacids. Brotogeris uersicolurus has been observed consuming seeds and flowers of Chorisia speciosa and Psdbombax sp. (Paranhos 1995). Brotogeris tirica and Qrrhura fiontalis consume seeds of Spirotheca passrfiroides and flowers of Psdbombax sp. (Galetti 1997). Brotogeris chrysopterw are known to eat fruits of Bombax spp. and flowers of Erioteca globosa (Roth 1984). Pionus mavimiliani has been observed consuming flowers of C. speciosa and Pseudobombax grandzfirum (Galetti 1993). Pseudobombax grandfirum (Bombacaceae) is a semi-deciduous tree 15-25 m in height that occurs in the Atlantic Forest from Rio de Janeiro, Minas Gerais to S5o Paulo, Mato Grosso do Sul. The fruit of I? grandzfirum is a dehiscent “pod.” Mature pods are found from September to October and the seeds, covered with cotton, are typically wind-dispersed (Lorenzi 1998). Here we report a massive seed predation of I? grandfirum by the Canary-winged Parakeet in a small forest fragment in southeast Brazil. The observations were carried out in a 9.5 ha semideciduous forest fragment located near S5o Carlos, southeast Brazil (21”55’S, 47”55’W). This area is surrounded by pasture and the region is completely disturbed, with the few remaining small patches of cerrado or semideciduous forest surrounded by pasture or sugarcane. Sixty hours of focal observations were performed on five l? grandfirurn from 0600 to 1800 h during 6 to 26 September 2000. Everytime that we observed a parakeet visiting the plant, we recorded the time

Received 24 May 2001; revision accepted 7 August 2002. 614 Francisco, Lunardi, and Galetti

of the visit, group size, the time spent by parakeets foraging on seeds, and the number of seeds preyed upon by parakeets (Galetti 2002). Bird activities could be observed accurately from observation points because plants lose their leaves in the fruiting period. We estimated the number of seeds by counting the number of fruits and multiplying the mean number of seeds in each fruit calculated from a sample of nine fruits. The I? grandzyorum trees produced 8-146 fruits (2= 67.2 ? 54.87, N = 5). The fruits were 23.66 2 2.29 cm in length (N = 6) and 37.75 ? 4.92 mm in width (N = 6). These fruits contained an average of 171.55 ? 74.70 seeds (N = 9). Therefore, the estimated number of seeds per plant was 11,528 ? 9,412 (N = 5). The seeds of I? grandrflorum were 6.45 t 0.22 rnm in length (N = 20), 5.54 ? 0.30 mm in width (N= 20), and weighed 0.097 t 0.009 g (N= 20). In 60 hours of focal observations on five different plants, we recorded 157 bird visits by parakeets, with an average of 2.61 ? 4.07 visits/hour (N = 60). The birds visited the plants alone or in flocks of up to 11 individuals (2 = 2.81 2 1.93, N = 58). The time spent foraging on plants varied from 20 seconds to 42 minutes 38 seconds (2 = 615.73 ? 771.04 sec, N = 23). Parakeets opened the fruits with their beaks, tearing away pieces of the wall and exposing the seeds for consumption. Only immature fruits were consumed and we did not observe birds dropping entire seeds while feeding. The number of visits on each plant was marginally correlated with the number of pods in the trees (Spearman’s rank correlation test: r, = 0.90, P = 0.083, N = 5). The average number of visits per plant per day was 31.4 t 25.44 (N = 5) and the birds consumed an average of 8.40 t 10.46 seeds/visit (N = 27). Thus, we estimated that parakeets consumed 263.76 seeds/plant/day, which represented 2.29 percent of the total fruit crop. Therefore, parakeets could have consumed the entire fruit crop in 43.7 days. Although we do not know exactly when parakeets started to consume seeds, opened pods remained on branches, and at the end of this study, we did not find any available seeds on pods in the five I? grandzyorum observed. Predation occurred while fruits were still unripe and no dehiscent pods were observed under sampled trees. Thus, we assumed that 100 percent of the seeds were removed. This reflects a high impact of this psittacid in a wind-dispersed tree. Abiotic seed dispersal fruits are impacted heavily by seed predation from vertebrates (especially psittacids and monkeys) in semi-deciduous forest fragments (Galetti & Rodrigues 1992, Galetti & Pedroni 1994). The intensity of seed predation on I? grandiJ9orum by B. versicolurus was very high when compared to our studies on parrot seed predation (Galetti & Rodrigues 1992). It seems that fruits in forest fragments have higher seed predation by psittacids than in continuous forests. For example, the intensity of seed predation by Amazona farinosa and A. autumnalis on Tetragastris panamensis (Burseraceae) was estimated to be 6.4 percent of the seed crop in Panama (Howe 1980). Pionus mestruus consumed ca 8 percent of the fruit crop of Albizia sp. in Brazilian Amazonia, while in forest fragments, I! mavimiliani destroyed 20 percent of the fruit crop of Inga spp. (Galetti & Rodrigues 1992) and other parrots consumed 10 percent of the fruit crop of Sterculia apetala (Janzen 1972). The high rate of seed predation by parrots in small forest fragments may represent the scarcity of resources in such areas, limiting the range of the parrots’ diet to very few plant species (Galetti & Rodrigues 1992). For example, Bombacaceae seeds comprised only 4 percent of the diet of B. tirica in a continuous Atlantic forest (Galetti 1997). Several psittacid species, such as Brotogeris spp. and Aratinga leucophtalmus, are positively affected by deforestation, increasing their densities in agricultural areas (MG, pers. obs.); however, all these species fed upon seeds in both the agricultural crops and native forested species found in the adjacent fragments (Galetti 1993). Our study showed that seed predation by parakeets may have a high impact on seed dispersal that will ultimately affect plant recruitment in such fragmented areas. Previous studies have reported much higher seed predation by rodents in small fragments and edges in larger forests and interior (Santos & Telleria 1994, 1997; Jules & Rathcke 1999). Studies on pre-dispersal seed predation by vertebrates, however, are scarce. The high consumption of I? grandzyorum seeds by parakeets seems to dramatically affect the demog- raphy of this wind-dispersed tree, suggesting that studies about Psittacidae seed predation may be of hndamental importance for the conservation of some plant species in fragmented habitats.

We are grateful to C. R. Francisco for permission to work in the study area. M. R. Francisco was Notes 615 supported by CAPES, V. 0. Lunardi by CAPES and PIBIC/CNPq, and M. Galetti by FAPESP and CNPq. We also thank D. Garcia and an anonymous reviewer for their comments on the manuscript.

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Mercival Roberto Franclsco2, Wtor de Oliveira Lunardl Programa de P6s-Graduaqlo em Ecologia e Recursos Naturais Universidade Federal de Slo Carlos Departamento de Gen6tica e Evoluplo Rod. Washington Luis, km 235, 13565-905 P.O. Box 676, Slo Carlos, Slo Paulo, Brazil and Mauro Galetti3 Plant Phenology and Seed Dispersal Research Group Departamento de Ecologia, Universidade Estadual Paulista 13506-900 Rio Claro. SP. Brazil Corresponding author; e-mail: [email protected] 3 e-mail: [email protected]