Does mammal community composition control recruitment in neotropical forests? Evidence from Panama

Ecology, April, 1997 by Nigel M. Asquith, S. Joseph Wright, Maria J. Clauss

Ecologists have long debated the role of top-down and bottom-up forces in structuring biological communities (Hairston et al. 1960, Paine 1966). Although top-down effects have more often been observed in aquatic systems (e.g., Carpenter et al. 1985), recent studies have found equally strong top-down forces in terrestrial systems (e.g., McLaren and Peterson 1994). In some circumstances, top-down forces can have important impacts on vegetation structure and species diversity (Brown and Heske 1990).

Terborgh (1992) hypothesized that a top-down interaction may structure vegetation dynamics in neotropical forests. Predators such as jaguar and puma appear to regulate the population densities of medium-sized mammals, which in turn may limit seedling recruitment. Changes in mammal community composition may therefore have profound effects on tree species diversity (Terborgh 1992). Much of the evidence relating to this hypothesis comes from islands in Gatun Lake (Panama), isolated in 1913, which now lack components of a full mammal community.

[TABULAR DATA FOR TABLE 1 OMITTED]

Barro Colorado Island (BCI), an island with neither jaguar nor puma resident, appears to support very high densities of some medium-sized mammals (Glanz 1982, 1991; but see Wright et al. 1994 for an alternative view). DeSteven and Putz (1984) and Sork (1987) found that seed predation was much higher and seedling survival much lower on BCI than on the adjacent mainland (but cf. Terborgh and Wright 1994). Other islands in Gatun Lake are too small ([less than] 1.2 ha) to support any terrestrial mammals and are now dominated by a restricted subset of tree species (Leigh et al. 1993).

Leigh et al. (1993) postulate that two factors have been of critical importance in the reduction of tree species diversity from small islands in Gatun Lake. Seeds that require burial by agouti (Dasyprocta punctata) to escape insect predation are unable to germinate on small islands (see also Forget 1990). The wind-influenced island microclimate then favors the seedlings of other species, such as the large-seeded Protium panamense (Leigh et al. 1993). As an alternative mechanism, Terborgh (1992) suggests that as medium-sized mammals are absent from small islands, large-seeded tree species can escape predation and are subsequently able to outcompete other species.

In this paper we compare rates of seed predation, germination, and seedling herbivory in Panamanian forests with different mammal communities. We experimentally examine factors that influence early mortality of three large-seeded tree species and test two specific predictions: (1) predation of large seeds is low on small islands, allowing escape of large-seeded tree species; (2) germination rates are low on small islands. We then discuss the mechanisms that appear to have caused the loss of tree species diversity from small Gatun Lake islands, and evaluate the hypothesis of mammalian control of neotropical forest dynamics (Terborgh 1992).

Study sites

The islands and peninsulas surrounding Gatun Lake are covered by tropical moist forest. Early aerial photographs suggest that many Gatun Lake islands have been forested since isolation (Leigh et al. 1993). Annual rainfall on BCI (9 [degrees] 10[minutes] N, 79 [degrees] 51 [minutes] W) is 2600 mm, with a 4-mo dry season beginning in December.

We conducted experiments in four forest types around Gatun Lake: five sites in mainland forests adjacent to the lake, five sites on BCI (1600 ha), and one site each on five medium-sized islands (15-80 ha) and five small islands ([less than]2 ha). All experimental sites were within 1 km of BCI, except for four of the medium islands, which were 4-5 km distant. Further details of the forest types are given in Leigh et al. (1982, 1993), Wright (1985), and Adler and Seamon (1991). Our small islands were islands 43, 44, 46, 48, and 49 in Adler and Seamon (1991). All granivorous and herbivorous mammals [greater than]1 kg in body mass found on the mainland are also present on BCI. The terrestrial mammalian granivore/herbivore community in each of the different forest types is shown in Table 1. Mainland forests and four medium islands are subject to limited poaching, while BCI, one medium island, and the small islands are not (Glanz 1991, S. J. Wright, personal observation).

Tree species

We investigated three native tree species. Dipteryx panamensis (Pitt.) Rec. & Mell (Leguminosae) is a common, large (40-50 m) canopy tree. Its drupes have a thin exocarp, and a hard thick-walled endocarp that encloses a single, large (4 cm) seed (DeSteven and Putz 1984). Gustavia superba (H.B.K.) Berg. (Lecythidaceae) is a small (typical dbh 10-15 cm) pioneer tree, common in the understory of secondary forest on BCI. Its large fruits (150-600 g) contain 5-50 seeds, each weighing 3-15 g (Sork 1987). Virola nobilis A. C. Smith (Myristicaceae) is a dioecious canopy tree. A fibrous capsule dehisces to expose a gray seed (2 x 1.5 cm) enclosed by a red 1 mm thick aril (Howe 1993). Primary dispersal of V. nobilis seeds is by birds and mammals (Howe 1993), D. panamensis seeds by bats (Bonnacorso et al. 1980), and G. superba fruits by gravity (Sork 1987). Seeds of all three species are consumed by mammalian granivores and may be secondarily dispersed and buried by scatterhoarding agouti (Dasyprocta punctata) (Forget and Milleron 1991, Forget 1992, 1993).