Directed seed dispersal by bellbirds in a tropical cloud forest

Abstract

A fundamental goal of plant population ecology is to understand the consequences for plant fitness of seed dispersal by animals. Theories of seed dispersal and tropical forest regeneration suggest that the advantages of seed dispersal for most plants are escape from seed predation near the parent tree and colonization of vacant sites, the locations of which are unpredictable in space and time. Some plants may gain in fitness as a fortuitous consequence of disperser behavior if certain species of dispersers nonrandomly place seeds in sites predictably favorable for seedling establishment. Such patterns of directed dispersal by vertebrates long have been suggested but never demonstrated for tropical forest trees. Here we report the pattern of seed distribution and 1-year seedling survival generated by five species of birds for a neotropical, shade-tolerant tree. Four of the species dispersed seeds to sites near the parent trees with microhabitat characteristics similar to those at random locations, whereas the fifth species, a bellbird, predictably dispersed seeds under song perches in canopy gaps. The pattern of seedling recruitment was bimodal, with a peak near parent trees and a second peak, corresponding to bellbird song perches, far (>40 m) from parent trees. Seedling survival was higher for seeds dispersed by bellbirds than by the other species, because of a reduction in seedling mortality by fungal pathogens in gaps. Thus, bellbirds play a significant role in seed dispersal by providing directed dispersal to favorable sites and therefore may influence plant recruitment patterns and species diversity in Neotropical forests.

Figure 1

The frequency of dispersed seeds (A and B) and seedlings surviving 1 year (C) as functions of distance from the closest fruiting O. endresiana tree and canopy cover for guans, quetzals, toucanets, and robins combined (n = 128) (A) and bellbirds (n = 56) (B). Each bar represents the proportion of seeds dispersed by particular dispersers (A and B) or surviving seedlings (C) in each distance/canopy cover category. In this study site, all bellbird perches were >40 m from the closest fruiting O. endresiana tree. Values <90% for canopy cover represent gaps (28). Note the bimodal pattern of seedling recruitment (C) reflects that of seed dispersal, with one peak close to the parent trees (A) and a second peak corresponding to the bellbird perches (B). The increase in seed input at greater distances is not a result of the increase in annulus area with distance but rather is due to the concentration of seeds in the vicinity of bellbird perches. In particular, the number of seeds dispersed to gaps by bellbirds was greater than expected by chance (X² = 36.45, df = 1, P < 0.001) based on the area of the study site (5 ha) in gaps (5.3%) and forest (94.7%). No seedlings survived in the two lowest canopy cover categories, suggesting a limit to the benefits of higher light levels.

Figure 2

Plot of all seed locations as functions of the first two axes of a principal component analysis of the correlation matrix (sas proc factor; ref. 30) of habitat variables. The first two factors explained 48% of total variance. The first factor is characterized most by high loadings of canopy cover (−0.86), number of stems (0.72), distance to nearest woody stem (0.65), and distance to parent (0.64). The second factor was characterized most by leaf litter (0.67). Note that seeds dispersed by bellbirds extend into regions farther from the parent trees and with more open canopy (i.e., higher loadings on factor 1) than seeds dispersed by the other four species. The loadings for factor 1 are significantly different among the random sites, bellbird sites, and other species’ sites (ANOVA: F = 71.6, df = 2, 252; P < 0.0001). The bellbird sites differ from random sites and from other species’ sites (post-hoc Fisher’s Protected LSD tests P values < 0.0001), but the random sites do not differ from the other species’ sites (P = 0.12).

Figure 3

One-year seedling survival, proportion of mortality caused by fungal pathogens, and seedling height (mean + 1 SD) for seeds dispersed by bellbirds (open bars) and four other species (shaded). Seeds dispersed by bellbirds were more likely to survive to 1 year (X² = 4.6, df = 1, P = 0.03), and the resulting seedlings (n = 17) were taller (t test = 2.37, df = 36, P = 0.02) than were seedlings from seeds dispersed by the other four species (n = 21). Bellbird sites had a lower incidence of mortality by fungal pathogens than did the seedlings from seeds dispersed by the other four species (X² = 4.28, df = 1, P = 0.03).