Seed dispersal.— Over all 3 yr, both the quantity (proportion) and quality (distance) of dispersed seeds in continuous forest were double those in fragments. In addition, the distance of the furthest dispersed seeds in continuous forest was triple that in fragments. Finally, predicted dispersal curves for each forest type show more seeds dispersed to all distances from parent crowns in continuous forest than in forest fragments.
The reduced seed dispersal of D. cestroides in forest fragments may be attributed to the declines of terrestrial and arboreal mammalian dispersers for this species. The responses of primates and large mammals to fragmentation at the BDFFP coincide with the changes in dispersal we observed in Duckeodendron. Of the six primate species at the BDFFP, black spider monkeys (Ateles paniscus) and bearded sakis disappeared from the forest fragments immediately after isolation and remained absent for at least 10 yr after isolation (Gilbert & Setz 2001). Bearded sakis are a known consumer of D. cestroides fruit. The other confirmed consumer of Duckeodendron, red howler monkeys, are less sensitive to fragmentation, occasionally occupying 10-ha fragments (Gilbert & Setz 2001). In a recent study, sand traps (ten 0.25 m2 for a week) in fragments and continuous forest at the BDFFP recorded many fewer medium and large terrestrial mammals in fragments (9 records) than in nearby continuous forest (60 records) (Timo 2003). Thus, it appears that reduced seed dispersal in forest fragments resulted from overall mammal reductions, not the disappearance of a single species—an anticipated result given the asymmetry of most dispersal mutualisms (Bascompte et al. 2006) and the switching of dispersers among preferred fruit species (Herrera 1998, Levey & Benkman 1999).
Rates of Duckeodendron fruit removal 1–2 mo after initial censuses indicated that terrestrial animals were important secondary dispersers or seed predators. Over 6 weeks, a camera trap aimed at ten experimentally placed seeds under the canopy of a D. cestroides in a nearby continuous forest site recorded the Guianan squirrel (Sciurus aestuans, six visits), the brown four-eyed opossum (Metachirus nudicaudatus, five visits), and a Marmosa or Marmosops sp. (one visit) (Yabe et al. 1998). Over a 2-week period, our camera traps at two continuous forest sites photographed a Margay (Leopardis wiedii) and three gray-winged trumpeters (Psophia crepitans) at Duckeodendron fruits, and two agoutis (Dasyoprocta sp.), a capybara (Hydrochaeris hydrochaeris), and one Guianan squirrel (S. aestuans) in the bait vicinity. Other potentially important terrestrial mammals, such as acouchies, agouties, pacas, and rats (Proechimys spp. and Oryxomys spp.), are all present in fragments at the BDFFP. These species tend to hoard seeds, so they could be important secondary dispersers, although we did not track secondary dispersal. Scatterhoarding has been shown to increase seed survival and escape from seed predation by rats (Asquith & Mejia-Chang 2005). Undetected scatterhoarded seeds in fragments could counter our results by increasing the number of dispersed seeds in fragments and reducing the difference we saw in dispersal between fragments and continuous forest. If so, more scatterhoarded seeds in fragments should have resulted in more seedlings in fragments, but our results showed more seedlings in continuous forest. Also, fragmentation may reduce populations of scatterhoarders, resulting in a lower probability of scatterhoarded seeds in fragments (Galetti et al. 2003). Therefore, it is unlikely that undetected scatterhoarded seeds in fragments would change our interpretation of fragmentation effects on seed dispersal.
Fruiting of tropical trees is often highly variable with years of high fruit production interspersed with years of low or no fruit production (Herrera et al. 1998). Here, for D. cestroides, fruit crop fluctuated over the 3 yr of our study; total fruit production in 2003 was about half of 2002 and 2004 (40% and 60%, respectively). When fruit production was high, differences between fragments and continuous forest in the proportion of seeds dispersed and dispersal distances were significantly different or nearly so. In these years, seeds in continuous forest were found up to 46 m (2002) and 30 m (2004) from the parent tree, triple and double, respectively, the maximum dispersal distance (14 m) in any fragment. In contrast, in 2003 when fruit production was low, there were no detectable differences between continuous forest and forest fragments in the percent of seed dispersed or distance of dispersed seeds. Therefore, differences in dispersal between fragments and continuous forest were sharp during years of high fruit production, exactly when dispersal was important.
Reduced dispersal differences in 2003 may be a consequence of reduced D. cestroides fruit production. In 2003, a crash in fruit production in neighboring French Guiana resulted in frugivorous animals leaving the area (P. M. Forget, pers. comm.). Although reduced fruit crop sizes often do not affect the distance that seeds are dispersed (Laska & Stiles 1994, Bleher & Böhning-Gaese 2000), they appear to determine the attractiveness of a fruiting tree and, consequently, the likelihood of disperser visitation (Jansen et al. 2004). The lack of dispersal differences between forest types in 2003, when fruit production was low, may reflect poor visitation leading to poor dispersal.
Just as low disperser visitation could explain the lack of dispersal for all trees in 2003, it could be argued that smaller fruit crops of trees in forest fragments could result in poor disperser visitation (Jordano 1995, Saracco et al. 2005) and explain the reduced seed dispersal we recorded here. Forest fragmentation could reduce fruit crop sizes, perhaps as a result of poor pollinator visitation and resulting low fertilization. We found that trees in continuous forest did produce more fruits than trees in forest fragments over the course of 3 yr. To be conservative in the analyses, we incorporated the total number of seeds counted as an offset variable (SAS Institute Inc. 2005) in the analysis, comparing the proportion of seeds dispersed in continuous forest to forest fragments while adjusting for fruiting effort of each tree in each year. A greater proportion of seeds were dispersed in continuous forest than in forest fragments for all 3 yr, indicating that the differences in seed dispersal found here are strong despite modest differences in fruit production. Therefore, if poor disperser visitation is responsible for low dispersal in fragments relative to continuous forest, it is likely a result of changes in the disperser community, not simply differences in fruit crops.
Although we grouped 10- and 100-ha fragments as a result of limited sample sizes, both percent dispersal and the distance where the last seed was found had responses in 100-ha fragments that were intermediate to those in 10-ha fragments and continuous forest in years of high fruit production (2002 and 2004) but not in years of low fruit production (2003) (analyses not shown). These trends suggest that shifts in seed dispersal depended on fragment size, and that fragment area should be considered in dispersal studies wherever possible.
A critical assumption in our study is that the seeds found in the dispersal transects were assigned to the appropriate parent tree. A recent seed dispersal study on Simarouba amara in Panama found that the nearest adult was not always the maternal parent to a seedling (Hardesty et al. 2006). Without molecular markers, we cannot be definite of seed parentage and therefore of dispersal rates and distances for Duckeodendron. However, all of our parent trees were isolated from other fruiting conspecifics or were placed with their transects radiating away from fruiting conspecifics. The latter case occurred only once in our study, a pair of trees in continuous forest where any errors in assigning parentage would have underestimated dispersal distances. The net effect of underestimated dispersal distances would have yielded a greater actual difference in dispersal between continuous forest and fragments than we observed.
A limitation of sampling for dispersed seeds on the ground is that rare instances of long-distance dispersal are missed. In addition, as we did not monitor fruit removal from tree crowns, we could not account for seeds removed directly from trees and dispersed beyond our transects. Such differences could be problematic if dispersers in fragments behave differently from those in continuous forest (McConkey & Drake 2006). Seeds dispersed far beyond parent crowns and our transects may represent individuals of the highest dispersal quality, if they have the greatest likelihood of survival to adulthood because they escape distance-dependent mortality. We did analyze the tail of our distributions by looking at the five furthest dispersed seeds, and they exhibited more exaggerated differences between fragments and continuous forest than did all seeds.
Reduced seed dispersal resulting from forest fragmentation has been reported in three other studies, all in the tropics. Cordeiro and Howe (2003) found fragmentation reduced dispersal agents and seed removal of the endemic tree Leptonychia usambarensis in the East Usambara Mountains of Tanzania, although they did not report direct counts of dispersed seeds. Wright and Duber (2001) used direct counts of seeds to show that dispersal of Attalea butyraceae in Panama was less in areas where mammal populations were reduced by both hunting and fragmentation. Similarly, Galetti et al. (2006) found that in Brazil's fragmented Atlantic forest the probability of seed removal of the large-seeded endemic palm, Astrocaryum aculeatissimum, decreased as mammal dispersers were eliminated by hunting and fragmentation. These studies all linked reductions in dispersal in hunted fragments to reductions in seedlings numbers or densities. Results from our study further support these findings that forest fragmentation does reduce seed dispersal, here based on direct counts and on the distances seeds were dispersed in areas experimentally fragmented, where hunting was not a factor.
Seedling establishment.— We estimated the effect of distance-dependent mortality on seeds and seedlings by looking for newly germinated seedlings shortly after fruitfall and comparing the percent of germinated seeds across distance classes. The Janzen–Connell hypothesis states that predators should operate more intensely at distances closer to the parent tree. In forest fragments, the pattern of seedling germination contrasted with the Janzen–Connell hypothesis as the percent of germinated seeds under the crown was not different from the percent at 0–10 m beyond the crown, and there were no seeds in the 10+ m class (Fig. 4B). While the percent did not change, there were more absolute numbers of seedlings under the crown because there were more seeds there (Fig. 4A). In continuous forest, distance-dependent mortality may be more important for Duckeodendron as the percent of germinated seeds 0–10 m beyond the crown was greater than under the crown.
Differences in the influence of distance from the parent tree on germination in continuous forest and forest fragments resulted in differences in the absolute numbers of seedlings. Although both forest types showed that the number of seedlings declined with distance, this decline occurred much closer to parent trees in fragments than in continuous forest (Fig. 4A). The accelerated decline in seedling numbers with distance from parent crowns in fragments resulted in significantly fewer seedlings 0–10 m from the parent crown. This difference in seedling numbers with distance can be attributed to the number of seeds dispersed over all distances: increased seed dispersal in continuous forest resulted in greater numbers of seedlings at distances beyond the crown. In fragments, the low number of dispersed seeds coupled with their decline in number as distance increased, resulted in few seedlings 0–10 m from parent crowns and a complete absence of seedlings more than 10 m beyond parent crowns. Although we did not detect a change in the percent of seeds that germinated in fragments 1–2 mo after fruitfall, seedlings close to parent trees might still show increased susceptibility to distance-responsive herbivores or pathogens over longer periods. In fragments, where all seedlings are concentrated around parent plants, distance-dependent seedling mortality could have an extreme effect, eliminating nearly all seedlings in fragments.
Fragmentation effects of disrupted mutualisms on trees may be difficult to detect because the results take longer to surface in long-lived species. In addition to reduced seed dispersal and fewer seedlings in fragments shown here, fragment trees may also be affected by decreased probability of fertilization (Cascante et al. 2002), increased seed abortion (Chacoff et al. 2004), increased seed predation by vertebrates (Francisco et al. 2002), and decreased seed predation by insects (Janzen 1978, Cascante et al. 2002). By studying the mutualistic processes involved in plant regeneration, such as seed dispersal and first-year seedling establishment, we can detect changes that forecast the next generation before they appear in the adult community.