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- Materials and methods
In contrast to temperate herbaceous communities, the role of local-scale seed limitation is unclear in tropical forests. Makana & Thomas (2004) performed seed addition experiments for two light-demanding African tree species and found that both were strongly seed-limited. Indirect evidence for seed limitation comes from seed trap studies, which suggest strong seed limitation in many tropical forest plant species (Hubbell et al. 1999; Dalling et al. 2002; Murray & Garcia-C. 2002; Terborgh et al. 2002). Additional evidence for seed limitation is provided by autocorrelation in the spatial distribution of tropical plants that occurs independently of environmental variation (Dalling et al. 1998; Valencia et al. 2004) and by correlations between seedling distributions and seed rain density predicted from seed trap studies (Dalling et al. 2002). These indirect measures cannot provide conclusive evidence for seed limitation, however, because it is unclear which sites are suitable for germination and seedling establishment (Levine & Murrell 2003). Furthermore, community-level seed production can be very high in tropical forests. For example, seed rain density averages 965 seeds m−2 year−1 for seeds with minimum dimension larger than 1.0 mm on Barro Colorado Island, Panama (Harms et al. 2000) and ≥ 500 seeds m−2 year−1 for seeds with minimum dimension larger than 1.5 mm at Cocha Cashu, Peru (Terborgh et al. 2002). Hence, it is far from clear whether seed input limits total seedling recruitment in tropical forests (Terborgh et al. 2002; Wright 2002). In fact, Webb & Peart (2001) argued that community-wide seed dispersal in an Indonesian forest approached the level at which seed dispersal limitation is unimportant in curtailing competitive exclusion.
Here, we test directly for local-scale seed limitation for 32 shade-tolerant species in old-growth tropical moist forest in Panama using seed sowing experiments (Turnbull et al. 2000). We asked the following questions:
Is seedling recruitment of individual species seed-limited?
Is seedling recruitment of the plant community as a whole seed-limited?
What is the relative importance of species identity, location, seed limitation and their interactions as controls of seedling recruitment? An important role for location or a location-by-species interaction would provide evidence that not all sites are equally suitable for germination and seedling establishment of all shade-tolerant species.
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- Materials and methods
This seed addition experiment demonstrated that seedling recruitment was strongly seed-limited for 31 of 32 shade-tolerant species in an old-growth tropical moist forest and that subsequent seedling survival was sufficiently high that significant effects of added seeds persisted for 2 years for 26 species. The experiment also produced strong evidence that the plant community as a whole was severely seed-limited in terms of both seedling recruitment and total understorey plant density. The total of number of focal species’ seedlings surviving 1 year plus all non-focal species’ seedlings emerging during the first year was significantly increased by all seed addition treatments. Furthermore, the average focal species’ seedling density when 2–25 seeds were added per 0.0079-m2 plot (≥ 37 seedlings m−2 after 2 years) greatly exceeded average natural understorey plant densities on BCI (12 plants m−2, this study) and in other lowland neotropical forests [Cocha Cashu, Peru: 20 plants m−2 (Terborgh et al. 2002); La Selva, Costa Rica: 9–15 seedlings m−2 (Marquis et al. 1986)]. Seed arrival clearly affects the species composition as well as the overall density of seedlings in the tropical forest understorey. Because seed arrival provides the spatial template for processes occurring in later ontogenetic stages, strong seed limitation of seedling recruitment is likely to have profound consequences for the adult plant community as well, although experimental demonstration of this will be difficult for long-lived species.
We included several herbaceous species, and after 2 years at least one (Geophila repens) achieved reproductive size (1.4 m stem length; cf. Croat 1978) in a seed addition plot. Furthermore, seedlings of several other species also grew to rather large size over the 2 years of the study and the surviving seedlings of all species generally experienced positive growth in both years (Table 2). Hence, there is no indication that seedlings emerging after seed addition in otherwise unoccupied understorey sites should have a particularly low chance of reaching later ontogenetic stages. The strong seed limitation documented here suggests that tropical forest understorey plant communities are strongly influenced by seed arrival patterns, in particular given the likely absence of strong competitive dynamics in this stratum of the forest. Acting together with seed limitation, competitive suppression by the overstorey and herbivory cause understorey plant density to be low and hence there is little scope for direct competitive interactions among understorey plants (Wright 2002).
Nathan & Muller-Landau (2000) emphasized the importance of adding seeds at variable densities to provide information on seedling recruitment at saturating seed arrival densities. The addition of 25 vs. five seeds per 0.0079-m2 plot elicited a strong increase in seedling recruitment for shade-tolerant species with seed mass < 0.2 g. Consequently, the saturating seed rain density must be > 5 seeds per 0.0079 m2 for these species. There is an indication that 25 seeds per 0.0079 m2 might be approaching saturation because the increase in recruitment (on average 3.6-fold) was less than the increase in the number of seeds added (5-fold). Regardless, following Nathan & Muller-Landau (2000) the high seedling densities achieved by the addition of 25 seeds per 0.0079 m2 provide the best estimate of the absolute degree of seed limitation. The observed rain of seeds with minimum dimension > 1 mm averages 7.6 seeds per 0.0079 m2 year−1, including a large proportion of seeds from light-demanding species in old-growth forest on BCI (Harms et al. 2000). Hence, even the five-seed addition rate is likely to exceed the annual seed rain for all shade-tolerant species combined, and certainly far exceeds the combined natural seed rain (0.44 seeds per 0.0079 m2 year−1) of the 32 shade-tolerant study species (Table 1).
Seed limitation may be caused by insufficient seed numbers (source limitation) or non-uniform seed distribution patterns (dispersal limitation) (Clark et al. 1998; Muller-Landau et al. 2002; Schupp et al. 2002). Muller-Landau et al. (2002) found both strong source and dispersal limitation in Beilschmiedia pendula and negligible source and moderate dispersal limitation in Trichilia tuberculata at our study site. Our experiment does not allow separation of these two components of limitation for individual species; however, the strong relationship between the proportion of sites where seeds arrive and population-level seed production suggests that source limitation may generally be most important at the species level (Fig. 1). Dispersal limitation can be discounted at the community level.
The estimated strength of seed limitation varies with temporal scale because the chance that a seed arrives can only increase with the passage of time (Muller-Landau et al. 2002). Summing seed rain over long periods may be misleading, however, because it ignores temporal variability in site favourability and hence the importance of being present when ‘windows of opportunity’ open (Schupp et al. 2002).
We found that the seedling establishment rate per seed added did not differ between small-, medium- and large-seeded species, in contrast to several previous reports from BCI (e.g. Harms et al. 2000; Dalling & Hubbell 2002) and general meta-analyses (Moles & Westoby 2002, 2004). A relationship between seedling establishment and seed size may have emerged if the very smallest seeds, e.g. of Miconia or Ficus spp., had been included. However, in a study of 18 BCI tree species Augspurger (1984) likewise found no correlation between seed size and seedling survival rate under shade. Our impression from the field was that strong vertebrate predation on large seeds both before and after germination equalized overall establishment. A large proportion of the medium and large seeds added to our experimental plots were altogether removed, often within a few days of placement (J.-C.S., personal observation).
Seed addition, species identity, location and their interactions all had significant effects on seedling establishment for the 11 small-seeded, shade-tolerant species that were represented at all experimental sites in this study (Table 5). Differential establishment among locations and species with similar sized seeds could reflect many ecological differences, including attributes of microsites (e.g. light and moisture availability, proximity to pests) and attributes of species (e.g. shade and drought tolerance, pest defence). Niche differences with respect to edaphic conditions and light availability are well documented for the BCI flora (Kitajima 1994; Harms et al. 2001; Engelbrecht & Kursar 2003; Svenning et al. 2004). Specialized pests and pathogens could also cause seed and seedling survivorship to vary spatially, being low close to an adult conspecific or where conspecific density is high (Hyatt et al. 2003; Janzen 1970) as has indeed been shown for many of our study species on BCI (Condit et al. 1992, 1994; Schupp 1992; Harms et al. 2000; Wright et al. 2005). Nonetheless, the seed addition treatment and interactions involving the seed addition treatment collectively accounted for 86% of the explained variance in seedling recruitment in our experiment (Table 5).
We conclude that seed limitation strongly influences the local species composition of the understorey seedling community and limits the overall density of understorey plants on BCI and that site and species identity also have strong effects on establishment after seeds arrive. Strong seed limitation may set the stage for neutral dispersal-assembly of the shade-tolerant plant community on BCI (Hubbell 2001). However, the species differences in average seedling establishment per seed and its variation among sites demonstrate that niche differences among species and/or negative density dependence also affect community structure (Harms et al. 2000; Svenning et al. 2004; Wright et al. 2005).