Seed dispersal increases local species richness and reduces spatial turnover of tropical tree seedlings

Abstract

Dispersal is thought to be a key process underlying the high spatial diversity of tropical forests. Just how important dispersal is in structuring plant communities is nevertheless an open question because it is very difficult to isolate dispersal from other processes, and thereby measure its effect. Using a unique situation, the loss of vertebrate seed dispersers on the island of Guam and their presence on the neighboring islands of Saipan and Rota, we quantify the contribution of vertebrate seed dispersal to spatial patterns of diversity of tree seedlings in treefall gaps. The presence of vertebrate seed dispersers approximately doubled seedling species richness within canopy gaps and halved species turnover among gaps. Our study demonstrates that dispersal plays a key role in maintaining local and regional patterns of diversity, and highlights the potential for ongoing declines in vertebrate seed dispersers to profoundly alter tropical forest composition.biodiversity loss | biotic homogenization | frugivory | mutualisms | tropical conservation T ropical forests typically have both high numbers of species per unit area and highly variable patterns of community composition through space (1, 2). Dispersal is thought to be a key process underlying this diversity, contributing to high local species richness by allowing the seeds arriving at a site to be drawn from a wide species pool (3, 4) and influencing the spatial arrangement of species by moving seeds away from parent trees, reducing conspecific aggregation (4-8). However, it has proven extremely difficult to quantify the contribution of seed dispersal to local diversity and spatial patterning in forests because it is confounded with other processes, including environmental variation, to which species differentially respond (2, 9); historical legacies, such as past disturbance (10); other biotic interactions, such as competition and predation (11, 12); and stochastic variation (13). Isolating the role of seed dispersal in maintaining diversity in tropical forests has nevertheless taken on new urgency due to widespread declines in populations of vertebrate dispersers throughout tropical regions (14-17). If vertebrate seed dispersal contributes substantially to the diversity and spatial patterning of trees in tropical forests, then declining vertebrate populations could lead to irrevocable changes in forest composition and structure.To separate the role of dispersal from other processes structuring tree communities, we would ideally manipulate dispersal while keeping other factors constant. For vertebrate dispersal, one approach would be to remove populations of vertebrate dispersers in treatment areas and compare these with untreated areas. However, vertebrate dispersal can occur over long distances (often up to several kilometers) (18), which requires manipulating vertebrate densities over areas larger than is logistically or ethically feasible. To overcome this, studies have used large-scale, unplanned manipulations (19) of vertebrate populations, comparing,...

Superorganisms or loose collections of species? A unifying theory of community patterns along environmental gradients

“…Dispersal thus tends to erase the spatial boundaries between zones, and to homogenise species composition. This recovers results from metacommunity theory showing that dispersal decreases beta‐diversity among communities (Mouquet & Loreau ; Leibold et al ), a theoretical prediction that is supported by empirical studies (Forbes & Chase ; Kneitel & Miller ; Simonis & Ellis ; Wandrag et al ). In nature, the absence of clear discontinuities in species composition along spatial environmental gradients, as observed in plant species along altitudinal gradients (Lieberman et al ; Vazquez & Givnish ) or in marine benthic organisms along depth gradients (Smale ), might thus reflects either a truly individualistic organisation or the effects of dispersal blurring the boundaries of discrete communities.…”

Introduction of mammalian seed predators and the loss of an endemic flightless bird impair seed dispersal of the New Zealand tree Elaeocarpus dentatus

“…Tawa Beilschmiedia tawa also appears to suffer from extremely low dispersal at some mainland sites (<10% of seeds captured below parent canopies had passed through a bird at three North Island sites; Silberbauer, ), although eight other studies on seed dispersal quantity in mainland New Zealand have found adequate dispersal rates (Kelly et al., ; Pegman, Perry, & Clout, ). On the Balearic Islands, introduced carnivorous mammals have indirectly lowered seedling recruitment of a perennial shrub by driving its mutualistic partner extinct (Traveset & Riera, ), while on Guam, the near‐total loss of frugivorous birds caused by the exotic brown tree snake ( Boiga irregularis ) may have caused a 61%–92% decline in seedling recruitment for two plant species (Rogers et al., ) and a reduction in seedlings of all tree species reaching canopy gaps away from parent trees (Wandrag, Dunham, Duncan, & Rogers, ). Whether the reduced dispersal we have recorded results in lowered recruitment for hinau depends on hinau's reliance on avian dispersal for improved germination (e.g., by gut passage, see Robertson, Trass, Ladley, & Kelly, ) and escape from disproportionate density‐ and distance‐dependent mortality beneath parent canopies (i.e., Janzen–Connell effects, see Comita et al., ).…”

Fauna as passengers and drivers in vegetation restoration: A synthesis of processes and evidence

“…; Wandrag et al . ). In these situations, a variety of impacts on seedlings of trees has been reported, including reduced diversity, greater spatial aggregation around parent trees and either high or lower densities depending on plant species, with greatest reductions in larger‐seeded species.…”

“…Second, the significance of animalplant interactions to plant recruitment has been strongly highlighted by recent reviews and investigations of 'empty forests'remnant mature forests where hunting or other impacts have extirpated many vertebrate animals in recent decades, while the habitat otherwise remains little-disturbed (Harrison et al 2013;Kurten 2013;Kurten et al 2015;Neuschulz et al 2016;Wandrag et al 2017). In these situations, a variety of impacts on seedlings of trees has been reported, including reduced diversity, greater spatial aggregation around parent trees and either high or lower densities depending on plant species, with greatest reductions in largerseeded species.…”