Treefall Gaps and the Maintenance of Species Diversity in a Tropical Forest

The maintenance of species diversity by treefall gaps is a long‐standing paradigm in forest ecology. Gaps are presumed to provide an environment in which tree species of differing competitive abilities partition heterogeneous resources. The empirical evidence to support this paradigm, however, remains scarce, and some recent studies even suggest that gaps do not maintain the diversity of shade‐tolerant species. Although there is evidence that gaps maintain the diversity of pioneer trees, most of this evidence comes from studies that did not make comparisons between gaps and intact forest sites (controls). Further, nearly all studies on the maintenance of diversity by gaps have ignored lianas, an important component of both old‐world and neotropical forests. We tested the hypothesis that treefall gaps maintain shade‐tolerant tree, pioneer tree, and liana species diversity in an old‐growth forest on Barro Colorado Island (BCI), Panama. We compared the density and species richness of these guilds between paired gap and non‐gap sites on both a per‐area and a per‐individual (per capita) basis. We found no difference in shade‐tolerant tree density and species richness between the gap and non‐gap sites. Both pioneer tree and liana density and species richness, however, were significantly higher in the gap than in the non‐gap sites on both a per‐area and a per‐individual basis. These results suggest that gaps maintain liana species diversity and that this effect is not merely a consequence of increased density. Furthermore, our data confirm the long‐held belief that gaps maintain pioneer tree species diversity. Because lianas and pioneer trees combined account for ∼43% of the woody plant species on BCI, and in other forests, our results are likely to be broadly applicable and suggest that gaps play a strong role in the maintenance of woody species diversity

Have we forgotten the forest because of the trees?

Recently, Brokaw and Busing argued that there is limited evidence for niche partitioning of tree species within forest gaps1. Consequently, gaps appear to play a relatively minor role in the maintenance of tree species diversity in forests via traditional resource partitioning. This conclusion is strongly supported by the existing empirical evidence, particularly for shade-tolerant tree species. Most studies of gaps, however, have failed to take into account plant groups other than trees2-4. Gaps may be a necessary habitat for the persistence of a large proportion of the vascular plant species other than shade-tolerant trees; specifically, pioneer trees, lianas, herbs, shrubs, and herbaceous vines2-8. For example, in a study on Barro Colorado Island (BCI), Panama, gaps had higher liana and pioneer tree diversity on both a per area and per stem basis (thereby removing the effect of density) compared to the surrounding forest2,3. These two plant groups alone account for approximately 43% of the woody species in this tropical forest2. There is also evidence that many forest herbs are gap dependent5,6. The role of gaps in the maintenance of shrubs is less clear, although there is some evidence that gaps promote shrub growth and reproduction7,8. Overall, when the major vascular plant groups are considered, as much as 65% of the flora of BCI may be gap dependent (Table 1). The specific mechanism that leads to the higher diversity of these groups in gaps remains unknown. Nonetheless, because these vascular plant groups represent a majority of the plant species in tropical forests worldwide4,9, gaps may often play a strong role in the maintenance of species diversity. Brokaw and Busing also argued that gaps might maintain diversity via the density effect10; Specifically, that gaps will have a higher diversity of trees solely because they have a higher density of trees compared to the surrounding forest. Tree density in gaps, however, declines (thins) with age, and thus the density effect could maintain diversity in the mature forest primarily in two ways. First, if individuals in gaps reach reproductive age prior to thinning then they could potentially colonize new gaps. Data are lacking, however, on whether trees reach reproductive age sooner (i.e., smaller size or age class) in gaps than in non-gap sites. Second, there must be niche partitioning. Without niche partitioning, thinning of individuals occurs randomly, and the initial increase in diversity would be merely a transitory result of the short-term increase in plant density2,11. Consequently, given the scanty evidence for niche partitioning and accelerated reproduction in gaps, the evidence for the density effect as a viable mechanism to explain the maintenance of diversity in forests is equivocal at best. We argue that papers sounding the death knell for the role of gaps in the maintenance of diversity in forests (e.g., Ref. 11) may be premature. The focus of most previous research on the ability of tree species to partition resources in gaps may have caused us to overlook the importance of gaps for many other groups of vascular plants (Table 1). Future research is necessary to quantify further the proportion of species in these and other groups (e.g., epiphytes) that require gaps for persistence in the community

The impact of lianas on tree regeneration in tropical forest canopy gaps: evidence for an alternative pathway of gap‐phase regeneration

1 Regeneration in forest canopy gaps is thought to lead invariably to the rapid recruitment and growth of trees and the redevelopment of the canopy. Our observations, however, suggest that an alternate successional pathway is also likely, whereby gap‐phase regeneration is dominated by lianas and stalled in a low‐canopy state for many years. We investigated gap‐phase regeneration in an old‐growth tropical forest on Barro Colorado Island (BCI) in Panama to test the following two hypotheses: (i) many gaps follow a pathway in which they remain at a low canopy height and are dominated by lianas and (ii) the paucity of trees in this pathway is a function of liana density. 2 We surveyed a total of 428 gaps of varying ages (c. 5, c. 10, and 13+ years old) and identified those which followed the conventional pathway of regeneration and others that remained stalled in a low‐canopy state for many years and were dominated by either lianas or palms. Each of these pathways will likely have different successional trajectories that will favour the growth of a distinct suite of mature species and ultimately result in contrasting species composition. 3 The successional pathway of liana‐dominated, stalled gaps is common throughout the forest. We estimate conservatively that 7.5% of the gaps that form each year will follow this pathway, probably due to the suppression of tree regeneration by lianas, and that many of these stalled gaps will persist for much longer than 13 years. Consequently, a high proportion of gaps in the forest at any given time will be stalled. Furthermore, liana tangles, which persist in the tropical forest understorey for extended periods of time, almost certainly originate in these gaps. 4 Liana abundance was positively correlated with pioneer tree abundance and diversity while negatively correlated with non‐pioneer tree abundance and diversity. Thus, lianas appear to inhibit non‐pioneer tree survival while indirectly enhancing that of pioneer trees. 5 Lianas are abundant in many types of tropical and temperate forests and a successional pathway involving liana‐dominated, stalled gaps may therefore be frequent and widespread

Lianas suppress tree regeneration and diversity in treefall gaps

Treefall gaps are hypothesized to maintain diversity by creating resource‐rich, heterogeneous habitats necessary for species coexistence. This hypothesis, however, is not supported empirically for shade‐tolerant trees, the dominant plant group in tropical forests. The failure of gaps to maintain shade‐tolerant trees remains puzzling, and the hypothesis implicated to date is dispersal limitation. In central Panama, we tested an alternative ‘biotic interference’ hypothesis: that competition between growth forms (lianas vs. trees) constrains shade‐tolerant tree recruitment, survival and diversity in gaps. We experimentally removed lianas from eight gaps and monitored them for 8 years, while also monitoring nine un‐manipulated control gaps. Removing lianas increased tree growth, recruitment and richness by 55, 46 and 65%, respectively. Lianas were particularly harmful to shade‐tolerant species, but not pioneers. Our findings demonstrate that competition between plant growth forms constrains diversity in a species‐rich tropical forest. Because lianas are abundant in many tropical systems, our findings may apply broadly

Liana diversity, abundance, and mortality in a tropical wet forest in Costa Rica

Lianas can have a large impact on the diversity, structure, and dynamics of tropical forests, yet they remain essentially unknown even in some of the most intensely studied tropical forests, such as La Selva Biological Station in Costa Rica. We quantified the diversity, abundance, and mortality of lianas in primary and selectively logged forest at La Selva for over 3 years, from January 1999 until July 2002. We measured, identified, permanently marked, and mapped all lianas ≥1.3 m in length and 2 mm in diameter, whether climbing or free-standing, in nine, m (864 m2) plots. There were no significant differences in density, diversity, or mortality between primary forest and areas that were selectively logged approximately 50 years prior to our study. We found a mean density of 1493 lianas ha−1 and a mean species richness of 23 species per 864 m2 plot. Annual mortality was 9.4% over all size-classes, but was the highest for the smallest individuals (\u3c2 cm in diameter). Annual mortality for larger individuals (≥5 cm) was much lower over the 3.5-year period (3.2% per year) and the five most abundant species suffered no mortality in this size-class. In contrast to many lowland neotropical forests, where Bignoniaceae and Fabaceae are reported to be the dominant liana families, at La Selva we found that Sapindaceae was the most speciose family and Dilleniaceae the most abundant. Moutabea aculeata (Polygalaceae) was the most abundant species, constituting approximately 17% of the individuals and having the lowest mortality of all 60 species. The 10 most abundant species at La Selva accounted for more than 60% of all individuals. Compared to other lowland sites in the neotropics, including other wet forests, the abundance and diversity of lianas at La Selva are very low

Establishment limitation reduces species recruitment and species richness as soil resources rise

At local spatial scales, species richness tends to fall as productivity rises. Most explanations have focused on increased extinction, but, instead, we test experimentally whether increased soil fertility reduces recruitment. Specifically, we test whether variation in recruitment is due to source limitation, germination limitation or establishment limitation, and how litter accumulation and seed predation contribute to these processes. We established four crossed experimental treatments in a perennial‐dominated early successional plant community over 3 years. We added seed of 30 species, manipulated access by selected seed predators, removed litter and added slow release fertilizer at four levels (0, 8, 16 and 32 g N m−2). Species recruitment and richness both decreased with increasing fertility, but, counter to our expectations, we found that neither seed additions nor litter removal could counteract the negative effects of fertilizer. Seed additions increased seedling density at all fertilizer levels, and seed predation appeared to have no influence on seedling densities. In spite of high seedling densities at all fertilizer levels, final stem density declined by 70% as fertilizer increased. A strong stem density–species richness relationship suggests that declines in final stem density caused more than half of the decline in species richness along this fertility gradient. These results suggest that establishment limitation, i.e. the reduction of growth and survival from seedling to adult, controls species recruitment in highly fertile sites. The high degree of recruitment limitation commonly observed in productive habitats suggests that high productivity causes establishment limitation, thereby isolating these communities from the regional species pool. We suggest that such isolation provides a mechanism to explain why the species composition of productive communities exhibits higher variability than the composition of less productive communities within the same regional source pool

Herbivore and Pathogen Damage on Grassland and Woodland Plants: A Test of The Herbivore Uncertainty Principle

Researchers can alter the behaviour and ecology of their study organisms by conducting such seemingly benign activities as non‐destructive measurements and observations. In plant communities, researcher visitation and measurement of plants may increase herbivore damage in some plant species while decreasing it in others. Simply measuring plants could change their competitive ability by altering the amount of herbivore damage that they suffer. Currently, however, there is only limited empirical evidence to support this `herbivore uncertainty principle\u27 (HUP). We tested the HUP by quantifying the amount of herbivore and pathogen damage in 13 plant species (\u3e 1400 individuals) at four different visitation intensities at Cedar Creek Natural History Area, Minnesota, USA. Altogether, we found very little evidence to support the HUP at any intensity of visitation. Researcher visitation did not alter overall plant herbivore damage or survival and we did not detect a significant visitation effect in any of the 13 species. Pathogen damage also did not significantly vary among visitation treatments, although there was some evidence that high visitation caused slightly higher pathogen damage. Based on our results, we question whether this phenomenon should be considered a `principle\u27 of plant ecology

Lianas in gaps reduce carbon accumulation in a tropical forest

Treefall gaps are the “engines of regeneration” in tropical forests and are loci of high tree recruitment, growth, and carbon accumulation. Gaps, however, are also sites of intense competition between lianas and trees, whereby lianas can dramatically reduce tree carbon uptake and accumulation. Because lianas have relatively low biomass, they may displace far more biomass than they contribute, a hypothesis that has never been tested with the appropriate experiments. We tested this hypothesis with an 8-yr liana removal experiment in central Panama. After 8 years, mean tree biomass accumulation was 180% greater in liana-free treefall gaps compared to control gaps. Lianas themselves contributed only 24% of the tree biomass accumulation they displaced. Scaling to the forest level revealed that lianas in gaps reduced net forest woody biomass accumulation by 8.9% to nearly 18%. Consequently, lianas reduce whole-forest carbon uptake despite their relatively low biomass. This is the first study to demonstrate experimentally that plant–plant competition can result in ecosystem-wide losses in forest carbon, and it has critical implications for recently observed increases in liana density and biomass on tropical forest carbon dynamics