Plant pathogens drive density-dependent seedling mortality in a tropical tree

One explanation for the extraordinary diversity of tropical forest trees is that density-dependent mortality from herbivores or pathogens puts locally rare species at an advantage. Density-dependent mortality of seeds and small seedlings is particularly intense in tropical forests, but its causes remain uncertain. Here, we show experimentally that pathogens from the Oomycota are associated with intense mortality in seedlings of a neotropical tree, Sebastiana longicuspis . Seedlings in untreated plots experienced eight times higher mortality compared with seedlings in plots treated with fungicide. Mortality was strongly density dependent: in fungicide-treated plots survival was unaffected by density, but survival in unsprayed plots was over three times higher at low density. Density-dependent mortality observed in a simultaneous, non-manipulative study was highly transient, suggesting that short-term observational studies may underestimate the intensity and form of pathogen-induced mortality. If such effects are widespread, plant pathogens may play a key role in maintaining and structuring tropical diversity.     

Testing for enemy‐mediated density‐dependence in the mortality of seedlings: field experiments with five Neotropical tree species

The coexistence of plant species in species‐rich tropical forests can be promoted by specialised enemies acting in a negatively density‐dependent manner. While survival of tropical tree seedlings is often negatively density‐dependent, the causes have rarely been identified. We tested whether insects and plant pathogens cause density‐dependent seedling recruitment and survival in five forest tree species in Belize, Central America. We manipulated densities of seeds or newly germinated seedlings in small (1 m² or 0.25 m²) plots close to fruiting conspecific trees. Using a factorial design, we excluded enemies from subsets of the plots with fungicides and insecticides. Seed germination (for two species) and early seedling survival (for all species) were monitored at approximately weekly intervals for up to eight weeks, during the period when plants are likely to be most susceptible to natural enemies. In Terminalia amazonia, seed germination was negatively density‐dependent and the proportion of seeds germinating increased when insects were excluded. However, the magnitude of the insecticide effect was independent of density. The only significant density effect for survival of young seedlings was in Acacia polyphylla; counter to expectation, seedling survival was higher at high densities. In a few cases pesticide application had a significant effect on seedling survival, but in only one case (Terminalia amazonia) was a significant pesticide × density interaction detected. Our results caution against generalising from studies conducted on a single species at a single time and place and illustrate the challenges of experimentally testing for enemy‐mediated negative density‐dependence. Experimental outcomes are likely to depend on the spatial scale at which the principal enemies disperse and respond to plant density, and the timescales over which they act. Gathering information on these variables will improve our understanding of the natural histories of tropical forest species and help inform the design of future experiments.     

Neighboring trees regulate the root‐associated pathogenic fungi on the host plant in a subtropical forest

Root‐associated fungi and host‐specific pathogens are major determinants of species coexistence in forests. Phylogenetically related neighboring trees can strongly affect the fungal community structure of the host plant, which, in turn, will affect the ecological processes. Unfortunately, our understanding of the factors influencing fungal community composition in forests is still limited. In particular, investigation of the relationship between the phytopathogenic fungal community and neighboring trees is incomplete. In the current study, we tested the host specificity of members of the root‐associated fungal community collected from seven tree species and determined the influence of neighboring trees and habitat variation on the composition of the phytopathogenic fungal community of the focal plant in a subtropical evergreen forest. Using high‐throughput sequencing data with respect to the internal transcribed spacer (ITS) region, we characterized the community composition of the root‐associated fungi and found significant differences with respect to fungal groups among the seven tree species. The density of conspecific neighboring trees had a significantly positive influence on the relative abundance of phytopathogens, especially host‐specific pathogens, while the heterospecific neighbor density had a significant negative impact on the species richness of host‐specific pathogens, as well as phytopathogens. Our work provides evidence that the root‐associated phytopathogenic fungi of a host plant depend greatly on the tree neighbors of the host plant.     

Limited contributions of plant pathogens to density‐dependent seedling mortality of mast fruiting Bornean trees

Fungal pathogens are implicated in driving tropical plant diversity by facilitating strong, negative density‐dependent mortality of conspecific seedlings (C‐NDD). Assessment of the role of fungal pathogens in mediating coexistence derives from relatively few tree species and predominantly the Neotropics, limiting our understanding of their role in maintaining hyper‐diversity in many tropical forests. A key question is whether fungal pathogen‐mediated C‐NDD seedling mortality is ubiquitous across diverse plant communities. Using a manipulative shadehouse experiment, we tested the role of fungal pathogens in mediating C‐NDD seedling mortality of eight mast fruiting Bornean trees, typical of the species‐rich forests of South East Asia. We demonstrate species‐specific responses of seedlings to fungicide and density treatments, generating weak negative density‐dependent mortality. Overall seedling mortality was low and likely insufficient to promote overall community diversity. Although conducted in the same way as previous studies, we find little evidence that fungal pathogens play a substantial role in determining patterns of seedling mortality in a SE Asian mast fruiting forest, questioning our understanding of how Janzen‐Connell mechanisms structure the plant communities of this globally important forest type.     

Evolutionary history and distance dependence control survival of dipterocarp seedlings

One important hypothesis to explain tree-species coexistence in tropical forests suggests that increased attack by natural enemies near conspecific trees gives locally rare species a competitive advantage. Host ranges of natural enemies generally encompass several closely related plant taxa suggesting that seedlings should also do poorly around adults of closely related species. We investigated the effects of adult Parashorea malaanonan on seedling survival in a Bornean rain forest. Survival of P. malaanonan seedlings was highest at intermediate distances from parent trees while heterospecific seedlings were unaffected by distance. Leaf herbivores did not drive this relationship. Survival of seedlings was lowest for P. malaanonan , and increased with phylogenetic dissimilarity from this species, suggesting that survival of close relatives of common species is reduced. This study suggests that distance dependence contributes to species coexistence and highlights the need for further investigation into the role of shared plant enemies in community dynamics.
Ecology Letters (2010) 13: 51–59     

Tri-trophic interactions affect density dependence of seed fate in a tropical forest palm

Natural enemies, especially host-specific enemies, are hypothesised to facilitate the coexistence of plant species by disproportionately inflicting more damage at increasing host abundance. However, few studies have assessed such Janzen-Connell mechanisms on a scale relevant for coexistence and no study has evaluated potential top-down influences on the specialized pests. We quantified seed predation by specialist invertebrates and generalist vertebrates, as well as larval predation on these invertebrates, for the Neotropical palm Attalea butyracea across ten 4-ha plots spanning 20-fold variation in palm density. As palm density increased, seed attack by bruchid beetles increased, whereas seed predation by rodents held constant. But because rodent predation on bruchid larvae increased disproportionately with increasing palm density, bruchid emergence rates and total seed predation by rodents and bruchids combined were both density-independent. Our results demonstrate that top-down effects can limit the potential of host-specific insects to induce negative-density dependence in plant populations.     

Signs of stabilisation and stable coexistence

Many empirical studies motivated by an interest in stable coexistence have quantified negative density dependence, negative frequency dependence, or negative plant–soil feedback, but the links between these empirical results and ecological theory are not straightforward. Here, we relate these analyses to theoretical conditions for stabilisation and stable coexistence in classical competition models. By stabilisation, we mean an excess of intraspecific competition relative to interspecific competition that inherently slows or even prevents competitive exclusion. We show that most, though not all, tests demonstrating negative density dependence, negative frequency dependence, and negative plant–soil feedback constitute sufficient conditions for stabilisation of two‐species interactions if applied to data for per capita population growth rates of pairs of species, but none are necessary or sufficient conditions for stable coexistence of two species. Potential inferences are even more limited when communities involve more than two species, and when performance is measured at a single life stage or vital rate. We then discuss two approaches that enable stronger tests for stable coexistence‐invasibility experiments and model parameterisation. The model parameterisation approach can be applied to typical density‐dependence, frequency‐dependence, and plant–soil feedback data sets, and generally enables better links with mechanisms and greater insights, as demonstrated by recent studies.     

Indirect interactions among tropical tree species through shared rodent seed predators: a novel mechanism of tree species coexistence

The coexistence of numerous tree species in tropical forests is commonly explained by negative dependence of recruitment on the conspecific seed and tree density due to specialist natural enemies that attack seeds and seedlings (‘Janzen–Connell’ effects). Less known is whether guilds of shared seed predators can induce a negative dependence of recruitment on the density of different species of the same plant functional group. We studied 54 plots in tropical forest on Barro Colorado Island, Panama, with contrasting mature tree densities of three coexisting large seeded tree species with shared seed predators. Levels of seed predation were far better explained by incorporating seed densities of all three focal species than by conspecific seed density alone. Both positive and negative density dependencies were observed for different species combinations. Thus, indirect interactions via shared seed predators can either promote or reduce the coexistence of different plant functional groups in tropical forest.     

The presence of generalist plant pathogens might not explain the long-term coexistence of plant species

Pathogens have been shown to contribute to the possibility of coexistence of competing plant species by creating ecological distinction between the coexisting species. This coexistence promoting mechanism resembles intra-specific density dependence as found in Lotka-Volterra models. However, plant species adapt in their level of resistance against pathogen infection and this adaptation has been shown to be traded-off by a reduction in growth rate. A model is developed to show that taking into account the possible adaptation of plant species to increase their resistance against pathogen infection by generalist pathogens has consequences for the coexistence of the plant species. The results show that in systems where plants adapt to the pathogen infection, coexistence becomes impossible. The implication of this finding is that plant pathogens might contribute less to the coexistence of plant species than is commonly thought.     

On the Sympatric Evolution and Evolutionary Stability of Coexistence by Relative Nonlinearity of Competition

If two species exhibit different nonlinear responses to a single shared resource, and if each species modifies the resource dynamics such that this favors its competitor, they may stably coexist. This coexistence mechanism, known as relative nonlinearity of competition, is well understood theoretically, but less is known about its evolutionary properties and its prevalence in real communities. We address this challenge by using adaptive dynamics theory and individual-based simulations to compare community stabilization and evolutionary stability of species that coexist by relative nonlinearity. In our analysis, evolution operates on the species'' density-compensation strategies, and we consider a trade-off between population growth rates at high and low resource availability. We confirm previous findings that, irrespective of the particular model of density dependence, there are many combinations of overcompensating and undercompensating density-compensation strategies that allow stable coexistence by relative nonlinearity. However, our analysis also shows that most of these strategy combinations are not evolutionarily stable and will be outcompeted by an intermediate density-compensation strategy. Only very specific trade-offs lead to evolutionarily stable coexistence by relative nonlinearity. As we find no reason why these particular trade-offs should be common in nature, we conclude that the sympatric evolution and evolutionary stability of relative nonlinearity, while possible in principle, seems rather unlikely. We speculate that this may, at least in part, explain why empirical demonstrations of this coexistence mechanism are rare, noting, however, that the difficulty to detect relative nonlinearity in the field is an equally likely explanation for the current lack of empirical observations, and that our results are limited to communities with non-overlapping generations and constant resource supply. Our study highlights the need for combining ecological and evolutionary perspectives for gaining a better understanding of community assembly and biogeographic patterns.     

Processes Driving Ontogenetic Succession of Galls in a Canopy Tree1

Herbivores can be associated with distinct ontogenetic stages of their host in a nonseasonal, directional, and continuous pattern of colonization and extinction of species populations called ontogenetic succession, but the processes behind this pattern are still largely unknown. We used plants of Cryptocarya aschersoniana Mez (Lauraceae) belonging to different ontogenetic stages, to examine how the density of different gall‐inducing insects varies along the ontogeny of the host, and how gall density is influenced by mechanisms associated with host quality (plant height, plant shape, leaf area, specific leaf area, and hypersensitivity), and by mechanisms associated with their natural enemies (parasitoids, pathogens, and predators). In a remnant of Araucaria Forest, located in the São Francisco de Paula National Forest (Brazil), gall density (ind./100 g of leaf ) was obtained for 42 plants of C. aschersoniana divided into three height classes. Two galling species were recorded, showing quite distinct density patterns among height classes of C. aschersoniana. While Hymenoptera gall density decreased almost 50 times from small plants to canopy trees, Hemiptera gall density increased almost 10 times. Path analyses showed that Hymenoptera density was higher in smaller plants, independent of other host traits, while Hemiptera density was higher in plants exhibiting smaller leaves. Natural enemies were not detected in the Hemiptera population, and mortality rates due to predators, parasitoids, and pathogens did not affect Hymenoptera density. Processes associated with plant quality play the main role in generating the observed ontogenetic succession pattern.     

Density dependence in forests is stronger in tropical and subtropical climates among closely related species

Density dependence has long been considered an important mechanism for species coexistence in forests. Density‐dependent processes can be important mechanisms driving differences in species diversity across latitudes. Here we examined the decline in strength of density dependence with increasing latitude, and particularly how density dependence affected both conspecifics and heterospecifics. Conspecific individuals within a species were predominantly aggregated at the three different latitudes of the three study sites in China. The percentage of aggregated species declined with increasing spatial scale and growth stages, which confirmed the overall importance of density dependence. Compared with a latitudinal gradient, the intensity of aggregation in the most northerly temperate (Changbaishan) plot was significantly higher than that in the tropical (Bawangling) or subtropical (Heishiding) plots. This showed that the strength of density dependence among conspecific individuals at low latitudes was stronger than that for high latitudes. We found that the more closely related species were more spatially adjacent in the temperate plot, while the opposite was true in the tropical and subtropical plots at most scales. After calculating the recruitment probability of all species of mature trees, we found that 19 of the 32 species in the tropical plot and 7 of the 12 species in the subtropical plot were less likely to recruit near closely related species. In the northern temperate plot, only one species demonstrated this phenomenon. These results therefore suggest that latitudinal variation in the intensity of negative density‐dependent recruitment resulting from specialist natural enemies (the Janzen–Connell hypothesis) may contribute to the latitudinal gradient of diversity in trees. The strength of density dependence at low latitudes was stronger than at high latitudes, regardless of whether this dependence was measured between only conspecific individuals or between individuals of closely related species.     

Density dependence across multiple life stages in a temperate old-growth forest of northeast China

Recent studies on species coexistence suggest that density dependence is an important mechanism regulating plant populations. However, there have been few studies of density dependence conducted for more than one life-history stage or that control for habitat heterogeneity, which may influence spatial patterns of survival and mask density dependence. We explored the prevalence of density dependence across multiple life stages, and the effects of controlling for habitat heterogeneity, in a temperate forest in northeast China. We used generalized linear mixed-effects models to test for density-dependent mortality of seedlings and spatial point pattern analysis to detect density dependence for sapling-to-juvenile transitions. Conspecific neighbors had a negative effect on survival of plants in both life stages. At the seedling stage, we found a negative effect of conspecific seedling neighbors on survival when analyzing all species combined. However, in species-level analyses, only 2 of 11 focal species were negatively impacted by conspecific neighbors, indicating wide variation among species in the strength of density dependence. Controlling for habitat heterogeneity did not alter our findings of density dependence at the seedling stage. For the sapling-to-juvenile transition stage, 11 of 15 focal species showed patterns of local scale (<10 m) conspecific thinning, consistent with negative density dependence. The results varied depending on whether we controlled for habitat heterogeneity, indicating that a failure to account for habitat heterogeneity can obscure patterns of density dependence. We conclude that density dependence may promote tree species coexistence by acting across multiple life-history stages in this temperate forest.     

EXPERIMENTAL MANIPULATION OF PUTATIVE SELECTIVE AGENTS PROVIDES EVIDENCE FOR THE ROLE OF NATURAL ENEMIES IN THE EVOLUTION OF PLANT DEFENSE

Although biologists have long assumed that plant resistance characters evolved under selection exerted by such natural enemies as herbivores and pathogens, experimental evidence for this assumption is sparse. We present evidence that natural enemies exert selection on particular plant resistance characters. Specifically, we demonstrate that elimination of natural enemies from an experimental field population of Arabidopsis thaliana alters the pattern of selection on genetic variation in two characters that have been shown to reduce herbivore damage in the field: total glucosinolate concentration and trichome density. The change in pattern of selection reveals that natural enemies imposed selection favoring increased glucosinolate concentration and increased trichome density, and thus, supports one of the major assumptions of the coevolution hypothesis. We also demonstrate that a pattern of stabilizing selection on glucosinolate concentration results from a balance between the costs and benefits associated with increasing levels of this resistance character. This result provides direct confirmation of the appropriateness of cost-benefit models for characterizing the evolution of plant defenses.     

When do localized natural enemies increase species richness?

The Janzen–Connell hypothesis states that local species‐specific density dependence, mediated through specialist enemies of offspring such as fungal pathogens and insect seed predators, can facilitate coexistence of species by preventing recruitment near conspecific adults. We use spatially explicit simulation models and analytical approximations to evaluate how spatial scales of offspring and enemy dispersal affect species richness. In comparison with model communities in which both offspring and enemies disperse long distances, species richness is substantially decreased when offspring disperse long distances and enemies disperse short distances. In contrast, when both offspring and enemies disperse short distances species richness more than doubles and adults of each species are highly spatially clumped. For the range of conditions typical of tropical forests, locally dispersing specialist enemies may decrease species richness relative to enemies that disperse long distances. In communities where dispersal distances of both offspring and enemies are short, local effects may enhance species richness.     

Consequences of changing rainfall for fungal pathogen-induced mortality in tropical tree seedlings

Most general circulation models predict that most tropical forests will experience lower and less frequent rainfall in future as a result of climate change, which may reduce the capacity of fungal pathogens to drive density-dependent tree mortality. This is potentially significant because fungal pathogens are thought to play a key role in promoting and structuring plant diversity in tropical forests through the Janzen-Connell mechanism. Therefore, we hypothesize that the drying of tropical forests will negatively impact species coexistence. To test one prediction of this hypothesis, we imposed experimental watering regimes on the seedlings of a tropical tree, Pleradenophora longicuspis, and measured mortality induced by fungal pathogens under shade house conditions. The frequency of watering had a strong impact on survival. Seedlings watered daily experienced significantly higher mortality than those watered every three or every six days, while increasing the volume of water applied also led to increased mortality, although this relationship was less pronounced. These results suggest that the capacity of fungal pathogens to drive density-dependent mortality may be reduced in drier climates and when rainfall is less frequent, with potential implications for the diversity enhancing Janzen-Connell mechanism.     

Enemies mediate distance- and density-dependent mortality of tree seeds and seedlings: a meta-analysis of fungicide,insecticide and exclosure studies

Conspecific negative distance- and density-dependence is often assumed to be one of the most important mechanisms controlling forest community assembly and species diversity globally. Plant pathogens, and insect and mammalian herbivores, are the most common natural enemy types that have been implicated in this phenomenon, but their general effects at different plant life stages are still unclear. Here, we conduct a meta-analysis of studies that involved robust manipulative experiments, using fungicides, insecticides and exclosures, to assess the contributions of different natural enemy types to distance- and density-dependent effects at seed and seedling stages. We found that distance- and density-dependent mortality caused by natural enemies was most likely at the seedling stage and was greater at higher mean annual temperatures. Conspecific negative distance- and density-dependence at the seedling stage is significantly weakened when fungicides were applied. By contrast, negative conspecific distance- and density-dependence is not a general pattern at the seed stage. High seed mass reduced distance- and density-dependent mortality at the seed stage. Seed studies excluding only large mammals found significant negative conspecific distance-dependent mortality, but exclusion of all mammals resulted in a non-significant effect of conspecifics. Our study suggests that plant pathogens are a major cause of distance- and density-dependent mortality at the seedling stage, while the impacts of herbivores on seedlings have been understudied. At the seed stage, large and small mammals, respectively, weaken and enhance negative conspecific distance-dependent mortality. Future research should identify specific agents of mortality, investigate the interactions among different enemy types and assess how global change may affect natural enemies and thus influence the strength of conspecific distance- and density-dependence.     

Do plants need niches? Some recent developments in plant community ecology

Species-rich plant communities appear to defy the competitive exclusion principle, showing relatively few obvious niche differences between coexisting species. Here we explore alternatives to the potentially endless search for new niche axes. Spatial aggregation in populations, non-transitive competition, episodes of density-independent mortality and various non-equilibrium theories allow trophically similar species to coexist for extended periods. In perennial plants or annuals with a seed pool, asynchrony between species in recruitment permits coexistence by the 'storage effect'. There is increasing evidence that species-specific herbivores and pathogens regulate populations of tropical trees to low levels at which competitive exclusion does not occur. The wide variety of alternatives to niche differentiation lead us to question whether plants need occupy different niches to coexist.     

Lower Within-Community Variance of Negative Density Dependence Increases Forest Diversity

Local abundance of adult trees impedes growth of conspecific seedlings through host-specific enemies, a mechanism first proposed by Janzen and Connell to explain plant diversity in forests. While several studies suggest the importance of this mechanism, there is still little information of how the variance of negative density dependence (NDD) affects diversity of forest communities. With computer simulations, we analyzed the impact of strength and variance of NDD within tree communities on species diversity. We show that stronger NDD leads to higher species diversity. Furthermore, lower range of strengths of NDD within a community increases species richness and decreases variance of species abundances. Our results show that, beyond the average strength of NDD, the variance of NDD is also crucially important to explain species diversity. This can explain the dissimilarity of biodiversity between tropical and temperate forest: highly diverse forests could have lower NDD variance. This report suggests that natural enemies and the variety of the magnitude of their effects can contribute to the maintenance of biodiversity.     

Habitat isolation affects plant–herbivore–enemy interactions on cherry trees

Understanding the interactions between herbivores and natural enemies in fragmented landscapes is essential for conservation biological control. Studies including multiple enemies affecting multiple herbivores, plant damage and growth are needed. Here, we separated independent effects of (1) isolation of cherry trees from woody habitat and (2) the amount of woody habitat in the surrounding landscape (500 m buffers) on interactions between different groups of herbivores with their natural enemies and resulting changes in the growth of young cherry trees. Most predatory arthropods declined with habitat isolation, except some aphid predators (ladybeetles and hoverflies). Herbivores either increased with isolation (herbivorous beetles) or showed no significant response (aphids). In contrast, the amount of woody habitat in the landscape was not relevant for herbivore–enemy interactions at the investigated scale. Plant growth was affected by bottom-up (nutrient availability) and top-down (aphid density) forces but did not change significantly with habitat amount or isolation. We conclude that herbivores can be released from natural enemies at isolated sites, in accordance with the hypothesis that habitat connectivity improves pest control. However, each herbivore group responded differently to the landscape context and had contrasting effects on the same host plant, demonstrating the difficulty to predict landscape effects on plant growth.