Insect herbivory on seedlings of rainforest trees: Effects of density and distance of conspecific and heterospecific neighbors.
ABSTRACT: Natural enemies of plants such as insect herbivores can contribute to structuring and maintaining plant diversity in tropical forests. Most research in this area has focused on the role of specialized enemies and the extent to which herbivory on individual plant species is density-dependent. Relatively few insect herbivores specialize on a single host plant species. Insect herbivores that feed on more than one plant species may link the regeneration dynamics of their host species through "apparent competition" or "apparent mutualism." We investigated herbivory and survival of seedlings of two tropical tree species (Cordia alliodora and Cordia bicolor) in the forests of Barro Colorado Island (Panama). We used experiments and observations to assess seedling fate in relation to the presence of conspecifics and heterospecifics across a range of spatial scales. Herbivory significantly increased seedling mortality and was highest at high local densities of C. alliodora seedlings. There was also evidence that high local densities of C. alliodora increased herbivory on co-occurring C. bicolor seedlings. Synthesis. The elevated rates of seedling herbivory at high densities of conspecifics documented in our study are consistent with the predictions of the Janzen-Connell hypothesis, which explains how so many plant species can coexist in tropical forests. Our data also highlight the possibility that herbivore-mediated density-dependence, facilitated by herbivores that feed on multiple plant species, can also occur across plant species. Enemy-mediated indirect effects of this sort have the potential to structure plant communities.
Project description:Animals can have both positive (e.g. via seed dispersal) and negative (e.g. via herbivory) impacts on plants. The net effects of these interactions remain difficult to predict and may be affected by overhunting and habitat disturbance, two widespread threats to tropical forests. Recent studies have documented their separate effects on plant recruitment but our understanding of how defaunation and logging interact to influence tropical tree communities is limited. From 2013 to 2016, we followed the fate of marked tree seedlings (n = 1489) from 81 genera in and outside experimental plots. Our plots differentially excluded small, medium and large-bodied mammal herbivores in logged and unlogged forest in Malaysian Borneo. We assessed the effects of experimental defaunation and logging on taxonomic diversity and plant trait (wood density, specific leaf area, fruit size) composition of seedling communities. Although seedling mortality was highest in the presence of all mammal herbivores (44%), defaunation alone did not alter taxonomic diversity nor plant trait composition. However, herbivores (across all body sizes) significantly reduced mean fruit size across the seedling community over time (95% confidence interval (CI): -0.09 to -0.01), particularly in logged forest (95% CI: -0.12 to -0.003). Our findings suggest that impacts of mammal herbivores on plant communities may be greater in forests with a history of disturbance and could subsequently affect plant functional traits and ecological processes associated with forest regeneration.
Project description:Herbivorous mammals and insect pre-dispersal seed predators are two types of herbivores that, despite their functional and morphological differences, tend to severely impact many plant species, highly decreasing their seed production and even imperiling the performance of their offspring through transgenerational effects. However, how they influence offspring resistance to herbivory remains largely unknown. In this study we experimentally examined the effects of ungulates and pre-dispersal seed predators on seed quality as well as on the emergence, survival and resistance to herbivory of the seedlings of a semiarid herb. We found that ungulates reduced seedling recruitment but increased seedling resistance to leaf miners. These effects were probably a consequence of insufficient carbon provisioning in seeds that reduced seed viability and provoked carbon limitation in seedlings. Pre-dispersal seed predators did not influence seedling recruitment, but seedlings from mothers damaged by ungulates and by pre-dispersal seed predators suffered less herbivory by grasshoppers. Remarkably, intra-individual differences in damage by pre-dispersal seed predators affected the rate of damage underwent by seedlings. That is, seedlings derived from fruits attacked by seed predators were more resistant to herbivores than siblings derived from un-attacked fruits in plant populations exposed to ungulates. To our knowledge, this is the first study reporting variation in transgenerational-induced resistance of seedlings from the same maternal plant. This study is a valuable contribution to the understanding of transgenerational effects of multiple herbivores and their implications for a deeper comprehension of the natural systems in which they co-occur.
Project description:<h4>Background and aims</h4>Seedling herbivory is an important selective filter in many plant communities. The removal of preferred food plants by both vertebrate and, more commonly, invertebrate herbivores can destroy entire seedling cohorts, and consequently dictate plant community assembly. Nevertheless, our understanding of how and why some seedlings are more prone to herbivore attack than their neighbours remains limited. For seedlings, where even minor tissue damage is fatal, avoiding contact with herbivores is probably advantageous and, on this basis, volatile organic compounds (VOCs) are strong candidates to fulfil a primary defensive role.<h4>Methods</h4>We quantified seedling selection by snails (Cornu aspersum) for 14 common, European grassland species. Seedling acceptability was subsequently compared with species-specific expression of constitutive secondary defence metabolites (CSDMs), and VOCs to determine their relative influence on seedling selection.<h4>Results</h4>We found no relationship between seedling acceptability and CSDMs, but seedling selection was strongly associated with VOC profiles. Monoterpenes (specifically β-ocimene) were identified as likely attractants, while green leaf volatiles (GLVs) (3-hexen-1-ol acetate) were strongly associated with low seedling acceptability.<h4>Conclusions</h4>By elucidating a relationship between VOCs and seedling acceptability, we contradict a long-held, but poorly tested, assumption that seedling selection by herbivores in (semi-)natural plant communities centres on CSDMs. Instead, our results corroborate recent work showing how GLVs, including 3-hexen-1-ol acetate, deter crop seedling selection by molluscs. Although our failure to establish any early-ontogenetic relationship between VOCs and CSDMs also suggests that the former do not 'advertise' possession of the latter, we nevertheless reveal the role that VOCs play in defending seedlings against herbivory before lethal damage occurs.
Project description:In tropical tree communities, processes occurring during early life stages play a critical role in shaping forest composition and diversity through differences in species' performance. Predicting the future of tropical forests depends on a solid understanding of the drivers of seedling survival. At the same time, factors determining spatial and temporal patterns of seedling survival can play a large role in permitting species coexistence in diverse communities. Using long-term data on the survival of more than 45 000 seedlings of 238 species in a Neotropical forest, we assessed the relative importance of key abiotic and biotic neighbourhood variables thought to influence individual seedling survival and tested whether species vary significantly in their responses to these variables, consistent with niche differences. At the community level, seedling survival was significantly correlated with plant size, topographic habitat, neighbourhood densities of conspecific seedlings, conspecific and heterospecific trees and annual variation in water availability, in descending order of effect size. Additionally, we found significant variation among species in their sensitivity to light and water availability, as well as in their survival within different topographic habitats, indicating the potential for niche differentiation among species that could allow for species coexistence.
Project description:Biodiversity loss may alter ecosystem processes, such as herbivory, a key driver of ecological functions in species-rich (sub)tropical forests. However, the mechanisms underlying such biodiversity effects remain poorly explored, as mostly effects of species richness - a very basic biodiversity measure - have been studied. Here, we analyze to what extent the functional and phylogenetic diversity of woody plant communities affect herbivory along a diversity gradient in a subtropical forest. We assessed the relative effects of morphological and chemical leaf traits and of plant phylogenetic diversity on individual-level variation in herbivory of dominant woody plant species across 27 forest stands in south-east China. Individual-level variation in herbivory was best explained by multivariate, community-level diversity of leaf chemical traits, in combination with community-weighted means of single traits and species-specific phylodiversity measures. These findings deviate from those based solely on trait variation within individual species. Our results indicate a strong impact of generalist herbivores and highlight the need to assess food-web specialization to determine the direction of biodiversity effects. With increasing plant species loss, but particularly with the concomitant loss of functional and phylogenetic diversity in these forests, the impact of herbivores will probably decrease - with consequences for the herbivore-mediated regulation of ecosystem functions.
Project description:1.Insect herbivory can strongly affect ecosystem processes, and its relationship with plant diversity is a central topic in biodiversity-functioning research. However, very little is known about this relationship from complex ecosystems dominated by long-lived individuals, such as forests, especially over gradients of high plant diversity.2.We analysed insect herbivory on saplings of 10 tree and shrub species across 27 forest stands differing in age and tree species richness in an extraordinarily diverse subtropical forest ecosystem in China. We tested whether plant species richness significantly influences folivory in these highly diverse forests or whether other factors play a more important role at such high levels of phytodiversity.3.Leaf damage was assessed on 58 297 leaves of 1284 saplings at the end of the rainy season in 2008, together with structural and abiotic stand characteristics.4.Species-specific mean damage of leaf area ranged from 3% to 16%. Herbivory increased with plant species richness even after accounting for potentially confounding effects of stand characteristics, of which stand age-related aspects most clearly covaried with herbivory. Intraspecific density dependence or other abiotic factors did not significantly influence overall herbivory across forest stands.5.Synthesis.The positive herbivory-plant diversity relationship indicates that effects related to hypotheses of resource concentration, according to which a reduction in damage by specialized herbivores might be expected as host plant concentration decreases with increasing plant diversity, do not seem to be major determinants for overall herbivory levels in our phytodiverse subtropical forest ecosystem. We discuss the potential role of host specificity of dominant herbivores, which are often expected to show a high degree of specialization in many (sub)tropical forests. In the forest system we studied, a much higher impact of polyphagous species than traditionally assumed might explain the observed patterns, as these species can profit from a broad dietary mix provided by high plant diversity. Further testing is needed to experimentally verify this assumption.
Project description: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.
Project description:Metalliferous soils can selectively shape plant species' physiology towards tolerance of high metal concentrations that are usually toxic to organisms. Some adapted plant species tolerate and accumulate metal in their tissues. These metals can serve as an elemental defence but can also decrease growth. Our investigation explored the capacity of natural metal accumulation in a tropical tree species, Eremanthus erythropappus (Asteraceae) and the effects of such bioaccumulation on plant responses to herbivory. Seedlings of E. erythropappus were grown in a glasshouse on soils that represented a metal concentration gradient (Al, Cu, Fe, Mn and Zn), and then the exposed plants were fed to the herbivores in a natural habitat. The effect of herbivory on plant growth was significantly mediated by foliar metal ion concentrations. The results suggest that herbivory effects on these plants change from negative to positive depending on soil metal concentration. Hence, these results provide quantitative evidence for a previously unsuspected interaction between herbivory and metal bioaccumulation on plant growth.
Project description:<h4>Background and aims</h4>Seedling herbivory is an important factor underlying plant community diversity and structure. While considerable research has characterized seedling defence in terms of resistance, very little is known about seedling tolerance of herbivory. Moreover, few studies have attempted to identify mechanisms of tolerance across a range of plant species.<h4>Methods</h4>Seedling tolerance of simulated herbivory was tested in a diverse pool of ten Hawaiian plant species, including several lobeliad species (family Campanulaceae), a grass, a herb and common woody trees and shrubs. Tolerance was measured as the relative survival and growth of damaged plants receiving 50 % defoliation with simultaneous jasmonic acid application compared with undamaged control plants, assessed 1·5 and 5 weeks after damage. Putative mechanisms of tolerance were measured, including photosynthetic parameters, light use efficiency, and biomass allocation reflecting growth priorities, and analysed using species-level regression analyses on tolerance indices.<h4>Key results</h4>No species fully tolerated 50 % defoliation at either harvest date, and simulated herbivory significantly reduced shoot as well as root biomass. Lobeliad species had particularly low tolerance. Species varied considerably in size, biomass allocation parameters and their constitutive (pre-damage) and induced (post-damage) photosynthetic parameters. However, only constitutive levels of non-photochemical quenching were significantly related to tolerance, indicating that species with more efficient light use (and less heat dissipation) are better at tolerating damage than species with high levels of heat dissipation.<h4>Conclusions</h4>Native Hawaiian plants expressed low tolerance to a conservative level of simulated herbivory. Root growth decreased in response to damage, but this was not associated with greater tolerance, suggesting this response may be due to allocation constraints following defoliation and not due to adaptive plasticity. Conservation of native island plants threatened by invasive herbivores should prioritize protection for seedlings for improved regeneration and the persistence of native plants in disturbed habitats.
Project description:The Janzen-Connell (JC) hypothesis provides a conceptual framework for explaining the maintenance of tree diversity in tropical forests. Its central tenet-that recruits experience high mortality near conspecifics and at high densities-assumes a degree of host specialization in interactions between plants and natural enemies. Studies confirming JC effects have focused primarily on spatial distributions of seedlings and saplings, leaving major knowledge gaps regarding the fate of seeds in soil and the specificity of the soilborne fungi that are their most important antagonists. Here we use a common garden experiment in a lowland tropical forest in Panama to show that communities of seed-infecting fungi are structured predominantly by plant species, with only minor influences of factors such as local soil type, forest characteristics, or time in soil (1-12 months). Inoculation experiments confirmed that fungi affected seed viability and germination in a host-specific manner and that effects on seed viability preceded seedling emergence. Seeds are critical components of reproduction for tropical trees, and the factors influencing their persistence, survival, and germination shape the populations of seedlings and saplings on which current perspectives regarding forest dynamics are based. Together these findings bring seed dynamics to light in the context of the JC hypothesis, implicating them directly in the processes that have emerged as critical for diversity maintenance in species-rich tropical forests.