Seed tannin composition of tropical plants.

Seeds collected from trees, shrubs and lianas growing on Barro Colorado Island, Panama, were analyzed for their content of phenolic compounds, oxidative activities and protein precipitation capacities. Proanthocyanidins and hydrolysable tannins were detected in one-third of 189 studied species. The most oxidatively active group of species were the ones containing prodelphinidins and ellagitannins whereas the species that had the highest protein precipitation capacity in relation to their total phenolics were the ones containing punicalagin. In addition, the oxidative activity and relative protein precipitation capacity were exceptionally high in the proanthocyanidin-rich genus Psychotria. This study offers a comprehensive overview on the tannin composition and the alkaline oxidative activities and protein precipitation capacities of the seeds of tropical plants.

Changes in oak (Quercus robur) photosynthesis after winter moth (Operophtera brumata) herbivory are not explained by changes in chemical or structural leaf traits.

Insect herbivores have the potential to change both physical and chemical traits of their host plant. Although the impacts of herbivores on their hosts have been widely studied, experiments assessing changes in multiple leaf traits or functions simultaneously are still rare. We experimentally tested whether herbivory by winter moth (Operophtera brumata) caterpillars and mechanical leaf wounding changed leaf mass per area, leaf area, leaf carbon and nitrogen content, and the concentrations of 27 polyphenol compounds on oak (Quercus robur) leaves. To investigate how potential changes in the studied traits affect leaf functioning, we related the traits to the rates of leaf photosynthesis and respiration. Overall, we did not detect any clear effects of herbivory or mechanical leaf damage on the chemical or physical leaf traits, despite clear effect of herbivory on photosynthesis. Rather, the trait variation was primarily driven by variation between individual trees. Only leaf nitrogen content and a subset of the studied polyphenol compounds correlated with photosynthesis and leaf respiration. Our results suggest that in our study system, abiotic conditions related to the growth location, variation between tree individuals, and seasonal trends in plant physiology are more important than herbivory in determining the distribution and composition of leaf chemical and structural traits.

A highly resolved food web for insect seed predators in a species-rich tropical forest.

The top-down and indirect effects of insects on plant communities depend on patterns of host use, which are often poorly documented, particularly in species-rich tropical forests. At Barro Colorado Island, Panama, we compiled the first food web quantifying trophic interactions between the majority of co-occurring woody plant species and their internally feeding insect seed predators. Our study is based on more than 200 000 fruits representing 478 plant species, associated with 369 insect species. Insect host-specificity was remarkably high: only 20% of seed predator species were associated with more than one plant species, while each tree species experienced seed predation from a median of two insect species. Phylogeny, but not plant traits, explained patterns of seed predator attack. These data suggest that seed predators are unlikely to mediate indirect interactions such as apparent competition between plant species, but are consistent with their proposed contribution to maintaining plant diversity via the Janzen-Connell mechanism.

Insect community structure covaries with host plant chemistry but is not affected by prior herbivory.

By feeding on plant tissue, insect herbivores can change several characteristics of their hosts. These changes have the potential to alter the quality of the plant for other herbivore species, potentially altering the structure of the community of species attacking the plant at a later point in time. We tested whether herbivory early in the season changes host plant performance, polyphenol chemistry, and the community structure of sessile herbivores later in the season. We experimentally manipulated densities of early-season moth caterpillars on a set of young oak trees and measured tree growth, reproduction, leaf chemistry, and the abundance and community composition of leafmining and galling species later in the season. The experimental manipulations of early-season herbivores did not affect late-season leaf chemistry or tree performance. Early-season herbivores had a weak negative effect on the abundance of gallers and a positive, tree-dependent effect on the overall diversity of late-season sessile herbivores. The chemical composition of leaves covaried with the species composition of the late-season leafmining and galling community. Both the chemical composition of the host tree and the late-season insect community structure were strongly affected by the growth location of the tree. Our results suggest that plant-mediated indirect effects between herbivores might play a limited role in this system, whereas the underlying variation in plant chemistry is an important factor structuring the associated insect community. Our results emphasize that factors other than prior herbivory can be important determinants of plant chemistry and the community composition of herbivores.

Dormancy-defense syndromes and tradeoffs between physical and chemical defenses in seeds of pioneer species.

Seeds of tropical pioneer trees have chemical and physical characteristics that determine their capacity to persist in the soil seed bank. These traits allow seeds to survive in the soil despite diverse predators and pathogens, and to germinate and recruit even decades after dispersal. Defenses in seedlings and adult plants often are described in terms of tradeoffs between chemical and physical defense, but the interplay of defensive strategies has been evaluated only rarely for seeds. Here we evaluated whether classes of seed defenses were negatively correlated across species (consistent with tradeoffs in defense strategies), or whether groups of traits formed associations across species (consistent with seed defense syndromes). Using 16 of the most common pioneer tree species in a neotropical lowland forest in Panama we investigated relationships among four physical traits (seed fracture resistance, seed coat thickness, seed permeability, and seed mass) and two chemical traits (number of phenolic compounds and phenolic peak area), and their association with seed persistence. In addition, seed toxicity was assessed with bioassays in which we evaluated the activity of seed extracts against representative fungal pathogens and a model invertebrate. We did not find univariate tradeoffs between chemical and physical defenses. Instead, we found that seed permeability - a trait that distinguishes physical dormancy from other dormancy types - was positively associated with chemical defense traits and negatively associated with physical defense traits. Using a linear discriminant analysis and a hierarchical cluster analysis we found evidence to distinguish three distinct seed defense syndromes that correspond directly with seed dormancy classes (i.e., quiescent, physical, and physiological). Our data suggest that short and long-term persistence of seeds can be achieved via two strategies: having permeable seeds that are well defended chemically, corresponding to the physiologically dormant defense syndrome; or having impermeable seeds that are well defended physically, corresponding to the physically dormant defense syndrome. In turn, transient seeds appear to have a lower degree of chemical and physical defenses, corresponding to the quiescent defense syndrome. Overall, we find that seed defense and seed dormancy are linked, suggesting that environmental pressures on seed persistence and for delayed germination can select for trait combinations defining distinct dormancy-defense syndromes.

Small-scale indirect plant responses to insect herbivory could have major impacts on canopy photosynthesis and isoprene emission.

Insect herbivores cause substantial changes in the leaves they attack, but their effects on the ecophysiology of neighbouring, nondamaged leaves have never been quantified in natural canopies. We studied how winter moth (Operophtera brumata), a common herbivore in temperate forests, affects the photosynthetic and isoprene emission rates of its host plant, the pedunculate oak (Quercus robur). Through a manipulative experiment, we measured leaves on shoots damaged by caterpillars or mechanically by cutting, or left completely intact. To quantify the effects at the canopy scale, we surveyed the extent and patterns of leaf area loss in the canopy. Herbivory reduced photosynthesis both in damaged leaves and in their intact neighbours. Isoprene emission rates significantly increased after mechanical leaf damage. When scaled up to canopy-level, herbivory reduced photosynthesis by 48 ± 10%. The indirect effects of herbivory on photosynthesis in undamaged leaves (40%) were much more important than the direct effects of leaf area loss (6%). If widespread across other plant-herbivore systems, these findings suggest that insect herbivory has major and previously underappreciated influences in modifying ecosystem carbon cycling, with potential effects on atmospheric chemistry.

Related herbivore species show similar temporal dynamics.

Within natural communities, different taxa display different dynamics in time. Why this is the case we do not fully know. This thwarts our ability to predict changes in community structure, which is important for both the conservation of rare species in natural communities and for the prediction of pest outbreaks in agriculture. Species sharing phylogeny, natural enemies and/or life-history traits have been hypothesized to share similar temporal dynamics. We operationalized these concepts into testing whether feeding guild, voltinism, similarity in parasitoid community and/or phylogenetic relatedness explained similarities in temporal dynamics among herbivorous community members. Focusing on two similar datasets from different geographical regions (Finland and Japan), we used asymmetric eigenvector maps as temporal variables to characterize species- and community-level dynamics of specialist insect herbivores on oak (Quercus). We then assessed whether feeding guild, voltinism, similarity in parasitoid community and/or phylogenetic relatedness explained similarities in temporal dynamics among taxa. Species-specific temporal dynamics varied widely, ranging from directional decline or increase to more complex patterns. Phylogeny was a clear predictor of similarity in temporal dynamics at the Finnish site, whereas for the Japanese site, the data were uninformative regarding a phylogenetic imprint. Voltinism, feeding guild and parasitoid overlap explained little variation at either location. Despite the rapid temporal dynamics observed at the level of individual species, these changes did not translate into any consistent temporal changes at the community level in either Finland or Japan. Overall, our findings offer no direct support for the notion that species sharing natural enemies and/or life-history traits would be characterized by similar temporal dynamics, but reveal a strong imprint of phylogenetic relatedness. As this phylogenetic signal cannot be attributed to guild, voltinism or parasitoids, it will likely derive from shared microhabitat, microclimate, anatomy, physiology or behaviour. This has important implications for predicting insect outbreaks and for informing insect conservation. We hope that future studies will assess the generality of our findings across plant-feeding insect communities and beyond, and establish the more precise mechanism(s) underlying the phylogenetic imprint.

Insect herbivory on seedlings of rainforest trees: Effects of density and distance of conspecific and heterospecific neighbors.

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.

Los enemigos naturales de plantas, tales como insectos herbívoros pueden contribuir a estructurar y mantener la diversidad arbórea en los bosques tropicales. La mayoría de investigaciones en ésta área se han centrado en el papel de enemigos especializados y en la medida en la que la herbivoría en plantas hospederas individuales depende de la densidad.Relativamente pocos insectos herbívoros se especializan en una única especie de planta hospedera. Los insectos herbívoros que se alimentan en más de una especie de planta pueden vincular la dinámica de regeneración de sus hospederas a través de "competencia aparente" o "mutualismo aparente".Nosotros investigamos la herbivoría y supervivencia de las plántulas de dos especies de árboles tropicales (Cordia alliodora y Cordia bicolor) en los bosques de la Isla de Barro Colorado (Panamá). Usamos experimentos y observaciones para evaluar el destino de las plántulas con relación a la densidad de conespecíficos y heteroespecíficos a través de un rango de escalas espaciales.La herbivoría aumentó significativamente la mortalidad de las plántulas, y fue significativamente más alta en densidades locales altas de C. alliodora. Hubo también evidencia que densidades locales altas de C. alliodora aumentaron la herbivoría en plántulas adyacentes de C. bicolor.Síntesis. Las elevadas tasas de herbivoría en plántulas a densidades altas de conespecíficos documentadas en nuestro estudio son consistentes con las predicciones de la hipótesis de Janzen­Connell, la cual provee una explicación a la alta diversidad de especies vegetales en los bosques tropicales. Nuestros datos también resaltan la posibilidad que efectos similares mediados por herbivoría puedan ocurrir a través de especies y sean facilitados por herbívoros especializados al nivel de género en lugar de especies. Efectos indirectos de ésta clase mediados por enemigos tienen el potencial de estructurar comunidades vegetales.

Pathogens and insect herbivores drive rainforest plant diversity and composition.

Tropical forests are important reservoirs of biodiversity, but the processes that maintain this diversity remain poorly understood. The Janzen-Connell hypothesis suggests that specialized natural enemies such as insect herbivores and fungal pathogens maintain high diversity by elevating mortality when plant species occur at high density (negative density dependence; NDD). NDD has been detected widely in tropical forests, but the prediction that NDD caused by insects and pathogens has a community-wide role in maintaining tropical plant diversity remains untested. We show experimentally that changes in plant diversity and species composition are caused by fungal pathogens and insect herbivores. Effective plant species richness increased across the seed-to-seedling transition, corresponding to large changes in species composition. Treating seeds and young seedlings with fungicides significantly reduced the diversity of the seedling assemblage, consistent with the Janzen-Connell hypothesis. Although suppressing insect herbivores using insecticides did not alter species diversity, it greatly increased seedling recruitment and caused a marked shift in seedling species composition. Overall, seedling recruitment was significantly reduced at high conspecific seed densities and this NDD was greatest for the species that were most abundant as seeds. Suppressing fungi reduced the negative effects of density on recruitment, confirming that the diversity-enhancing effect of fungi is mediated by NDD. Our study provides an overall test of the Janzen-Connell hypothesis and demonstrates the crucial role that insects and pathogens have both in structuring tropical plant communities and in maintaining their remarkable diversity.

Antagonistic interaction networks are structured independently of latitude and host guild.

An increase in species richness with decreasing latitude is a prominent pattern in nature. However, it remains unclear whether there are corresponding latitudinal gradients in the properties of ecological interaction networks. We investigated the structure of 216 quantitative antagonistic networks comprising insect hosts and their parasitoids, drawn from 28 studies from the High Arctic to the tropics. Key metrics of network structure were strongly affected by the size of the interaction matrix (i.e. the total number of interactions documented between individuals) and by the taxonomic diversity of the host taxa involved. After controlling for these sampling effects, quantitative networks showed no consistent structural patterns across latitude and host guilds, suggesting that there may be basic rules for how sets of antagonists interact with resource species. Furthermore, the strong association between network size and structure implies that many apparent spatial and temporal variations in network structure may prove to be artefacts.

Cross-kingdom interactions matter: fungal-mediated interactions structure an insect community on oak.

Although phytophagous insects and plant pathogens frequently share the same host plant, interactions among such phylogenetically distant taxa have received limited attention. Here, we place pathogens and insects in the context of a multitrophic-level community. Focusing on the invasive powdery mildew Erysiphe alphitoides and the insect community on oak (Quercus robur), we demonstrate that mildew-insect interactions may be mediated by both the host plant and by natural enemies, and that the trait-specific outcome of individual interactions can range from negative to positive. Moreover, mildew affects resource selection by insects, thereby modifying the distribution of a specialist herbivore at two spatial scales (within and among trees). Finally, a long-term survey suggests that species-specific responses to mildew scale up to generate landscape-level variation in the insect community structure. Overall, our results show that frequently overlooked cross-kingdom interactions may play a major role in structuring terrestrial plant-based communities.

Can we predict indirect interactions from quantitative food webs?--an experimental approach.

1. Shared enemies may link the dynamics of their prey. Recently, quantitative food webs have been used to infer that herbivorous insect species attacked by the same major parasitoid species will affect each other negatively through apparent competition. Nonetheless, theoretical work predicts several alternative outcomes, including positive effects. 2. In this paper, we use an experimental approach to link food web patterns to realized population dynamics. First, we construct a quantitative food web for three dominant leaf miner species on the oak Quercus robur. We then measure short- and long-term indirect effects by increasing leaf miner densities on individual trees. Finally, we test whether experimental results are consistent with natural leaf miner dynamics on unmanipulated trees. 3. The quantitative food web shows that all leaf miner species share a minimum of four parasitoid species. While only a small fraction of the parasitoid pool is shared among Tischeria ekebladella and each of two Phyllonorycter species, the parasitoid communities of the congeneric Phyllonorycter species overlap substantially. 4. Based on the structure of the food web, we predict strong short- and long-term indirect interactions between the Phyllonorycter species, and limited interactions between them and T. ekebladella. As T. ekebladella is the main source of its own parasitoids, we expect to find intraspecific density-dependent parasitism in this species. 5. Consistent with these predictions, parasitism in T. ekebladella was high on trees with high densities of conspecifics in the previous generation. Among leaf miner species sharing more parasitoids, we found positive rather than negative interactions among years. No short-term indirect interactions (i.e. indirect interactions within a single generation) were detected. 6. Overall, this study is the first to experimentally demonstrate that herbivores with overlapping parasitoid communities may exhibit independent population dynamics - or even apparent mutualism. Hence, it proves the potential for versatile indirect interactions in nature, and suggests that the link between patterns in food web structure and realized population dynamics should be verified by rigorous experiments.

Testing the Janzen-Connell mechanism: pathogens cause overcompensating density dependence in a tropical tree.

The Janzen-Connell hypothesis is a leading explanation for plant-species diversity in tropical forests. It suggests that specialized natural enemies decrease offspring survival at high densities beneath parents, giving locally rarer species an advantage. This mechanism, in its original form, assumes that density dependence is overcompensating: mortality must be disproportionately high at the highest densities, with few offspring recruiting below their parents. We tested this assumption using parallel shadehouse and field density-series experiments on seedlings of a tropical tree, Pleradenophora longicuspis. We found strong, overcompensating mortality driven by fungal pathogens, causing 90% (shadehouse) or 100% (field) mortality within 4 weeks of germination, and generating a negative relationship between initial and final seedling densities. Fungicide treatment led to much lower, density-independent, mortality. Overcompensating mortality was extremely rapid, and could be missed without detailed monitoring. Such dynamics may prevent dead trees from being replaced by conspecifics, promoting coexistence as envisioned by the Janzen-Connell hypothesis.

A meta-analysis of preference-performance relationships in phytophagous insects.

The extent to which behavioural choices reflect fine-tuned evolutionary adaptation remains an open debate. For herbivorous insects, the preference-performance hypothesis (PPH) states that female insects will evolve to oviposit on hosts on which their offspring fare best. In this study, we use meta-analysis to assess the balance of evidence for and against the PPH, and to evaluate the role of individual factors proposed to influence host selection by female insects. We do so in an explicitly bitrophic context (herbivores versus plants). Overall, our analyses offer clear support for the PPH: Offspring survive better on preferred plant types, and females lay more eggs on plant types conducive to offspring performance. We also found evidence for an effect of diet breadth on host choice: female preference for 'good quality plants' was stronger in oligophagous insects than in polyphagous insects. Nonetheless, despite the large numbers of preference-performance studies conducted to date, sample sizes in our meta-analysis are low due to the inconsistent format used by authors to present their results. To improve the situation, we invite authors to contribute to the data base emerging from this work, with the aim of reaching a strengthened synthesis of the subject field.

Spatial population structure of a specialist leaf-mining moth.

1. The spatial structure of natural populations may profoundly influence their dynamics. Depending on the frequency of movements among local populations and the consequent balance between local and regional population processes, earlier work has attempted to classify metapopulations into clear-cut categories, ranging from patchy populations to sets of remnant populations. In an alternative, dichotomous scheme, local populations have been classified as self-sustaining populations generating a surplus of individuals (sources) and those depending on immigration for persistence (sinks). 2. In this paper, we describe the spatial population structure of the leaf-mining moth Tischeria ekebladella, a specialist herbivore of the pedunculate oak Quercus robur. We relate moth dispersal to the distribution of oaks on Wattkast, a small island (5 km(2)) off the south-western coast of Finland. 3. We build a spatially realistic metapopulation model derived from assumptions concerning the behaviour of individual moths, and show that the model is able to explain part of the variation in observed patterns of occurrence and colonization. 4. While the species was always present on large trees, a considerable proportion of the local populations associated with small oaks showed extinction-recolonization dynamics. The vast majority of moth individuals occur on large trees. 5. According to model predictions, the dominance of local vs. regional processes in tree-specific moth dynamics varies drastically across the landscape. Most local populations may be defined broadly as 'sinks', as model simulations suggest that in the absence of immigration, only the largest oaks will sustain viable moth populations. Large trees in areas of high oak density will contribute most to the overall persistence of the metapopulation by acting as sources of moths colonizing other trees. 6. No single 'metapopulation type' will suffice to describe the oak-moth system. Instead, our study supports the notion that real populations are often a mix of earlier identified categories. The level to which local populations may persist after landscape modification will vary across the landscape, and sweeping classifications of metapopulations into single categories will contribute little to understanding how individual local populations contribute to the overall persistence of the system.

Resource selection by female moths in a heterogeneous environment: what is a poor girl to do?

1. According to the preference-performance hypothesis, female insects select resources that maximize offspring performance. To achieve high fitness, leaf miner females should then adjust their oviposition behaviour in response to leaf attributes signalling high host quality. 2. Here we investigate resource selection in Tischeria ekebladella, a leaf-mining moth of the pedunculate oak (Quercus robur), in relation to two alternative hypotheses: (1) females select their resources with respect to their future quality for developing larvae; or (2) temporal changes in resource quality prevent females from selecting the best larval resources. 3. Specifically, we test whether females show the strongest selection at the levels at which quality varies the most (shoots and leaves); whether they respond to specific leaf attributes (leaf size, phenolic content and conspecific eggs); and whether female preference is reflected in offspring performance. 4. Female choice of leaves was found to be non-random. Within trees, the females preferred certain shoots, but when the shoots were on different trees the degree of discrimination was about four times larger than when they were on the same trees. 5. While females typically lay more eggs on large leaves, this is not a result of active selection of large leaves, but rather a result of females moving at random and ovipositing at regular intervals. 6. The females in our study did not adjust their oviposition behaviour in response to leaf phenolic contents (as measured by the time of larval feeding). Neither did they avoid leaves with conspecific eggs. 7. Female choice of oviposition sites did not match patterns of offspring performance: there was no positive association between offspring survival and counts of eggs. 8. We propose that temporal variation in resource quality may prevent female moths from evaluating resource quality reliably. To compensate for this, females may adopt a risk-spreading strategy when selecting their resources.