Evaluating the Spatio-Temporal Factors that Structure Network Parameters of Plant-Herbivore Interactions

Despite the dynamic nature of ecological interactions, most studies on species networks offer static representations of their structure, constraining our understanding of the ecological mechanisms involved in their spatio-temporal stability. This is the first study to evaluate plant-herbivore interaction networks on a small spatio-temporal scale. Specifically, we simultaneously assessed the effect of host plant availability, habitat complexity and seasonality on the structure of plant-herbivore networks in a coastal tropical ecosystem. Our results revealed that changes in the host plant community resulting from seasonality and habitat structure are reflected not only in the herbivore community, but also in the emergent properties (network parameters) of the plant-herbivore interaction network such as connectance, selectiveness and modularity. Habitat conditions and periods that are most stressful favored the presence of less selective and susceptible herbivore species, resulting in increased connectance within networks. In contrast, the high degree of selectivennes (i.e. interaction specialization) and modularity of the networks under less stressful conditions was promoted by the diversification in resource use by herbivores. By analyzing networks at a small spatio-temporal scale we identified the ecological factors structuring this network such as habitat complexity and seasonality. Our research offers new evidence on the role of abiotic and biotic factors in the variation of the properties of species interaction networks.     

Relative impacts of environmental variation and evolutionary history on the nestedness and modularity of tree–herbivore networks

Nestedness and modularity are measures of ecological networks whose causative effects are little understood. We analyzed antagonistic plant–herbivore bipartite networks using common gardens in two contrasting environments comprised of aspen trees with differing evolutionary histories of defence against herbivores. These networks were tightly connected owing to a high level of specialization of arthropod herbivores that spend a large proportion of the life cycle on aspen. The gardens were separated by ten degrees of latitude with resultant differences in abiotic conditions. We evaluated network metrics and reported similar connectance between gardens but greater numbers of links per species in the northern common garden. Interaction matrices revealed clear nestedness, indicating subsetting of the bipartite interactions into specialist divisions, in both the environmental and evolutionary aspen groups, although nestedness values were only significant in the northern garden. Variation in plant vulnerability, measured as the frequency of herbivore specialization in the aspen population, was significantly partitioned by environment (common garden) but not by evolutionary origin of the aspens. Significant values of modularity were observed in all network matrices. Trait-matching indicated that growth traits, leaf morphology, and phenolic metabolites affected modular structure in both the garden and evolutionary groups, whereas extra-floral nectaries had little influence. Further examination of module configuration revealed that plant vulnerability explained considerable variance in web structure. The contrasting conditions between the two gardens resulted in bottom-up effects of the environment, which most strongly influenced the overall network architecture, however, the aspen groups with dissimilar evolutionary history also showed contrasting degrees of nestedness and modularity. Our research therefore shows that, while evolution does affect the structure of aspen–herbivore bipartite networks, the role of environmental variations is a dominant constraint.     

Global patterns of leaf defenses in oak species

Plant defensive traits drive patterns of herbivory and herbivore diversity among plant species. Over the past 30 years, several prominent hypotheses have predicted the association of plant defenses with particular abiotic environments or geographic regions. We used a strongly supported phylogeny of oaks to test whether defensive traits of 56 oak species are associated with particular components of their climatic niche. Climate predicted both the chemical leaf defenses and the physical leaf defenses of oaks, whether analyzed separately or in combination. Oak leaf defenses were higher at lower latitudes, and this latitudinal gradient could be explained entirely by climate. Using phylogenetic regression methods, we found that plant defenses tended to be greater in oak species that occur in regions with low temperature seasonality, mild winters, and low minimum precipitation, and that plant defenses may track the abiotic environment slowly over macroevolutionary time. The pattern of association we observed between oak leaf traits and abiotic environments was consistent with a combination of a seasonality gradient, which may relate to different herbivore pressures, and the resource availability hypothesis, which posits that herbivores exert greater selection on plants in resource-limited abiotic environments.     

Structure of trophic and mutualistic networks across broad environmental gradients

This study aims to understand how inherent ecological network structures of nestedness and modularity vary over large geographic scales with implications for community stability. Bipartite networks from previous research from 68 locations globally were analyzed. Using a meta‐analysis approach, we examine relationships between the structure of 22 trophic and 46 mutualistic bipartite networks in response to extensive gradients of temperature and precipitation. Network structures varied significantly across temperature gradients. Trophic networks showed decreasing modularity with increasing variation in temperature within years. Nestedness of mutualistic networks decreased with increasing temperature variability between years. Mean annual precipitation and variability of precipitation were not found to have significant influence on the structure of either trophic or mutualistic networks. By examining changes in ecological networks across large‐scale abiotic gradients, this study identifies temperature variability as a potential environmental mediator of community stability. Understanding these relationships contributes to our ability to predict responses of biodiversity to climate change at the community level.     

Comparing the plant–herbivore network topology of different insect guilds in Neotropical savannas

1. Herbivorous insects can be classified into several trophic guilds with different levels of specialisation on their host plants, which may influence the topological structure of their trophic networks. The present study tested the hypothesis that the structure of plant–herbivore networks differs between guilds of galling, sucking, and chewing insects. 2. Six areas of Neotropical savannas were studied in two localities in the North of the state of Minas Gerais, Brazil. In each area, interactions between plant and insect species were used to build networks for different guilds. 3. In total, 18 plant–herbivore networks were built, comprising 317 insect morphospecies, 50 plant species, and 489 distinct interactions. The networks were characterised using species richness and different network topological measures (connectance, modularity, nestedness, and specialisation). 4. The results obtained showed no difference in species richness, network size, and connectance between distinct insect herbivore guilds. However, it was found that modularity was higher for exophagous than galling insect networks and nestedness was higher for chewers than for other guilds. On the other hand, galling insect networks showed higher specialisation than exophagous insect networks, and sucking insect networks were more specialised than chewing insect networks. 5. The findings of the present study indicate that, although species richness did not differ between insect guilds of herbivores in Neotropical savannas, the topological structure of networks is sensitive to biological and ecological differences between these herbivore groups. The present study stands out as the first to systematically compare the network structure of different herbivore guilds in Neotropical savannas.     

Contrasting Effects of Land Use Intensity and Exotic Host Plants on the Specialization of Interactions in Plant-Herbivore Networks

Human land use tends to decrease the diversity of native plant species and facilitate the invasion and establishment of exotic ones. Such changes in land use and plant community composition usually have negative impacts on the assemblages of native herbivorous insects. Highly specialized herbivores are expected to be especially sensitive to land use intensification and the presence of exotic plant species because they are neither capable of consuming alternative plant species of the native flora nor exotic plant species. Therefore, higher levels of land use intensity might reduce the proportion of highly specialized herbivores, which ultimately would lead to changes in the specialization of interactions in plant-herbivore networks. This study investigates the community-wide effects of land use intensity on the degree of specialization of 72 plant-herbivore networks, including effects mediated by the increase in the proportion of exotic plant species. Contrary to our expectation, the net effect of land use intensity on network specialization was positive. However, this positive effect of land use intensity was partially canceled by an opposite effect of the proportion of exotic plant species on network specialization. When we analyzed networks composed exclusively of endophagous herbivores separately from those composed exclusively of exophagous herbivores, we found that only endophages showed a consistent change in network specialization at higher land use levels. Altogether, these results indicate that land use intensity is an important ecological driver of network specialization, by way of reducing the local host range of herbivore guilds with highly specialized feeding habits. However, because the effect of land use intensity is offset by an opposite effect owing to the proportion of exotic host species, the net effect of land use in a given herbivore assemblage will likely depend on the extent of the replacement of native host species with exotic ones.     

Community heterogeneity and the evolution of interactions between plants and insect herbivores

Plant communities vary tremendously in terms of productivity, species diversity, and genetic diversity within species. This vegetation heterogeneity can impact both the likelihood and strength of interactions between plants and insect herbivores. Because altering plant-herbivore interactions will likely impact the fitness of both partners, these ecological effects also have evolutionary consequences. We review several hypothesized and well-documented mechanisms whereby variation in the plant community alters the plant-herbivore interaction, discuss potential evolutionary outcomes of each of these ecological effects, and conclude by highlighting several avenues for future research. The underlying theme of this review is that the neighborhood of plants is an important determinant of insect attack, and this results in feedback effects on the plant community. Because plants exert selection on herbivore traits and, reciprocally, herbivores exert selection on plant-defense traits, variation in the plant community likely contributes to spatial and temporal variation in both plant and insect traits, which could influence macroevolutionary patterns.     

Seed‐dispersal networks respond differently to resource effects in open and forest habitats

While patterns in species diversity have been well studied across large‐scale environmental gradients, little is known about how species’ interaction networks change in response to abiotic and biotic factors across such gradients. Here we studied seed‐dispersal networks on 50 study plots distributed over ten different habitat types on the southern slopes of Mt Kilimanjaro, Tanzania, to disentangle the effects of climate, habitat structure, fruit diversity and fruit availability on different measures of interaction diversity. We used direct observations to record the interactions of frugivorous birds and mammals with fleshy‐fruited plants and recorded climatic conditions, habitat structure, fruit diversity and availability. We found that Shannon interaction diversity (H) increased with fruit diversity and availability, whereas interaction evenness (E_H) and network specialization (H₂) responded differently to changes in fruit availability depending on habitat structure. The direction of the effects of fruit availability on E_H and H₂ differed between open habitats at the mountain base and structurally complex habitats in the forest belt. Our findings illustrate that interaction networks react differently to changes in environmental conditions in different ecosystems. Hence, our findings demonstrate that future projections of network structure and associated ecosystem functions need to account for habitat differences among ecosystems.     

Evolution of nutrient uptake reveals a trade-off in the ecological stoichiometry of plant-herbivore interactions

Nutrient limitation determines the primary production and species composition of many ecosystems. Here we apply an adaptive dynamics approach to investigate evolution of the ecological stoichiometry of primary producers and its implications for plant-herbivore interactions. The model predicts a trade-off between the competitive ability and grazing susceptibility of primary producers, driven by changes in their nutrient uptake rates. High nutrient uptake rates enhance the competitiveness of primary producers but also increase their nutritional quality for herbivores. This trade-off enables coexistence of nutrient exploiters and grazing avoiders. If herbivores are not selective, evolution favors runaway selection toward high nutrient uptake rates of the primary producers. However, if herbivores select nutritious food, the model predicts an evolutionarily stable strategy with lower nutrient uptake rates. When the model is parameterized for phytoplankton and zooplankton, the evolutionary dynamics result in plant-herbivore oscillations at ecological timescales, especially in environments with high nutrient availability and low selectivity of the herbivores. High herbivore selectivity stabilizes the community dynamics. These model predictions show that evolution permits nonequilibrium dynamics in plant-herbivore communities and shed new light on the evolutionary forces that shape the ecological stoichiometry of primary producers.     

Environmental gradients and herbivore feeding preferences in coastal salt marshes

Current theories of plant-herbivore interactions suggest that plants may differ in palatability to herbivores as a function of abiotic stress; however, studies of these theories have produced mixed results. We compared the palatability of eight common salt marsh plants that occur across elevational and salinity stress gradients to six common leaf-chewing herbivores to determine patterns of plant palatability. The palatability of every plant species varied across gradients of abiotic stress in at least one comparison, and over half of the comparisons indicated significant differences in palatability. The direction of the preferences, however, was dependent on the plant and herbivore species studied, suggesting that different types of stress affect plants in different ways, that different plant species respond differently to stress, and that different herbivore species measure plant quality in different ways. Overall, 51% of the variation in the strength of the feeding preferences could be explained by a knowledge of the strength of the stress gradient and the type of gradient, plant and herbivore studied. This suggests that the prospects are good for a more complex, conditional theory of plant stress and herbivore feeding preferences that is based on a mechanistic understanding of plant physiology and the factors underlying herbivore feeding preferences.     

Natural enemies of herbivores maintain their biological control potential under short‐term exposure to future CO2, temperature,and precipitation patterns

Climate change will profoundly alter the physiology and ecology of plants, insect herbivores, and their natural enemies, resulting in strong effects on multitrophic interactions. Yet, manipulative studies that investigate the direct combined impacts of changes in CO₂, temperature, and precipitation on the third trophic level remain rare. Here, we assessed how exposure to elevated CO₂, increased temperature, and decreased precipitation directly affect the performance and predation success of species from four major groups of herbivore natural enemies: an entomopathogenic nematode, a wolf spider, a ladybug, and a parasitoid wasp. A four‐day exposure to future climatic conditions (RCP 8.5), entailing a 28% decrease in precipitation, a 3.4°C raise in temperature, and a 400 ppm increase in CO₂ levels, slightly reduced the survival of entomopathogenic nematodes, but had no effect on the survival of other species. Predation success was not negatively affected in any of the tested species, but it was even increased for wolf spiders and entomopathogenic nematodes. Factorial manipulation of climate variables revealed a positive effect of reduced soil moisture on nematode infectivity, but not of increased temperature or elevated CO₂. These results suggest that natural enemies of herbivores may be well adapted to short‐term changes in climatic conditions. These findings provide mechanistic insights that will inform future efforts to disentangle the complex interplay of biotic and abiotic factors that drive climate‐dependent changes in multitrophic interaction networks.     

Interference competition and temporal niche shifts: elephants and herbivore communities at waterholes

Scarcity of resources may result in high levels of animal aggregation; interference competition can occur in such a scenario and play a role in resource acquisition. Here, we test the hypothesis that animals could minimize interference competition by shifting their temporal niches in relation to competitors. In Hwange National Park, Zimbabwe, we monitored waterholes in order to study agonistic interactions between elephants and other herbivore species. We also used a long-term data set from a yearly survey of waterhole attendance by herbivores to evaluate the influence of the presence of elephants on the use of waterholes by other herbivore species. Our results show that in drier years, waterholes are crowded with elephants early in the afternoon. In general, the species most affected by interference competition with elephants shift their temporal niches at the waterholes, thus maintaining a constant temporal overlaps with elephants. The species less affected by interference competition with elephants show no temporal niche shifts and increase their temporal overlap with elephants at waterholes, as predicted from a noncompetition hypothesis. This study provides evidence that interference competition with a behaviorally dominant large species influences the temporal niches of smaller species, and suggests that the potential costs associated with interference between elephants and other herbivores at waterholes are linked to shifts in diurnal activities rather than interactions and water acquisition itself.     

Competition and facilitation in multispecies plant-herbivore systems of productive environments

We develop a multispecies plant-herbivore model to explore how plant competition for light and the selectivity of herbivores affect abundance patterns of plants and herbivores along productivity gradients. The model considers a small and a tall plant species, a generalist herbivore, and a selective herbivore. The selective herbivore feeds only on the small plant species. In the absence of the generalist herbivore, the tall plant species becomes increasingly dominant with increasing productivity, and the small plant and its selective herbivore disappear. The model shows that generalist herbivores can facilitate selective herbivores by suppressing competition for light. This favours the small plant species, and thereby the selective herbivores. The model predictions are qualitatively consistent with field studies of multispecies plant-herbivore systems.     

Causes and consequences of migration by large herbivores

Many populations of large herbivores migrate seasonally between discrete home ranges. Current evidence suggests that migration is generally selected for as a means of enhancing access to high quality food and/or reducing the risk of predation. The relative importance of these alternative selection pressures should depend on the demographic circumstances facing a given population. Seasonal migration also has important implications for the structure and dynamics of large herbivore communities. Migrants should tend to be regulated by food availability, while residents should tend to be regulated by predators As a result, migrants should often outnumber residents by a considerable margin - a pattern seen in several tropical and temperate ecosystems. Differences in the mode of regulation could also imply that competition for resources will be weak in purely resident assemblages, but strong in communities dominated by migrants. Continual grazing by resident herbivores can sometimes lead to degeneration of vegetation, while systems supporting migrants are apparently more resilient. This implies that migration can have an important impact on the long-term persistence of plant-herbivore systems, particularly in areas with slow rates of vegetation regeneration.     

Phytochemical diversity impacts herbivory in a tropical rainforest tree community

Metabolomics provides an unprecedented window into diverse plant secondary metabolites that represent a potentially critical niche dimension in tropical forests underlying species coexistence. Here, we used untargeted metabolomics to evaluate chemical composition of 358 tree species and its relationship with phylogeny and variation in light environment, soil nutrients, and insect herbivore leaf damage in a tropical rainforest plot. We report no phylogenetic signal in most compound classes, indicating rapid diversification in tree metabolomes. We found that locally co-occurring species were more chemically dissimilar than random and that local chemical dispersion and metabolite diversity were associated with lower herbivory, especially that of specialist insect herbivores. Our results highlight the role of secondary metabolites in mediating plant–herbivore interactions and their potential to facilitate niche differentiation in a manner that contributes to species coexistence. Furthermore, our findings suggest that specialist herbivore pressure is an important mechanism promoting phytochemical diversity in tropical forests.     

Oak-insect herbivore interactions along a temperature and precipitation gradient

The interactions between herbivorous insects and their host plants are expected to be influenced by changing climates. Modern oaks provide an excellent system to examine this assumption because their interactions with herbivores occur over broad climatic and spatial scales, they vary in their defensive and nutritional investment in leaves by being deciduous or evergreen, and their insect herbivores range from generalists to highly specialized feeders. In this study, we surveyed leaf-litter samples of four oak species along an elevation gradient, from coastal northern California, USA, to the upper montane woodlands of the Sierra Nevada, to examine the relationship between climatic factors (mean annual temperature and precipitation) and oak herbivory levels at multiple scales; across all oak species pooled, between evergreen and deciduous species and within species.Overall, temperature and precipitation did not appear to have a significant effect on most measures of total herbivore damage (percent leaves damaged per tree, percent leaf area removed and average number of feeding damage marks per leaf) and the strongest predictor of herbivore damage overall was the identity of the host species. However, increases in precipitation were correlated with an increase in the actual leaf area removed, and specialized insects, such as those that make leaf mines and galls, were the most sensitive to differences in precipitation levels. This suggests that the effects of changing climate on some plant–insect interactions is less likely to result in broad scale increases in damage with increasing temperatures or changing precipitation levels, but is rather more likely to be dependent on the type of herbivore (specialist vs. generalist) and the scale (species vs. community) over which the effect is examined.     

High specialization and limited structural change in plant‐herbivore networks along a successional chronosequence in tropical montane forest

Secondary succession is well‐understood, to the point of being predictable for plant communities, but the successional changes in plant‐herbivore interactions remains poorly explored. This is particularly true for tropical forests despite the increasing importance of early successional stages in tropical landscapes. Deriving expectations from successional theory, we examine properties of plant‐herbivore interaction networks while accounting for host phylogenetic structure along a succession chronosequence in montane rainforest in Papua New Guinea. We present one of the most comprehensive successional investigations of interaction networks, equating to > 40 person years of field sampling, and one of the few focused on montane tropical forests. We use a series of nine 0.2 ha forest plots across young secondary, mature secondary and primary montane forest, sampled almost completely for woody plants and larval leaf chewers (Lepidoptera) using forest felling. These networks comprised of 12 357 plant‐herbivore interactions and were analysed using quantitative network metrics, a phylogenetically controlled host‐use index and a qualitative network beta diversity measure. Network structural changes were low and specialisation metrics surprisingly similar throughout succession, despite high network beta diversity. Herbivore abundance was greatest in the earliest stages, and hosts here had more species‐rich herbivore assemblages, presumably reflecting higher palatability due to lower defensive investment. All herbivore communities were highly specialised, using a phylogenetically narrow set of hosts, while host phylogenetic diversity itself decreased throughout the chronosequence. Relatively high phylogenetic diversity, and thus high diversity of plant defenses, in early succession forest may result in herbivores feeding on fewer hosts than expected. Successional theory, derived primarily from temperate systems, is limited in predicting tropical host‐herbivore interactions. All succession stages harbour diverse and unique interaction networks, which together with largely similar network structures and consistent host use patterns, suggests general rules of assembly may apply to these systems.     

The specialization and structure of antagonistic and mutualistic networks of beetles on rainforest canopy trees

Different kinds of species interactions can lead to different structures within ecological networks. Antagonistic interactions (such as between herbivores and host plants) often promote increasing host specificity within a compartmentalized network structure, whereas mutualistic networks (such as pollination networks) are associated with higher levels of generalization and form nested network structures. However, we recently showed that the host specificity of flower‐visiting beetles from three different feeding guilds (herbivores, fungivores, and predators) in an Australian rainforest canopy was equal to that of herbivores on leaves, suggesting that antagonistic herbivores on leaves are no more specialized than flower‐visitors. We therefore set out to test whether similarities in the host specificity of these different assemblages reflect similarities in underlying network structures. As shown before at the species level, mutualistic communities on flowers showed levels of specialization at the network scale similar to those of the antagonistic herbivore community on leaves. However, the network structure differed, with flower‐visiting assemblages displaying a significantly more nested structure than folivores, and folivores displaying a significantly more compartmentalized structure than flower‐visitors. These results, which need further testing in other forest systems, demonstrate that both antagonistic and mutualistic interactions can result in equally high levels of host specialization among beetle assemblages in tropical rainforests. If this is a widespread phenomenon, it may alter our current perceptions of food web dynamics, species diversity patterns, and co‐evolution in tropical rainforests. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2015, 114 , 287–295.     

Evolutionary history and precipitation seasonality shape niche overlap in Neotropical bat–plant pollination networks

Species interactions are one dimension of a niche. Niche overlap arises when two species share an interaction partner. In pollination systems, environmental and biotic factors affect niche overlap. Here, we explored the effects of climate seasonality, plant and bat richness, morphological traits, and phylogenetic distance in shaping the niche overlap of Neotropical bat–plant pollination networks. We examined a dataset of 22 bat–plant pollination networks in the Neotropical region. We measured niche overlap in bats and plants with the Morisita-Horn index (Ĉ_H) and used a SAR model to test the relationships between niche overlap and both abiotic and biotic factors. We found a lower niche overlap among bats in communities composed of phylogenetically distant bat species. Moreover, plant and bat overlap was lower in regions with higher precipitation seasonality. Our results indicate that climate seasonality and bat evolutionary history drive niche overlap in Neotropical bat–plant pollination interactions. These findings suggest that a higher precipitation seasonality promotes the emergence of temporal modules, which reduces niche overlap, likely due to seasonal species phenologies. Furthermore, the method used to record the interactions affects the degree of niche overlap. Interactions recorded with pollen samples tend to have higher niche overlap than direct observations. The responses of morphological traits and phylogenetic distances in bat niche overlap were uncoupled, suggesting an effect of historical processes independent of morphological traits. Our findings reinforce the importance of evolutionary history and ecological processes in imprinting patterns of interaction niche overlap.