Ecosystem engineering and leaf quality together affect arthropod community structure and diversity on white oak (Quercus alba L.).

Shelter building caterpillars act as ecosystem engineers by creating and maintaining leaf shelters, which are then colonized by other arthropods. Foliage quality has been shown to influence initial colonization by shelter-building caterpillars. However, the effects of plant quality on the interactions between ecosystem engineers and their communities have yet to be studied at the whole plant level. We examined how leaf tying caterpillars, as ecosystem engineers, impact arthropod communities on Quercus alba (white oak), and the modifying effect of foliage quality on these interactions. We removed all leaf tying caterpillars and leaf ties on 35 Q. alba saplings during the season when leaf tying caterpillars were active (June-September), and compared these leaf tie removal trees to 35 control trees whose leaf ties were left intact. Removal of these ecosystem engineers had no impact on overall arthropod species richness, but reduced species diversity, and overall arthropod abundance and that of most guilds, and changed the structure of the arthropod community as the season progressed. There was an increase in plant-level species richness with increasing number of leaf ties, consistent with Habitat Diversity Hypothesis. In turn, total arthropod density, and that of both leaf tying caterpillars and free-feeding caterpillars were affected by foliar tannin and nitrogen concentrations, and leaf water content. The engineering effect was greatest on low quality plants, consistent with the Stress-Gradient Hypothesis. Our results demonstrate that interactions between ecosystem engineering and plant quality together determine community structure of arthropods on Q. alba in Missouri.

Climate variability and aridity modulate the role of leaf shelters for arthropods: A global experiment.

Current climate change is disrupting biotic interactions and eroding biodiversity worldwide. However, species sensitive to aridity, high temperatures, and climate variability might find shelter in microclimatic refuges, such as leaf rolls built by arthropods. To explore how the importance of leaf shelters for terrestrial arthropods changes with latitude, elevation, and climate, we conducted a distributed experiment comparing arthropods in leaf rolls versus control leaves across 52 sites along an 11,790 km latitudinal gradient. We then probed the impact of short- versus long-term climatic impacts on roll use, by comparing the relative impact of conditions during the experiment versus average, baseline conditions at the site. Leaf shelters supported larger organisms and higher arthropod biomass and species diversity than non-rolled control leaves. However, the magnitude of the leaf rolls' effect differed between long- and short-term climate conditions, metrics (species richness, biomass, and body size), and trophic groups (predators vs. herbivores). The effect of leaf rolls on predator richness was influenced only by baseline climate, increasing in magnitude in regions experiencing increased long-term aridity, regardless of latitude, elevation, and weather during the experiment. This suggests that shelter use by predators may be innate, and thus, driven by natural selection. In contrast, the effect of leaf rolls on predator biomass and predator body size decreased with increasing temperature, and increased with increasing precipitation, respectively, during the experiment. The magnitude of shelter usage by herbivores increased with the abundance of predators and decreased with increasing temperature during the experiment. Taken together, these results highlight that leaf roll use may have both proximal and ultimate causes. Projected increases in climate variability and aridity are, therefore, likely to increase the importance of biotic refugia in mitigating the effects of climate change on species persistence.

Ecosystem engineering in the arboreal realm: heterogeneity of wood-boring beetle cavities and their use by cavity-nesting ants.

Wood-boring beetle larvae act as ecosystem engineers by creating stem cavities that are used secondarily as nests by many arboreal ant species. Understanding the heterogeneity and distribution of available cavities and their use by ants is therefore key to understanding arboreal ant community assembly and diversity. Our goals were to quantify the abundance and diversity of beetle-produced cavity resources in a tropical canopy, reveal how ants use these resources, and determine which characteristics of the cavity resource contribute to ant use. We dissected branches from six common tree species in the Brazilian Cerrado savanna, measuring cavity characteristics and identifying the occupants. We sampled 2310 individual cavities, 576 of which were used as nests by 25 arboreal ant species. We found significant differences among tree species in the proportion of stem length bored by beetles, the number of cavities per stem length, average entrance-hole size, and the distribution of cavity volumes. The likelihood that a cavity was occupied was greater for cavities with larger entrance-hole sizes and larger volumes. In particular, there was a strong positive correlation between mean head diameters of ant species and the mean entrance-hole diameter of the cavities occupied by those ant species. Wood-boring beetles contribute to the structuring of the Cerrado ant community by differentially attacking the available tree species. In so doing, the beetles provide a wide range of entrance-hole sizes which ant species partition based on their body size, and large volume cavities that ants appear to prefer.

Revisiting ecological dominance in arboreal ants: how dominant usage of nesting resources shapes community assembly.

Ecologically dominant species can shape the assembly of ecological communities via altering competitive outcomes. Moreover, these effects may be amplified under limited niche differentiation. Nevertheless, the influences of ecological dominance and niche differentiation on assembly are rarely considered together. Here, we provide a novel examination of dominance in a diverse arboreal ant community, defining dominance by the prevalent usage of nesting resources and addressing how it influences community assembly. We first used a series of quantitative observational and experimental studies to address the natural nesting ecology, colony incidence on surveyed trees, and level of dominance over newly available nesting resources by our focal species, Cephalotes pusillus. The experimental studies were then used further to examine whether C. pusillus shapes assembly via an influence on cavity usage by co-occurring species. C. pusillus was confirmed as a dominant user of cavity nesting resources, with highly generalized nesting ecology, occupying about 50% of the trees within the focal system, and accounting for more than a third of new cavity occupation in experiments. Our experiments showed further that the presence of C. pusillus was associated with modest effects on species richness, but significant decreases in cavity-occupation levels and significant shifts in the entrance-size usage by co-occurring species. These results indicate that C. pusillus, as a dominant user of nesting resources, shapes assembly at multiple levels. Broadly, our findings highlight that complex interactions between a dominant species and the resource-usage patterns of other species can underlie species assembly in diverse ecological communities.

Tri-trophic interactions: bridging species, communities and ecosystems.

A vast body of research demonstrates that many ecological and evolutionary processes can only be understood from a tri-trophic viewpoint, that is, one that moves beyond the pairwise interactions of neighbouring trophic levels to consider the emergent features of interactions among multiple trophic levels. Despite its unifying potential, tri-trophic research has been fragmented, following two distinct paths. One has focused on the population biology and evolutionary ecology of simple food chains of interacting species. The other has focused on bottom-up and top-down controls over the distribution of biomass across trophic levels and other ecosystem-level variables. Here, we propose pathways to bridge these two long-standing perspectives. We argue that an expanded theory of tri-trophic interactions (TTIs) can unify our understanding of biological processes across scales and levels of organisation, ranging from species evolution and pairwise interactions to community structure and ecosystem function. To do so requires addressing how community structure and ecosystem function arise as emergent properties of component TTIs, and, in turn, how species traits and TTIs are shaped by the ecosystem processes and the abiotic environment in which they are embedded. We conclude that novel insights will come from applying tri-trophic theory systematically across all levels of biological organisation.

The global distribution of diet breadth in insect herbivores.

Understanding variation in resource specialization is important for progress on issues that include coevolution, community assembly, ecosystem processes, and the latitudinal gradient of species richness. Herbivorous insects are useful models for studying resource specialization, and the interaction between plants and herbivorous insects is one of the most common and consequential ecological associations on the planet. However, uncertainty persists regarding fundamental features of herbivore diet breadth, including its relationship to latitude and plant species richness. Here, we use a global dataset to investigate host range for over 7,500 insect herbivore species covering a wide taxonomic breadth and interacting with more than 2,000 species of plants in 165 families. We ask whether relatively specialized and generalized herbivores represent a dichotomy rather than a continuum from few to many host families and species attacked and whether diet breadth changes with increasing plant species richness toward the tropics. Across geographic regions and taxonomic subsets of the data, we find that the distribution of diet breadth is fit well by a discrete, truncated Pareto power law characterized by the predominance of specialized herbivores and a long, thin tail of more generalized species. Both the taxonomic and phylogenetic distributions of diet breadth shift globally with latitude, consistent with a higher frequency of specialized insects in tropical regions. We also find that more diverse lineages of plants support assemblages of relatively more specialized herbivores and that the global distribution of plant diversity contributes to but does not fully explain the latitudinal gradient in insect herbivore specialization.

Unravelling Darwin's entangled bank: architecture and robustness of mutualistic networks with multiple interaction types.

Trying to unravel Darwin's entangled bank further, we describe the architecture of a network involving multiple forms of mutualism (pollination by animals, seed dispersal by birds and plant protection by ants) and evaluate whether this multi-network shows evidence of a structure that promotes robustness. We found that species differed strongly in their contributions to the organization of the multi-interaction network, and that only a few species contributed to the structuring of these patterns. Moreover, we observed that the multi-interaction networks did not enhance community robustness compared with each of the three independent mutualistic networks when analysed across a range of simulated scenarios of species extinction. By simulating the removal of highly interacting species, we observed that, overall, these species enhance network nestedness and robustness, but decrease modularity. We discuss how the organization of interlinked mutualistic networks may be essential for the maintenance of ecological communities, and therefore the long-term ecological and evolutionary dynamics of interactive, species-rich communities. We suggest that conserving these keystone mutualists and their interactions is crucial to the persistence of species-rich mutualistic assemblages, mainly because they support other species and shape the network organization.

Chemical similarity and local community assembly in the species rich tropical genus Piper.

Community ecologists have strived to find mechanisms that mediate the assembly of natural communities. Recent evidence suggests that natural enemies could play an important role in the assembly of hyper-diverse tropical plant systems. Classic ecological theory predicts that in order for coexistence to occur, species differences must be maximized across biologically important niche dimensions. For plant-herbivore interactions, it has been recently suggested that, within a particular community, plant species that maximize the difference in chemical defense profiles compared to neighboring taxa will have a relative competitive advantage. Here we tested the hypothesis that plant chemical diversity can affect local community composition in the hyper-diverse genus Piper at a lowland wet forest location in Costa Rica. We first characterized the chemical composition of 27 of the most locally abundant species of Piper. We then tested whether species with different chemical compositions were more likely to coexist. Finally, we assessed the degree to which Piper phylogenetic relationships are related to differences in secondary chemical composition and community assembly. We found that, on average, co-occurring species were more likely to differ in chemical composition than expected by chance. Contrary to expectations, there was no phylogenetic signal for overall secondary chemical composition. In addition we found that species in local communities were, on average, more phylogenetically closely related than expected by chance, suggesting that functional traits other than those measured here also influence local assembly. We propose that selection by herbivores for divergent chemistries between closely related species facilitates the coexistence of a high diversity of congeneric taxa via apparent competition.

Ode to Ehrlich and Raven or how herbivorous insects might drive plant speciation.

Fifty years ago, Ehrlich and Raven proposed that insect herbivores have driven much of plant speciation, particularly at tropical latitudes. There have been no explicit tests of their hypotheses. Indeed there were no proposed mechanisms either at the time or since by which herbivores might generate new plant species. Here we outline two main classes of mechanisms, prezygotic and postzygotic, with a number of scenarios in each by which herbivore-driven changes in host plant secondary chemistry might lead to new plant lineage production. The former apply mainly to a sympatric model of speciation while the latter apply to a parapatric or allopatric model. Our review suggests that the steps of each mechanism are known to occur individually in many different systems, but no scenario has been thoroughly investigated in any one system. Nevertheless, studies of Dalechampia and its herbivores and pollinators, and patterns of defense tradeoffs in trees on different soil types in the Peruvian Amazon provide evidence consistent with the original hypotheses of Ehrlich and Raven. For herbivores to drive sympatric speciation, our findings suggest that interactions with both their herbivores and their pollinators should be considered. In contrast, herbivores may drive speciation allopatrically without any influence by pollinators. Finally, there is evidence that these mechanisms are more likely to occur at low latitudes and thus more likely to produce new species in the tropics. The mechanisms we outline provide a predictive framework for further study of the general role that herbivores play in diversification of their host plants.

The impact of plant chemical diversity on plant-herbivore interactions at the community level.

Understanding the role of diversity in ecosystem processes and species interactions is a central goal of ecology. For plant-herbivore interactions, it has been hypothesized that when plant species diversity is reduced, loss of plant biomass to herbivores increases. Although long-standing, this hypothesis has received mixed support. Increasing plant chemical diversity with increasing plant taxonomic diversity is likely to be important for plant-herbivore interactions at the community level, but the role of chemical diversity is unexplored. Here we assess the effect of volatile chemical diversity on patterns of herbivore damage in naturally occurring patches of Piper (Piperaceae) shrubs in a Costa Rican lowland wet forest. Volatile chemical diversity negatively affected total, specialist, and generalist herbivore damage. Furthermore, there were differences between the effects of high-volatility and low-volatility chemical diversity on herbivore damage. High-volatility diversity reduced specialist herbivory, while low-volatility diversity reduced generalist herbivory. Our data suggest that, although increased plant diversity is expected to reduce average herbivore damage, this pattern is likely mediated by the diversity of defensive compounds and general classes of anti-herbivore traits, as well as the degree of specialization of the herbivores attacking those plants.

Extrafloral nectaries have a limited effect on the structure of arboreal ant communities in a Neotropical savanna.

How environmental contexts shape the strength of species interactions, and their influence on community structure, remains a key focus for the field of community ecology. In particular, the extent to which local competitive interactions impact community structure, and whether this differs across contexts, persists as a general issue that is unresolved across a broad range of animal systems. Studies of arboreal ants have shown that competitive interactions over carbon-rich exudates from extrafloral nectaries (EFNs) and homopteran aggregations can have positive and negative effects on the local abundances of individual species. Nevertheless, it is still unclear the extent to which these local effects scale to community-level effects. Here we address the role of food from extrafloral nectaries on the structure of arboreal ant communities in a savanna of central Brazil. We did this with a combination of a diversity survey across tree species with and without EFNs, a repeated survey at times of peak EFN activity, and testing of our survey findings with two experimental manipulations of nectar availability that also provided supplementary nesting cavities. Species richness, but not composition, differed significantly between trees with and without EFNs. However, trees with EFNs had, on average, only 9% more species than those without EFNs. Furthermore, ant species richness did not differ significantly between periods of high and low EFN activity. Although nectar supplementation significantly affected nest occupation rates, this difference was seen solely in. the experiment with a massive supply of nectar and there was no effect on total ant richness or identity of the focal assemblages. Our findings suggest that the effects of extrafloral nectar on the abundances of arboreal ants at local scales do not scale to a strong structuring force at the community level. We suggest that this is most likely due to a lack of specificity of community members for EFN tree species, and the diffuse temporal and spatial nature of the availability of active EFNs. These properties mean that observable short-lived activity and competition over particular EFNs does not ultimately drive lasting changes in the associated assemblage of species, and therefore, the community as a whole.

Apparent competition and native consumers exacerbate the strong competitive effect of an exotic plant species.

Direct and indirect effects can play a key role in invasions, but experiments evaluating both are rare. We examined the roles of direct competition and apparent competition by exotic Amur honeysuckle (Lonicera maackii) by manipulating (1) L. maackii vegetation, (2) presence of L. maackii fruits, and (3) access to plants by small mammals and deer. Direct competition with L. maackii reduced the abundance and richness of native and exotic species, and native consumers significantly reduced the abundance and richness of native species. Although effects of direct competition and consumption were more pervasive, richness of native plants was also reduced through apparent competition, as small-mammal consumers reduced richness only when L. maackii fruits were present. Our experiment reveals the multiple, interactive pathways that affect the success and impact of an invasive exotic plant: exotic plants may directly benefit from reduced attack by native consumers, may directly exert strong competitive effects on native plants, and may also benefit from apparent competition.

Herbivore pressure increases toward the equator.

Increases in species diversity and density from higher to lower latitudes are well documented. Nevertheless, the consequences of these changes in diversity for structuring ecological communities and influencing biotic evolution are largely unknown. It is widely believed that this increase in species diversity is associated with increased intensity of ecological interactions closer to the equator. For plant-herbivore interactions in particular, the predictions are that, at lower latitudes, plants will be attacked by more individual herbivores, more herbivore species, and more specialized herbivores and, therefore, will suffer greater damage. We used a large-scale latitudinal transect from Mexico to Bolivia to quantify changes in leaf damage, diversity, and abundance of lepidopteran larvae on two widely distributed host species of the genus Piper (Piperaceae). We show that both density and species richness of herbivores were highest at the equator and decreased with increasing latitude, both northward and southward. Contrary to expectation, however, this increase in herbivore diversity was attributable to the addition of generalist not specialist species. Finally, and again contrary to expectation, the increase in herbivore density with decreasing latitude did not produce a corresponding damage gradient. We propose that the lack of a latitudinal concordance between increases in herbivore density and diversity with decreasing latitude, and the resulting herbivore damage, supports the hypothesis of better plant antiherbivore defenses at lower latitudes. Furthermore, the changes in the relative abundance of generalist vs. specialist species suggest that the nature of the selective pressure is intrinsically different between higher and lower latitudes.

Native leaf-tying caterpillars influence host plant use by the invasive Asiatic oak weevil through ecosystem engineering.

We tested the effect of leaf-tying caterpillars, native ecosystem engineers, on the abundance and host feeding of an invasive insect, the Asiatic oak weevil, Cyrtepistomus castaneus (Roelofs). Leaf quality was previously thought to be the sole factor determining host use by C. castaneus, but adult weevils congregate in leaf ties made by lepidopteran larvae (caterpillars). Adult weevil abundance was naturally higher on Quercus alba and Q. velutina compared to four other tree species tested (Acer rubrum, Carya ovata, Cornus florida, and Sassafras albidum). These differences were associated with more natural leaf ties on the two Quercus species. In the laboratory, weevils fed on all six species but again preferred Q. alba and Q. velutina. When artificial ties were added to all six tree species, controlling for differences in leaf-tie density, adult weevil density increased on all six tree species, damage increased on all species but A. rubrum, and host ranking changed based on both abundance and damage. We conclude that leaf ties increase the local abundance of C. castaneus adults and their feeding. Thus, these native leaf-tying caterpillars engender the success of an invasive species via structural modification of potential host plants, the first described example of this phenomenon.

Emerging Trends in Ant-Pollinator Conflict in Extrafloral Nectary-Bearing Plants.

The net outcomes of mutualisms are mediated by the trade-offs between the costs and benefits provided by both partners. Our review proposes the existence of a trade-off in ant protection mutualisms between the benefits generated by the ants' protection against the attack of herbivores and the losses caused by the disruption of pollination processes, which are commonly not quantified. This trade-off has important implications for understanding the evolution of extrafloral nectaries (EFNs), an adaptation that has repeatedly evolved throughout the flowering plant clade. We propose that the outcome of this trade-off is contingent on the specific traits of the organisms involved. We provide evidence that the protective mutualisms between ants and plants mediated by EFNs have optimal protective ant partners, represented by the optimum point of the balance between positive effects on plant protection and negative effects on pollination process. Our review also provides important details about a potential synergism of EFN functionality; that is, these structures can attract ants to protect against herbivores and/or distract them from flowers so as not to disrupt pollination processes. Finally, we argue that generalizations regarding how ants impact plants should be made with caution since ants' effects on plants vary with the identity of the ant species in their overall net outcome.

Invasive honeysuckle eradication reduces tick-borne disease risk by altering host dynamics.

Despite the ubiquity of invasive organisms and their often deleterious effects on native flora and fauna, the consequences of biological invasions for human health and the ecological mechanisms through which they occur are rarely considered. Here we demonstrate that a widespread invasive shrub in North America, Amur honeysuckle (Lonicera maackii), increases human risk of exposure to ehrlichiosis, an emerging infectious disease caused by bacterial pathogens transmitted by the lone star tick (Amblyomma americanum). Using large-scale observational surveys in natural areas across the St. Louis, Missouri region, we found that white-tailed deer (Odocoileus virginianus), a preeminent tick host and pathogen reservoir, more frequently used areas invaded by honeysuckle. This habitat preference translated into considerably greater numbers of ticks infected with pathogens in honeysuckle-invaded areas relative to adjacent honeysuckle-uninvaded areas. We confirmed this biotic mechanism using an experimental removal of honeysuckle, which caused a decrease in deer activity and infected tick numbers, as well as a proportional shift in the blood meals of ticks away from deer. We conclude that disease risk is likely to be reduced when honeysuckle is eradicated, and suggest that management of biological invasions may help ameliorate the burden of vector-borne diseases on human health.

Both host plant and ecosystem engineer identity influence leaf-tie impacts on the arthropod community of Quercus.

Many insect herbivores build shelters on plants, which are then colonized by other arthropod species. To understand the impacts of such ecosystem engineering on associated species, the contributions of ecosystem engineer and host-plant identities must be understood. We investigated these contingencies at the patch scale using two species of leaf-tying caterpillars, which vary in size and tie construction mode, on eight species of oak (Quercus) trees, which vary in leaf size and leaf chemistry. We created three types of artificial leaf ties by clipping together pairs of adjacent leaves using metal hair clips. We left the first type of leaf tie empty while adding individuals of the leaf-tying caterpillars of either Pseudotelphusa quercinigracella or Psilocorsis cryptolechiella to the other two. We also created a control treatment of untied leaves by affixing clips to single leaves. Leaf ties increased occupancy in the early season and arthropod alpha diversity throughout the experiment, on average fourfold. Furthermore, the presence of leaf ties increased arthropod species density on average three times and abundance 10-35 times, depending on the plant species. The mean phenolic content of the leaves of each oak species was positively correlated with the leaf-tie effect on abundance and negatively correlated with the leaf-tie effect on species diversity. Species diversity, but not abundance, was affected by the identity of the tie-maker. Arthropod species composition differed between untied leaves and artificial leaf ties, and between ties made by the two leaf-tier species. Our results demonstrate that the presence of leaf ties adds to habitat diversity within the oak-herbivore system, not only by creating a new kind of microhabitat (the leaf tie) within trees, but also by exacerbating differences among the eight oak species in apparent habitat quality. The identity of the leaf-tying caterpillar adds to this heterogeneity by creating leaf ties of different size, thus influencing subsequent colonization by other leaf-tying caterpillars of different sizes.

Species richness and niche space for temperate and tropical folivores.

We measured structural and chemical traits of the leaves of native, broad-leaved trees in two temperate localities [southern Ontario, Canada (34 species), and Missouri (36 species)] and one tropical locality [central Panama (samples of 21 and 23 species)] to test the hypothesis that the greater diversity of tree species and herbivore species in the tropics is associated with greater resource niche space for herbivores. Variables were leaf toughness, water content, dry mass per unit area, several structural and nutritional carbohydrates, common mineral elements, including nitrogen and phosphorus, and several defensive compounds, including tannins and alkaloids. The four samples were almost fully separable by discriminant analysis on the basis of these leaf traits. Variance in log-transformed trait values among species was lowest in the most northern sample, but did not differ significantly between Missouri and Panama. Niche space, estimated as the square root of the total variance in the log-transformed variables within each locality, varied approximately as Panama = 1, Missouri = 0.8, Ontario = 0.5. Although niche space decreases towards higher latitudes, the change does not match the ca. sixfold decrease in tree species richness or the ca. fourfold decrease in Lepidopteran species richness over the latitude range of our samples. Accordingly, tropical folivore diversity is associated with greater resource niche overlap, greater niche specialization, and/or more completely filled niches, or with variation in niche dimensions not measured in this study.

Testing the low latitude/high defense hypothesis for broad-leaved tree species.

We tested the hypothesis that leaves of broad-leaved tree species are more highly defended at low latitudes than at high latitudes. We used canonical discriminant analysis to compare tree species from Panama (9°N, 39 species), Missouri, USA (38°N, 37 species), and southern Ontario, Canada (44°N, 34 species) with respect to two structural and five nutritional traits, taking into account each species' tolerance to shade. Trees from the three locations differed significantly, with Panamanian species the most distinct. Defenses of shade-tolerant species were significantly greater than those of shade-intolerant species, but only for the Panamanian sample, which is consistent with the low latitude/high defense hypothesis. Because we sampled many of the same tree species from Missouri and southern Ontario, and many tree species in the same taxonomic families in Missouri and Panama, we were able to control for the potential confounding effects of phylogeny. Overall defense levels, calculated by summing the z-scores for individual traits in each location, were significantly higher for Panama compared to Missouri, and marginally so for Missouri compared to southern Ontario, again consistent with the low latitude/high defense hypothesis. Traits contributing to these differences were mostly structural factors (e.g., fiber) and to a lesser degree nutritional traits, while secondary compounds made no independent contribution to differences in overall defense levels (four traits compared between Panama and Missouri). Contrary to our expectation, the number and types of secondary compounds per species reported in the literature for our species did not differ between temperate and tropical locations, while the diversity of these compounds was greater for the temperate species. Overall, our results provide some support for the hypothesis that leaf defenses against herbivory are better developed in tropical than in temperate trees, but the differences were due to structural and nutritional factors rather than secondary compounds.