Ian S. Pearse

Phylogenetic and trait similarity to a native species predict herbivory on non-native oaks

Introduced plants tend to experience less herbivory than natives, although herbivore loads vary widely. Herbivores may switch hosts onto an introduced plant for at least two reasons. They may recognize the novel plant as a potential host based on similarity of the plants traits to the traits of one of its native hosts, a similarity that may or may not exhibit phylogenetic signal. Alternatively, herbivores may feed optimally, assessing which introduced plants provide the best nutrition irrespective of similarity to native species. Here, we created a phylogeny of 57 oak (Quercus) taxa, which were grown outside of their ranges in a common botanical garden that contained one abundant native oak (Quercus lobata). We used the phylogeny to estimate the phylogenetic conservatism of herbivory by two feeding guilds of insects (leaf chewers and leaf miners) and 11 plant traits expected to affect herbivore performance. We found high phylogenetic signal in chewing damage but not mining damage and all traits except for leaf maturation time. Introduced oaks that are more closely related to the native oak received more chewing and mining damage than distantly related oaks, and introduced oaks that had greater overall similarity in leaf traits also received higher chewing damage but not mining damage. These results demonstrate that interactions between introduced plants and their herbivores are driven independently by traits that track plant phylogeny and leaf traits that likely affect herbivore performance.

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.

Similarity and Specialization of the Larval versus Adult Diet of European Butterflies and Moths

Many herbivorous insects feed on plant tissues as larvae but use other resources as adults. Adult nectar feeding is an important component of the diet of many adult herbivores, but few studies have compared adult and larval feeding for broad groups of insects. We compiled a data set of larval host use and adult nectar sources for 995 butterfly and moth species (Lepidoptera) in central Europe. Using a phylogenetic generalized least squares approach, we found that those Lepidoptera that fed on a wide range of plant species as larvae were also nectar feeding on a wide range of plant species as adults. Lepidoptera that lack functional mouthparts as adults used more plant species as larval hosts, on average, than did Lepidoptera with adult mouthparts. We found that 54% of Lepidoptera include their larval host as a nectar source. By creating null models that described the similarity between larval and adult nectar sources, we furthermore showed that Lepidoptera nectar feed on their larval host more than would be expected if they fed at random on available nectar sources. Despite nutritional differences between plant tissue and nectar, we show that there are similarities between adult and larval feeding in Lepidoptera. This suggests that either behavioral or digestive constraints are retained throughout the life cycle of holometabolous herbivores, which affects host breadth and identity.

Insect herbivores selectively suppress the HPL branch of the oxylipin pathway in host plants

Insect herbivores have developed a myriad of strategies to manipulate the defense responses of their host plants. Here we provide evidence that chewing insects differentially alter the oxylipin profiles produced by the two main and competing branches of the plant defensive response pathway, the allene oxide synthase (AOS) and hydroperoxide lyase (HPL) branches, which are responsible for wound-inducible production of jasmonates (JAs), and green leafy volatiles (GLVs) respectively. Specifically, we used three Arabidopsis genotypes that were damaged by mechanical wounding or by insects of various feeding guilds (piercing aphids, generalist chewing caterpillars and specialist chewing caterpillars). We established that emission of GLVs is stimulated by wounding incurred mechanically or by aphids, but release of these volatiles is constitutively impaired by both generalist and specialist chewing insects. Simultaneously, however, these chewing herbivores stimulated JA production, demonstrating targeted insect suppression of the HPL branch of the oxylipin pathway. Use of lines engineered to express HPL constitutively, in conjunction with quantitative RT-PCR-based expression analyses, established a combination of transcriptional and post-transcriptional reprogramming of the HPL pathway genes as the mechanistic basis of insect-mediated suppression of the corresponding metabolites. Feeding studies suggested a potential evolutionary advantage of suppressing GLV production, as caterpillars preferably consumed leaf tissue from plants that had not been primed by these volatile cues.

The role of leaf defensive traits in oaks on the preference and performance of a polyphagous herbivore, Orgyia vetusta

1. Leaves possess traits that mediate the preference and performance of herbivores. Most evidence for the importance of leaf traits as defences against herbivory comes from studies of few model plant species.

Diet mixing enhances the performance of a generalist caterpillar, Platyprepia virginalis

1. Platyprepia virginalis caterpillars are dietary generalists and feed on multiple host species within a single day. We conducted field experiments to evaluate their performance on diets consisting of only their primary food, Lupinus arboreus, or diets consisting of L. arboreus plus other acceptable host species.

Extinction cascades partially estimate herbivore losses in a complete Lepidoptera–plant food web

The loss of species from an ecological community can have cascading effects leading to the extinction of other species. Specialist herbivores are highly diverse and may be particularly susceptible to extinction due to host plant loss. We used a bipartite food web of 900 Lepidoptera (butterfly and moth) herbivores and 2403 plant species from Central Europe to simulate the cascading effect of plant extinctions on Lepidoptera extinctions. Realistic extinction sequences of plants, incorporating red-list status, range size, and native status, altered subsequent Lepidoptera extinctions. We compared simulated Lepidoptera extinctions to the number of actual regional Lepidoptera extinctions and found that all predicted scenarios underestimated total observed extinctions but accurately predicted observed extinctions attributed to host loss (n = 8, 14%). Likely, many regional Lepidoptera extinctions occurred for reasons other than loss of host plant alone, such as climate change and habitat loss. Ecological networks can be useful in assessing a component of extinction risk to herbivores based on host loss, but further factors may be equally important.

Complex consequences of herbivory and interplant cues in three annual plants.

Information exchange (or signaling) between plants following herbivore damage has recently been shown to affect plant responses to herbivory in relatively simple natural systems. In a large, manipulative field study using three annual plant species (Achyrachaena mollis, Lupinus nanus, and Sinapis arvensis), we tested whether experimental damage to a neighboring conspecific affected a plants lifetime fitness and interactions with herbivores. By manipulating relatedness between plants, we assessed whether genetic relatedness of neighboring individuals influenced the outcome of having a damaged neighbor. Additionally, in laboratory feeding assays, we assessed whether damage to a neighboring plant specifically affected palatability to a generalist herbivore and, for S. arvensis, a specialist herbivore. Our study suggested a high level of contingency in the outcomes of plant signaling. For example, in the field, damaging a neighbor resulted in greater herbivory to A. mollis, but only when the damaged neighbor was a close relative. Similarly, in laboratory trials, the palatability of S. arvensis to a generalist herbivore increased after the plant was exposed to a damaged neighbor, while palatability to a specialist herbivore decreased. Across all species, damage to a neighbor resulted in decreased lifetime fitness, but only if neighbors were closely related. These results suggest that the outcomes of plant signaling within multi-species neighborhoods may be far more context-specific than has been previously shown. In particular, our study shows that herbivore interactions and signaling between plants are contingent on the genetic relationship between neighboring plants. Many factors affect the outcomes of plant signaling, and studies that clarify these factors will be necessary in order to assess the role of plant information exchange about herbivory in natural systems.

Communicative interactions involving plants: information, evolution, and ecology.

The role of information obtained via sensory cues and signals in mediating the interactions of organisms with their biotic and abiotic environments has been a major focus of work on sensory and behavioral ecology. Information-mediated interactions also have important implications for broader ecological patterns emerging at the community and ecosystem levels that are only now beginning to be explored. Given the extent to which plants dominate the sensory landscapes of terrestrial ecosystems, information-mediated interactions involving plants should be a major focus of efforts to elucidate these broader patterns. Here we explore how such efforts might be enhanced by a clear understanding of information itself-a central and potentially unifying concept in biology that has nevertheless been the subject of considerable confusion-and of its relationship to adaptive evolution and ecology. We suggest that information-mediated interactions should be a key focus of efforts to more fully integrate evolutionary biology and ecology.

The predictability of traits and ecological interactions on 17 different crosses of hybrid oaks

Herbivory on hybrid plants has the potential to affect patterns of plant evolution, such as limiting gene-flow through hybrids, and can also affect herbivore biodiversity. However, few studies have surveyed multiple hybrid species to identify phylogenetic patterns in the inheritance of plant traits that may drive herbivory. We surveyed 15 leaf traits and patterns of chewing, mining, and galling herbivory in a common garden of 17 artificially crossed hybrid oak species and each of their parental species over a 2-year period. Using a phylogeny of oaks, we tested whether hybrids that resulted from more divergent parents received more herbivory than those derived from closely related parents (as would be predicted by a build-up of incompatibilities in defensive systems over evolutionary time) and found only marginal evidence in support of this. We found that chewing damage to hybrids was weakly predicted by the relatedness of a parental species to the single native oak. The levels of chewing and mining herbivory on hybrids were typically intermediate to those of their parental species, though less than the parental mean for chewing damage in 2008. Most leaf traits of hybrids were also intermediate to those of their parental species. There was no clear pattern in terms of an association between 11 species of cynipid gall wasps and hybrids. The patterns of (1) intermediate levels of herbivory on hybrids and (2) no trend in herbivory on hybrids based on the phylogenetic relatedness of parental species suggest that herbivory may not play a general role in limiting hybrid fitness (and thus gene-flow through hybrids) in oaks.