Phytochemistry-mediated disruption of ant-aphid interactions by root-feeding nematodes.

Plants link interactions between aboveground and belowground organisms. Herbivore-induced changes in plant chemistry are hypothesized to impact entire food webs by changing the strength of trophic cascades. Yet, few studies have explored how belowground herbivores affect the behaviors of generalist predators, nor how such changes may act through diverse changes to the plant metabolome. Using a factorial experiment, we tested whether herbivory by root-knot nematodes (Meloidogyne incognita) affected the aboveground interaction among milkweed plants (Asclepias fascicularis or Asclepias speciosa), oleander aphids (Aphis nerii), and aphid-tending ants (Linepithema humile). We quantified the behaviors of aphid-tending ants, and we measured the effects of herbivore treatments on aphid densities and on phytochemistry. Unexpectedly, ants tended aphids primarily on the leaves of uninfected plants, whereas ants tended aphids primarily at the base of the stem of nematode-infected plants. In nematode-infected plants, aphids excreted more sugar per capita in their ant-attracting honeydew. Additionally, although plant chemistry was species-specific, nematode infection generally decreased the richness of plant secondary metabolites while acting as a protein sink in the roots. Path analysis indicated that the ants' behavioral change was driven in part by indirect effects of nematodes acting through changes in plant chemistry. We conclude that belowground herbivores can affect the behaviors of aboveground generalist ant predators by multiple paths, including changes in phytochemistry, which may affect the attractiveness of aphid honeydew rewards.

A whole-plant perspective reveals unexpected impacts of above- and belowground herbivores on plant growth and defense.

Trade-offs between plant growth and defense are central to theoretical frameworks used to study the ecology and evolution of plant defense against herbivores. However, these frameworks, as well as the experiments designed to test them, rarely include belowground herbivores. We experimentally challenged seedlings of the tropical shrub Solanum lycocarpum (Solanaceae) with either aboveground foliar herbivores (Spodoptera caterpillars) or belowground root herbivores (the nematode Meloidogyne incognita) and measured the resulting changes in plant growth rates, biomass allocation, and the concentration of defensive terpenoids in roots and leaves. We found that plants that suffered aboveground herbivory responded with aboveground growth but belowground defense. Similarly, belowground herbivory resulted in root growth but elevated defenses of leaves. These results underscore the importance of belowground plant-herbivore interactions, and suggest that, in contrast to theoretical predictions, plants can simultaneously invest in both growth and defense. Finally, they emphasize the need for a "whole-plant" perspective in theoretical and empirical evaluations of plant-herbivore interactions.

Is There a Temperate Bias in Our Understanding of How Climate Change Will Alter Plant-Herbivore Interactions? A Meta-analysis of Experimental Studies.

Climate change can drive major shifts in community composition and interactions between resident species. However, the magnitude of these changes depends on the type of interactions and the biome in which they take place. We review the existing conceptual framework for how climate change will influence tropical plant-herbivore interactions and formalize a similar framework for the temperate zone. We then conduct the first biome-specific tests of how plant-herbivore interactions change in response to climate-driven changes in temperature, precipitation, ambient CO2, and ozone. We used quantitative meta-analysis to compare predicted and observed changes in experimental studies. Empirical studies were heavily biased toward temperate systems, so testing predicted changes in tropical plant-herbivore interactions was virtually impossible. Furthermore, most studies investigated the effects of CO2 with limited plant and herbivore species. Irrespective of location, most studies manipulated only one climate change factor despite the fact that different factors can act in synergy to alter responses of plants and herbivores. Finally, studies of belowground plant-herbivore interactions were also rare; those conducted suggest that climate change could have major effects on belowground subsystems. Our results suggest that there is a disconnection between the growing literature proposing how climate change will influence plant-herbivore interactions and the studies testing these predictions. General conclusions will also be hampered without better integration of above- and belowground systems, assessing the effects of multiple climate change factors simultaneously, and using greater diversity of species in experiments.

Do biological control agents adapt to local pest genotypes? A multiyear test across geographic scales.

Parasite local adaptation has been a major focus of (co)evolutionary research on host-parasite interactions. Studies of wild host-parasite systems frequently find that parasites paired with local, sympatric host genotypes perform better than parasites paired with allopatric host genotypes. In contrast, there are few such tests in biological control systems to establish whether biological control parasites commonly perform better on sympatric pest genotypes. This knowledge gap prevents the optimal design of biological control programs: strong local adaptation could argue for the use of sympatric parasites to achieve consistent pest control. To address this gap, we tested for local adaptation of the biological control bacterium Pasteuria penetrans to the root-knot nematode Meloidogyne arenaria, a global threat to a wide range of crops. We measured the probability and intensity of P. penetrans infection on sympatric and allopatric M. arenaria over the course of 4 years. Our design accounted for variation in adaptation across scales by conducting tests within and across fields, and we isolated the signature of parasite adaptation by comparing parasites collected over the course of the growing season. Our results are largely inconsistent with local adaptation of P. penetrans to M. arenaria: in 3 of 4 years, parasites performed similarly well in sympatric and allopatric combinations. In 1 year, however, infection probability was 28% higher for parasites paired with hosts from their sympatric plot, relative to parasites paired with hosts from other plots within the same field. These mixed results argue for population genetic data to characterize the scale of gene flow and genetic divergence in this system. Overall, our findings do not provide strong support for using P. penetrans from local fields to enhance biological control of Meloidogyne.

Attack frequency and the tolerance to herbivory of Neotropical savanna trees.

Tolerance is the ability of a plant to regrow or reproduce following damage. While experimental studies typically measure tolerance in response to the intensity of herbivory (i.e., the amount of leaf tissue removed in one attack), the impact of how many times plants are attacked during a growing season (i.e., the frequency of damage) is virtually unexplored. Using experimental defoliations that mimicked patterns of attack by leaf-cutter ants (Atta spp.), we examined how the frequency of herbivory influenced plant tolerance traits in six tree species in Brazil's Cerrado. For 2 years we quantified how monthly and quarterly damage influenced individual survivorship, relative growth rate, plant architecture, flowering, and foliar chemistry. We found that the content of leaf nitrogen (N) increased among clipped individuals of most species, suggesting that Atta influences the allocation of resources in damaged plants. Furthermore, our clipping treatments affected tree architecture in ways thought to promote tolerance. However, none of our focal species exhibited a compensatory increase in growth (increment in trunk diameter) in response to herbivory as relative growth rates were significantly lower in clipped than in unclipped individuals. In addition, the probability of survival was much lower for clipped plants, and lower for plants clipped monthly than those clipped quarterly. For plants that did survive, simulated herbivory dramatically reduced the probability of flowering. Our results were similar across a phylogenetically distinct suite of species, suggesting a potential extendability of these findings to other plant species in this system.

A diverse parasite pool can improve effectiveness of biological control constrained by genotype-by-genotype interactions.

The outcomes of biological control programs can be highly variable, with natural enemies often failing to establish or spread in pest populations. This variability has posed a major obstacle in use of the bacterial parasite Pasteuria penetrans for biological control of Meloidogyne species, economically devastating plant-parasitic nematodes for which there are limited management options. A leading hypothesis for this variability in control is that infection is successful only for specific combinations of bacterial and nematode genotypes. Under this hypothesis, failure of biological control results from the use of P. penetrans genotypes that cannot infect local Meloidogyne genotypes. We tested this hypothesis using isofemale lines of M. arenaria derived from a single field population and multiple sources of P. penetrans from the same and nearby fields. In strong support of the hypothesis, susceptibility to infection depended on the specific combination of host line and parasite source, with lines of M. arenaria varying substantially in which P. penetrans source could infect them. In light of this result, we tested whether using a diverse pool of P. penetrans could increase infection and thereby control. We found that increasing the diversity of the P. penetrans inoculum from one to eight sources more than doubled the fraction of M. arenaria individuals susceptible to infection and reduced variation in susceptibility across host lines. Together, our results highlight genotype-by-genotype specificity as an important cause of variation in biological control and call for the maintenance of genetic diversity in natural enemy populations.

Whole-Plant Metabolic Allocation Under Water Stress.

Trade-offs between plant growth and defense depend on environmental resource availability. Plants are predicted to prioritize growth when environmental resources are abundant and defense when environmental resources are scarce. Nevertheless, such predictions lack a whole-plant perspective-they do not account for potential differences in plant allocation above- and belowground. Such accounting is important because leaves and roots, though both critical to plant survival and fitness, differ in their resource-uptake roles and, often, in their vulnerability to herbivores. Here we aimed to determine how water availability affects plant allocation to multiple metabolic components of growth and defense in both leaves and roots. To do this, we conducted a meta-analysis of data from experimental studies in the literature. We assessed plant metabolic responses to experimentally reduced water availability, including changes in growth, nutrients, physical defenses, primary metabolites, hormones, and other secondary metabolites. Both above- and belowground, reduced water availability reduced plant biomass but increased the concentrations of primary metabolites and hormones. Importantly, however, reduced water had opposite effects in different organs on the concentrations of other secondary metabolites: reduced water increased carbon-based secondary metabolites in leaves but reduced them in roots. In addition, plants suffering from co-occurring drought and herbivory stresses exhibited dampened metabolic responses, suggesting a metabolic cost of multiple stresses. Our study highlights the needs for additional empirical studies of whole-plant metabolic responses under multiple stresses and for refinement of existing plant growth-defense theory in the context of whole plants.