Michael J. Wise

Effects of Resource Availability on Tolerance of Herbivory: A Review and Assessment of Three Opposing Models

Although it is widely acknowledged that a plant’s tolerance of herbivore damage depends on resource availability in the plant’s environment, there is no consensus on whether higher resource levels lead to greater or to lower tolerance. The prevailing model, the compensatory continuum hypothesis (CCH), predicts that tolerance of herbivory should be greater in high‐resource or low‐competition conditions. The main rival hypothesis, the growth rate model (GRM), makes the opposite prediction: tolerance of herbivory should be greater in more stressful conditions. The tolerance predictions of a recently introduced model, the limiting resource model (LRM), are more flexible and depend on the type of resource and herbivore under consideration. We reviewed 48 studies (from 40 published articles) of plant tolerance of leaf damage in conditions differing in levels of light, inorganic nutrients, water stress, or competition. The results of 31%, 48%, and 95% of the studies were consistent with the predictions of the CCH, GRM, and LRM, respectively. Thus, by considering which resource is primarily affected by herbivory and which resource is limiting a plant’s fitness, the LRM offers a substantial advance in predicting how tolerance will be affected by environmental differences in resource availability.

Prior flea beetle herbivory affects oviposition preference and larval performance of a potato beetle on their shared host plant

Abstract 1. The herbaceous plant Solanum carolinense (L.) (Solanaceae) is host to a number of specialist insects, including the leaf‐feeding beetles Epitrix fuscula (Crotch) and Leptinotarsa juncta (Germar) (Coleoptera: Chrysomelidae). Potted individuals of S. carolinense were subjected to one of two treatments: exposure to herbivory by E. fuscula or exclusion of all herbivores. The effects of E. fuscula herbivory on larval performance and oviposition preference of L. juncta were investigated.

Impact of two specialist insect herbivores on reproduction of horse nettle, Solanum carolinense.

The frequency of coevolution as a process of strong mutual interaction between a single plant and herbivore species has been questioned in light of more commonly observed, complex relationships between a plant and a suite of herbivore species. Despite recognition of the possibility of diffuse coevolution, relatively few studies have examined ecological responses of plants to herbivores in complex associations. We studied the impact of two specialist herbivores, the horse nettle beetle, Leptinotarsa juncta, and the eggplant flea beetle, Epitrix fuscula, on reproduction of their host, Solanum carolinense. Our study involved field and controlled-environment experimental tests of the impact on sexual and potential asexual reproduction of attack by individuals of the two herbivore species, individually and in combination. Field tests demonstrated that under normal levels of phytophagous insect attack, horse nettle plants experienced a reduction in fruit production of more than 75% compared with plants from which insects were excluded. In controlled-environment experiments using enclosure-exclosure cages, the horse nettles two principal herbivores, the flea beetle and the horse nettle beetle, caused decreases in sexual reproduction similar to those observed in the field, and a reduction in potential asexual reproduction, represented by root biomass. Attack by each herbivore reduced the numbers of fruits produced, and root growth, when feeding in isolation. When both species were feeding together, fruit production, but not root growth, was lower than when either beetle species fed alone. Ecological interactions between horse nettle and its two primary herbivores necessary for diffuse coevolution to occur were evident from an overall analysis of the statistical interactions between the two herbivores for combined assessment of fruit and vegetative traits. For either of these traits alone, the interactions necessary to promote diffuse coevolution apparently were lacking.

Applying the Limiting Resource Model to Plant Tolerance of Apical Meristem Damage

Apical meristem damage (AMD) is a common result of herbivory. AMD can have dramatically variable effects on plant architecture and fitness, ranging from a total loss of reproductive capacity to overcompensation. We explored the influence of environmental stresses and meristem limitation on tolerance of AMD by applying the limiting resource model (LRM) of plant tolerance to 17 previously published studies and a new empirical study on Solidago altissima. In the S. altissima experiment, AMD released axillary meristems from apical dominance, and fertilizer addition enabled plants to take full advantage of the lateral branches. AMD caused a 58% reduction in seed production in nutrient‐stressed plants but only a 6% reduction in seed production in fertilized plants. In 12 of the 18 studies reviewed, tolerance was greater in the high‐resource (or low‐competition) treatment; in two, tolerance was greater in the low‐resource treatment; and in four, resource level did not affect tolerance of AMD. The results of 15 studies (83%) were consistent with LRM predictions. Overcompensation was observed in six studies, and it occurred only in the high‐resource treatments in five of these studies, as would be expected from applying the LRM.

Compensation for floral herbivory in Solanum carolinense : identifying mechanisms of tolerance

While a plant’s capacity to tolerate damage by herbivores can be studied as a single trait, it is important to recognize that tolerance is generally a result of the combined action of several different traits. Here, we report on a pair of experiments to identify mechanisms for tolerating floral herbivory in Solanum carolinense, an andromonoecious perennial herb that regularly suffers from high levels of florivory. We measured the effect of actual and simulated florivory on host-plant fitness and assessed which plant traits exhibited plasticity in response to florivory. In addition, for each of nine plant genets, we calculated tolerance indices and determined which traits were genetically correlated with tolerance. Traits that served to help S. carolinense tolerate florivory in terms of sexual reproduction included initiating more inflorescences, aborting fewer buds prior to anthesis and fewer ovaries after fertilization, and increasing the ratio of perfect:male flowers. In addition, the greater the levels of florivory, the more the plants allocated to root growth, which may promote tolerance through greater potential future reproduction. The plant population contained significant genetic variation for tolerance itself and for nearly all of the putative tolerance mechanisms, which suggests that S. carolinense has the potential to evolve greater tolerance through a variety of different routes in response to natural selection.

EVOLUTION OF RESISTANCE TO A MULTIPLE‐HERBIVORE COMMUNITY: GENETIC CORRELATIONS, DIFFUSE COEVOLUTION, AND CONSTRAINTS ON THE PLANT'S RESPONSE TO SELECTION

Although plants are generally attacked by a community of several species of herbivores, relatively little is known about the strength of natural selection for resistance in multiple‐herbivore communities—particularly how the strength of selection differs among herbivores that feed on different plant organs or how strongly genetic correlations in resistance affect the evolutionary responses of the plant. Here, we report on a field study measuring natural selection for resistance in a diverse community of herbivores of Solanum carolinense. Using linear phenotypic‐selection analyses, we found that directional selection acted to increase resistance to seven species. Selection was strongest to increase resistance to fruit feeders, followed by flower feeders, then leaf feeders. Selection favored a decrease in resistance to a stem borer. Bootstrapping analyses showed that the plant population contained significant genetic variation for each of 14 measured resistance traits and significant covariances in one‐third of the pairwise combinations of resistance traits. These genetic covariances reduced the plants overall predicted evolutionary response for resistance against the herbivore community by about 60%. Diffuse (co)evolution was widespread in this community, and the diffuse interactions had an overwhelmingly constraining (rather than facilitative) effect on the plants evolution of resistance.

Costs and benefits of gregarious feeding in the meadow spittlebug, Philaenus spumarius

Abstract 1. To study the function of group living in a non‐social animal, costs and benefits of feeding in different group sizes (one to eight) were measured for nymphs of the meadow spittlebug (Philaenus spumarius) on tall goldenrod (Solidago altissima).

Good mothers, bad mothers, and the nature of resistance to herbivory in Solidago altissima.

Evidence of poor correspondence between an insect herbivore’s oviposition preferences and the performance of its offspring has generally been attributed either to maladaptive behavior of the insect mother or inadequate measurement by the researcher. In contrast, we hypothesize that many cases of “bad mothers” in herbivores may be a byproduct of the hierarchical way natural selection works on resistance in host plants. Epistatic selection on the components of resistance (i.e., antixenosis and antibiosis) may generate negative genetic correlations between the resistance components, which could counteract the efforts of herbivores to oviposit on the best hosts for the performance of their offspring. In common garden and greenhouse experiments, we measured aspects of antixenosis and antibiosis resistance in 26 genets of tall goldenrod, Solidago altissima, against two common herbivores: the gall-inducing fly Eurosta solidaginis and the spittlebug Philaenus spumarius. Goldenrod antixenosis and antibiosis were positively correlated against E. solidaginis and negatively correlated against P. spumarius. Analogously, population-wide preference–performance correlations were positive for the gall flies and negative for the spittlebugs. Several natural history differences between the two insects could make gall flies better mothers, including better synchrony of the phenologies of the flies and the host plant, the much narrower host range of the gall flies than the spittlebugs, and the more sedentary lifestyle of the gall fly larvae than the spittlebug nymphs. If these results are typical in nature, then negative genetic correlations in antixenosis and antibiosis in plants may often result in zero or negative population-wide correlations between preference and performance in herbivores, and thus may be an important reason why herbivorous insects often appear to be bad mothers.

On quantifying tolerance of herbivory for comparative analyses.

Abstract As the evolutionary importance of plant tolerance of herbivory is increasingly appreciated, more and more studies are not just measuring a plants tolerance, but are comparing tolerance among plant genotypes, populations, species, and environments. Here, we suggest that caution must be taken in such comparative studies in the choice of measurement scales (and data transformations) for damage levels and plant performance. We demonstrate with a simple scenario of two plant groups of equal tolerance how the choice of scales can lead one to infer that the first group is more tolerant, the second group is more tolerant, or the two groups are equally tolerant—using the identical dataset. We conclude that to make reliable, logically consistent inferences when comparing tolerances among groups of plants, damage and performance should both be on an additive scale or both on a multiplicative scale.

The Herbivores of Solanum carolinense (Horsenettle) in Northern Virginia: Natural History and Damage Assessment

Abstract I studied interactions between the herbaceous weed Solanum carolinense (horsenettle) and its herbivore community in northern Virginia from 1996–2002. Thirty-two species regularly fed on the plant, including 31 insects from 6 taxonomic orders and Microtus pennsylvanicus (meadow vole). An intensive field experiment on 960 horsenettle individuals in 2001 revealed high levels of damage to all parts of the plants. Two chrysomelid beetles—Epitrix fuscula (eggplant flea beetle) and Leptinotarsa juncta (false potato beetle)—damaged leaves on nearly every plant. Roughly half of the flowers were destroyed by herbivores, with Anthonomus nigrinus (potato bud weevil) destroying 30%. Nearly three-fourths of the fruits were damaged by three species: the tephritid fly Zonosemata electa (pepper maggot), false potato beetle, and meadow vole. The weevil Trichobaris trinotata (potato stalk borer) bored in stems of 73% of the plants, and the most damaging root feeder was the moth Synanthedon rileyana (Rileys clearwing). A literature review on the horsenettle-herbivore community is integrated with new observations as a guide for applied and basic research on this economically significant species.