Gregory M. English-Loeb

Drought stress in tomatoes : changes in plant chemistry and potential nonlinear consequences for insect herbivores

Insect herbivores respond variably to drought-stressed plants; in some cases herbivore performance (e.g. fecundity, survival) is enhanced, in others it is negatively affected. We used tomato plants to examine the consequences of drought stress intensity on plant chemistry potentially important to insect herbivores in order to gain insights into resolving these conflicting results. In a series of experiments conducted out-of-doors, we measured the concentration of five chemicals previously shown to act as growth reducers against herbivores (2 oxidative enzymes, 2 phenolics, proteinase inhibitor) in control plants and drought-stressed plants over a period of about 14 d. Three of the five defenses increased in response to increasing drought (polyphenol oxidase, rutin, chlorogenic acid), one showed no response (peroxidase) and one was inconsistent in its response (proteinase inhibitor). Simultaneously, we measured three chemicals thought to be important nutrients for insect herbivores (water content, total nitrogen, and soluble carbohydrates). Water content declined with increasing drought stress intensity, total nitrogen increased at severe stress in one experiment and did not respond in a second, and soluble carbohydrates showed a convex response to drought stress. In one experiment we also fed leaf tissue, incorporated into non-nutritive agar, from control and drought-stressed plants to neonate Spodoptera exigua larvae. Growth of these larvae over a 7-d period was negatively affected by drought stress while survival was not significantly affected. This study represents one of the first to assess both chemical defenses and nutrients in plants subjected to drought as it develops from slight stress to a very severe condition. Depending on the direction and shape of response curves for nutrients and defenses, many possible effects on herbivores are predicted, some of them complex and nonlinear. By studying the particular kinetics of defenses and nutrients in plants we may be in a better position to understand why insect herbivores show such variable responses to drought-stressed plants.

Consequences of variation in flowering phenology for seed head herbivory and reproductive success in Erigeron glaucus (Compositae)

SummaryWe examined the relationship between flowering phenology, reproductive success (seed production only), and seed head herbivory for 20 similarly sized clones of Erigeron glaucus growing at Bodega Bay Reserve, northern California, USA. Although clones tended to reach peak flowering on the same date, they differed in the proportion of their total flowers produced around that date (flowering synchrony). Clones also differed in the number and density of flower heads presented at any one time to pollinators and herbivores (floral display). Both of these characteristics had consequences for herbivory and plant reproductive success. The proportion of flower heads damaged by insect herbivores was greater for clones that concentrated flowering activity during the main flowering period for the population as a whole (high synchrony) compared to clones that spread flowering out temporally. The primary reason for this result was that clones with low flowering synchrony produced a significant proportion of their flower heads during the fall and therefore, escaped attack by the tephritid fly, Tephritis ovatipennis. Clones with intermediate synchrony had lower seed success (total number of viable seeds produced over the year) than clones with either low or high synchrony. The proportion of flower heads damaged by insect herbivores and number of tephritid flies reared from flower heads were both negatively correlated to floral display while seed head mass and germination rates were positively related to display. Thus, clones which produced dense floral displays were favored both in terms of reduced herbivory and increased successful seed production.

TACHINID PARASITOIDS AFFECT HOST PLANT CHOICE BY CATERPILLARS TO INCREASE CATERPILLAR SURVIVAL

Current models of parasite–host interactions generally emphasize considerations of parasite virulence and parasite transmission rather than host responses to attack. We describe a situation in which parasitism causes a host to change its feeding behavior and this change improves the expected fitness of the host and probably the fitness of its parasites. We have found that a tachinid parasitoid (Thelaira americana) often emerges from its caterpillar host (Platyprepia virginalis) without killing the host. Whether the host caterpillar survives its parasites depends in part on what it has been eating. Unparasitized caterpillars were more likely to survive to adulthood when feeding on lupine, whereas parasitized caterpillars were more likely to survive on poison hemlock. Development time and pupal masses of caterpillars (both parasitized and unparasitized) were not found to be affected by the host plants that they fed on. Survival of fly larvae in caterpillars that we determined were parasitized using ultrasound was not affected by host plant. However, fly pupae that emerged from caterpillars that had been reared on hemlock were heavier than those emerging from lupine-fed caterpillars. This was due primarily to the direct effect of diet on the flies and less so to the indirect benefit to flies whose host caterpillars survived their parasites by feeding on hemlock. Parasitized caterpillars were more likely to select hemlock, and unparasitized caterpillars were more likely to select lupine when offered both host plants in field tests. These results were consistent for the two years that the choice experiments were conducted. These results were also consistent with the hypothesis that caterpillars change their food plant choices so as to increase their conditional success. Conditional food choices that increase success depending upon parasite load are well accepted for humans, controversial for other primates, and unknown for insects. If caterpillars alter their host plant choices as a result of their parasite load, then this phenomenon could help to explain the evolution of host plant choices that have defied explanation in the past. Such a suggestion assumes that nonlethal parasitism is a common phenomenon. We believe that this may be the case since we did not detect the nonlethal nature of this interaction until we began the unconventional practice of rearing in the field. Other workers have described nonlethal parasitism for several tachinid–host systems, and many families of flies are similar to tachinids except that their hosts are vertebrates; these interactions are nonlethal. Future empirical work, as well as models of parasite–host interactions, should consider the possibility that hosts alter their plant choices depending upon their parasite loads.

Abundance of phytoseiid mites on Vitis species: effects of leaf hairs, domatia, prey abundance and plant phylogeny

We observed the number of predatory mites (Phytoseiidae:Typhlodromus caudiglans) on the foliage of 20 North American species of grapes (Vitis spp) plus the domesticated EuropeanVitis vinifera, all grown in a common garden. We found relatively few phytophagous mites. The numbers of phytophagous mites were not correlated with the plant characteristics that we measured. We found approximately five times as many predatory mites as phytophagous mites and the numbers of these phytoseiid predators were not affected by the availability of prey. Similarly, numbers of phytoseiids were unaffected by plant gender and, hence, the availability of pollen, another source of food. The numbers of phytoseiids were not clustered according to the taxonomic grouping of the tested plant species. Leaf surface characteristics explained over 25% of the variance in the numbers of phytoseiids. Numbers of phytoseiids were positively associated with the density of vein hairs, the density of bristles in leaf axils, and the presence of leaf domatia. These results suggest that sheltered habitats rather than food availability may limit the numbers of phytoseiid mites on grapevines.

Predator-mediated apparent competition between two herbivores that feed on grapevines

We have been releasing economically unimportant herbivorous mites of one species early in the season and protecting grapevines against another, more damaging herbivorous mite throughout the growing season. In this experiment, releases of economically unimportant Willamette mites alone, or of predatory mites alone, failed to reduce populations of the damaging Pacific spider mite. However, where both herbivorous Willamette mites and predatory mites were released together populations of Pacific mites were reduced. This interaction between effects of Willamette mites and predatory mites suggests that predation against Pacific mites was more effective where alternate prey (Willamette mites) were available for the predators. The “apparent competition” between Willamette mites and Pacific mites, mediated through their shared predator, can be an important force in the agroecosystem although its importance varies from year to year and vineyard to vineyard.

Leaf pubescence and two-spotted spider mite webbing influence phytoseiid behavior and population density

Phytoseiid mites, both in agricultural and natural systems, can play an important role in the regulation of herbivorous mites. Host plant traits, such as leaf pubescence, may influence the dynamics between predator and prey. In this study, we examined the influence of leaf surface characteristics (leaf pubescence and two-spotted spider mite webbing) on the behavior of two species of predatory mites, the generalist Typhlodromus pyri and the spider mite specialist Phytoseiulus persimilis. In laboratory trials, T. pyri females consistently spent more time and deposited more eggs on leaf discs from trichome-rich apple varieties compared to relatively trichome-poor varieties. A similar result was found when the choice involved trichome-rich and trichome-poor apple varieties planted into the same pot where leaves were allowed to touch so that the mites could freely move from leaf to leaf. To further explore the effect of structure created by pubescence and to remove possible confounding effects of chemical cues, we added cotton fibers to trichome-free bean leaves. T. pyri females consistently spent more time and deposited more eggs on the side of a glabrous bean leaf with artificial cotton fibers versus the side without added fibers. When given a choice between two densities of cotton fibers, T. pyri females consistently selected the highest density of available fibers in which to to reside and oviposit. T. pyri also preferred cotton fiber configurations in which it could move underneath and access the plant surface. The artificial pubescent leaf was also used to test the effect of leaf hairs and two-spotted spider mite webbing on the behavior of P. persimilis. P. persimilis females preferred residing and ovipositing on surfaces with cotton fibers or two-spotted spider mite webbing than on bean leaf areas without these structures. When presented a choice between cotton fibers or webbing, the behavior of P. persimilis females depended on the cotton fiber density. In a mixed-variety apple orchard, we investigated the relationship between leaf pubescence and phytoseiid density under field conditions. We found a highly significant, positive relationship between density of trichomes on leaves and abundance of T. pyri, whereas spider mite prey numbers were uniformly low and unrelated to trichome density. These field results suggest that the behavioral responses found in our laboratory experiments have population consequences.

Plant drought stress and outbreaks of spider mites: a field test

A4bstract. I conducted a field experiment to clarify the relationship between drought stress of bush beans, Phaseolus vulgaris, and outbreaks of the twospotted spider mite, Tetranychus urticae, in the presence or absence of an important spider mite predator, Phytoseiulus persimilis. Spider mite populations were highest on well-watered and on severely stressed bean plants and lowest on slight-to-moderately stressed plants, indicating a nonlinear relationship. The predator exaggerated this pattern, reducing mite populations the most on moderately stressed plants and having the least impact on mites from severely stressed plants. Number of mites per unit leaf mass (a measure of mite injury to plants) was highest on severely stressed plants, lowest on slightly stressed plants, and intermediate on well-watered plants. Bean yield was negatively influenced by drought stress, with those plants that experienced high numbers of mites per unit leaf mass appearing to be more sensitive to drought than plants with low numbers of mites. The implications of these data for understanding the causes of pest outbreaks are discussed.

Host-Plant-Mediated Interactions between a Generalist Folivore and its Tachinid Parasitoid

We investigated the consequences of feeding on different species of host-plants on the performance of a generalist lepidopteran larva (Platyprepia virginalis (Bvd.) Arctiidae) and its interactions with a tachinid fly parasitoid (Thelairia bryanti Curran). Growth rate of P. virginalis was not different for larvae reared individually on either poison hemlock, Conium maculatum L., bush lupine, Lupinus arboreus Sims, or fiddle neck, Amsinckia menziesii (Lehm.) under laboratory conditions. 3. Further, larvae caged in the field on either hemlock or lupine did not differ in developmental rates or pupal mass. In 1 of 2 years survivorship was higher for moth larvae caged on hemlock

MITE VACCINATIONS FOR SUSTAINABLE MANAGEMENT OF SPIDER MITES IN VINEYARDS

We have successfully released phytophagous Willamette mites into Zinfandel vineyards that have had chronic problems with the economically more damaging Pacific spider mites. These releases induced resistance in the grapevines, causing smaller populations of Pacific mites and higher berry sugar concentrations. This study addresses the sustainability of our techniques. We define a sustainable technique as one that (1) is effective, (2) requires low inputs of resources, (3) is self-perpetuating, (4) produces minimal pollution, (5) produces minimal effects on non-target organisms, and (6) is compatible with other agronomic practices. Most of these criteria are met by our inoculation techniques; here we seek to determine the persistence of Willamette mites from one season to the next, and to evaluate effects of several commonly used agronomic practices on our vaccinations. Our data suggest that Willamette mites can be introduced a single time into a vineyard; they will reduce populations of Pacific mites and persist from year to year in the absence of miticides or other disruptions. We observed Willamette mites overwintering commonly on the grapevines and on box elder (Acer negundo) foliage adjacent to vineyards. Pacific mites were not observed overwintering in vineyards, and we surmise that they generally blow into vineyards during each growing season. We did not observe Willamette mites overwintering on cover crops although other phytophagous mites and predatory mites were found. In preliminary observations, we found no strong effects (positive or negative) associated with cover-cropping in terms of mite management. Vineyards with Pacific mites are often treated with miticides, either dicofol or propargite. We found that dicofol (but not propargite) was extremely disruptive to mite populations; after an initial kill, applications of dicofol were consistently associated with resurgences of mites that exceeded numbers found in unsprayed controls. Unlike applications of miticides, introductions of Willamette mites to control Pacific mites satisfy our criteria for sustainable agriculture. Here we demonstrated that they are self-perpetuating at low numbers from one season to the next. Furthermore, releasing Willamette mites for control of Pacific mites is compatible with some, but not all, management practices.

Leaf pubescence mediates the abundance of non-prey food and the density of the predatory mite Typhlodromus pyri

Plants with leaves having numerous trichomes or domatia frequently harbor greater numbers of phytoseiid mites than do plant with leaves that lack these structures. We tested the hypothesis that this pattern occurs, in part, with Typhlodromus pyri because trichomes increase the capture of pollen or fungal spores that serve as alternative food. Using a common garden orchard, we found that apple varieties with trichome-rich leaves had 2–3 times more pollen and fungal spores compared to varieties with trichome-sparse leaves. We also studied the effects of leaf trichome density and pollen augmentation on T. pyri abundance to test the hypothesis that leaf trichomes mediate pollen and fungal spore capture and retention and thereby influence phytoseiid numbers. Cattail pollen (Typha sp.) was applied weekly to mature ‘McIntosh’ and ‘Red Delicious’ trees grown in an orchard and, in a separate experiment, to potted trees of the same varieties. ‘McIntosh’ trees have leaves with many trichomes whereas leaves on the ‘Red Delicious’ trees have roughly half as many trichomes. With both field-grown and potted trees, adding cattail pollen to ‘Red Delicious’ trees increased T. pyri numbers compared to ‘Red Delicious’ trees without pollen augmentation. In contrast, cattail pollen augmentation had no effect on T. pyri populations on ‘McIntosh’ trees. Augmentation with cattail pollen most likely supplemented a lower supply of naturally available alternative food on ‘Red Delicous’ leaves and thereby enhanced predator abundance. These studies indicate that larger populations of T. pyri on pubescent plants are due, in part, to the increased capture and retention of pollen and fungal spores that serve as alternative foods.