Stephen C. Welter

DOES "ENEMY-FREE SPACE" EXIST? EXPERIMENTAL HOST SHIFTS OF AN HERBIVOROUS FLY

Natural enemies have been proposed as important agents of natural selection on herbivorous insects that may facilitate host plant shifts and increases in diet breadth. However, there is little experimental field work to support claims of host-shifting via escape from natural enemies, i.e., to enemy-free space. In this study, we took the unique approach of experimentally creating a host shift for a specialized leafmining fly, Liriomyza helianthi (Diptera: Agromyzidae). We manually transferred leafminer larvae from their normal host plant, Helianthus annuus (Asteraceae), to a variety of novel plants: Helianthus maximilianii, Ambrosia artemisiifolia, Taraxacum officinale, and Centaurea solstitialis. By exposing trans- ferred larvae on normal and novel plants to natural enemy attack under field conditions, we were able to examine whether host-shifting can provide an herbivore with enemy-free space. Our data show that enemy-free space does exist for L. helianthi immediately following a host shift, as mortality in novel plants averaged 17% less than in the normal host. Nevertheless, there was significant within- and between-year heterogeneity in results over the 3-yr period of the study. We found that escape from natural enemies was related to annual variation in the diversity and abundance of parasitoid species. In years when par- asitoid assemblages were dominated by endoparasitoids, mortality of larvae averaged 22% lower in novel hosts. However, when generalist ectoparasitoids, Diglyphus spp. (Hyme- noptera: Eulophidae), were present, there was no advantage of developing in novel plants, a result that could be explained by the less discriminating nature of the ectoparasitoids. When overall levels of mortality from natural enemies were high, the benefit of novel plants was also reduced. This pattern suggests that, as available larval hosts become scarce, parasitoids may be more likely to forage on novel host plants in search for prey, thus diminishing the opportunity for enemy-free space. Nevertheless, our study showed that enemy-free space can exist for an herbivorous insect utilizing a novel host plant, and that natural enemies may, in some cases, offset physiological fitness costs often associated with developing in novel plants. If all else is equal, the balance of these factors may facilitate the inclusion of novel host plants into the feeding repertoire of an herbivore.

Tolerance to herbivory by a stemboring caterpillar in architecturally distinct maizes and wild relatives

In a screenhouse experiment in southwest Mexico, we infested two maize cultivars, a land-race and a modern high-yielding variety, and two wild teosintes, Zea diploperennis and Zea mays parviglumis, with newly hatched larvae of the stemborer, Diatraea grandiosella. While subsequent damage levels, when corrected for differences in plant size, were highest in the wild perennial, Zea diploperennis, this taxon showed the lowest absolute and proportional reductions in growth and reproduction, i.e., it was most tolerant to the damage. Higher growth rates were not associated with tolerance. Rather, a greater number of tillers and leaves in the wild taxa allowed for compartmentalization of damage and greater developmental plasticity. These results, when combined with previous findings on effective defense patterns, indicate that tolerance in maizes and wild relatives may be positively associated with defense against stemboring by the same insect. Because the probable mechanisms for defense (tissue fiber) and tolerance (plant architecture) are unrelated, a positive association is contrary to the predictions of some optimal defense theories, which posit a negative relationship between tolerance and defense.

Correlated Insecticide Cross-Resistance in Azinphosmethyl Resistant Codling Moth (Lepidoptera: Tortricidae)

Abstract Resistance to several classes of insecticides was correlated with azinphosmethyl resistance in codling moth, Cydia pomonella (L.), in California. In tests of laboratory and field populations, cross-resistance was positively correlated with azinphosmethyl and two organophosphates (diazinon, phosmet), a carbamate (carbaryl), a chlorinated hydrocarbon (DDT), and two pyrethroids (esfenvalerate and fenpropathrin). Additionally, negatively correlated cross-resistance was identified between azinphosmethyl and two other organophosphates, chlorpyrifos and methyl parathion. Patterns of resistance observed in laboratory colonies were confirmed with field bioassays. In bioassays of field populations, azinphosmethyl resistance was observed to increase from 1991 to 1993, although levels of resistance remained <13-fold. Because orchards with azinphosmethyl resistance have had difficulties with suppression of codling moth, and cross-resistance was found for all tested classes of insecticides, strategies for managing resistance will need to be developed so as to protect current and future control tactics. The two insecticides with negatively correlated cross-resistance are discussed as potential tools for resistance management.

Detecting Cacopsylla pyricola (Hemiptera: Psyllidae) in predator guts using COI mitochondrial markers.

Cacopsylla pyricola (Förster) is one of the most important pests of pear in North America, where several native predators have been considered for integrated pest management (IPM) programmes. Two molecular markers of 271 and 188 bp were developed from C. pyricola cytochrome oxidase I (COI) fragments, in order to study the detection of this species in the gut of arthropod predators. Primer sensitivity and the detection period for pear psylla remains in the guts of Anthocoris tomentosus Pericart were determined. The sensitivity threshold was defined at 10-5 dilution of a C. pyricola fifth-instar nymph in all samples. Predator adults were evaluated immediately after ingestion of one to five C. pyricola nymphs (t = 0) and after 2, 4, 6, 8, 16, 24 and 32 h. Detection of the presence of C. pyricola DNA always lasted longer using the shorter fragment and was observed after 32 h of digestion using both markers. The primers amplifying the 188 bp fragment amplified all four psyllid species tested, whereas the primers designed to amplify the 271 bp fragment did so exclusively for C. pyricola and its close relative, Cacopsylla pyri (Linnaeus). Both primers failed to amplify DNA from representative species of the Coccinellidae, Chrysopidae, Hemerobiidae, Anthocoridae, Miridae, Salticidae, Aphididae, Tetranychidae and the Tortricidae, suggesting their suitability for general trophic studies.

Crop domestication disrupts a native tritrophic interaction associated with the sunflower, Helianthus annuus (Asterales: Asteraceae)

Abstract.  1. Crop domestication has been a largely overlooked factor that may explain why insect herbivores tend to be more abundant and less attacked in agricultural habitats than in native habitats. This study explores how domestication of the sunflower, Helianthus annuus L., affects the sunflower moth, Homoeosoma electellum (Lepidoptera: Pyralidae), and its parasitoids.

Abundance of a Native Moth Homoeosoma electellum (Lepidoptera: Pyralidae) and Activity of Indigenous Parasitoids in Native and Agricultural Sunflower Habitats

Abstract Insect herbivores have been assumed to be more abundant in agricultural habitats than in native habitats; however, this hypothesis is rarely tested explicitly by comparing field populations of domesticated plants and their wild ancestors. This study examined the abundance of the sunflower moth, Homoeosoma electellum (Hulst), and its parasitism by natural enemies in agricultural and native sunflower habitats. Nutrient levels and plant population factors in the two habitat types were measured to identify factors associated with the patterns of herbivory and parasitism. Adult male and larval H. electellum were consistently more abundant in agricultural habitats. In contrast, parasitism of H. electellum was 6–10 times higher in native sunflower habitats than in agricultural habitats. Also, fewer parasitoid species were found in agricultural habitats, and parasitism by individual parasitoid species was reduced by 90%. Larval densities per flower head were higher on agricultural plants, but parasitoids failed to respond to the higher densities. The relationship between flower age and larval infestation differed between agricultural and wild flowers; larval age tracked agricultural flower age, but on wild flowers, larvae moved from older to younger flowers. Among the three nutrients sampled, only nitrogen was positively correlated with habitat differences. These results indicate that patterns of trophic interactions varied by habitat type and were related to plant phenotypic changes and environmental habitat factors such as crop domestication, nitrogen fertilization, and plant phenology.

Integrating pesticide effects with inundative biological control: interpretation of pesticide toxicity curves for Anaphes iole in strawberries

We examined pesticide residue effects on the egg parasitoid Anaphes iole Girault (Hymenoptera: Mymaridae), an inundative biological control agent for Lygus hesperus Knight (Heteroptera: Miridae) in strawberries (Fragaria×ananassa Duchesne). Our objectives were to identify compatible pesticides, determine appropriate parasitoid release timings for minimizing harmful effects, and develop an approach for interpreting pesticide toxicity curves. Six insecticides, 2 acaricides and 6 fungicides were tested, and survivorship of adult A. iole exposed to foliar residues for 48 h, at 4–6 different times after pesticide application, was examined. A logistic function was developed for incorporating control mortality at each test date. Values for LT50 (Lethal Time for 50% mortality) and mortalities on day 1 (initial mortality) and day 13 (estimated maximum time parasitoid releases can be delayed under extreme summer conditions) were estimated. In the study, insecticide residues proved to be the most toxic, followed by those from acaricides while most fungicides were least toxic. Among insecticides, fenpropathrin, bifenthrin and carbaryl caused the greatest mortality (estimated mortality on day 13 > 75%). Residues of naled resulted in the least mortality (LT50LT50=3.2 days) followed by methomyl (LT50=8.3 days) and malathion (LT50=13.2 days). Estimated mortality = 12.3% on day 13 for the acaricide propargite and < 1% for abamectin. For the fungicides benomyl, captan, myclobutanil and thiram, estimated mortality on day 1 was < 1%, and for iprodione it was < 6%, indicating compatibility with A. iole releases. For sulfur, LT50=0, but the mortality decay curve was relatively flat (estimated mortality on day 13=13.6%). These results suggest possibilities for integrating A. iole releases with certain pesticide programs by appropriate timing of pesticide applications to minimize negative impacts.

Potential for Outbreaks of Leafrollers (Lepidoptera: Tortricidae) in California Apple Orchards Using Mating Disruption for Codling Moth Suppression

Abstract Two species of leafrollers, Argyrotaenia citrana (Fernald) and Pandemis pyrusana Kearfott, represent serious obstacles to the implementation of mating disruption for control of codling moth in coastal California apple orchards. Larval and adult densities of A. citrana and P. pyrusana and subsequent fruit damage were compared under different codling moth control treatments. Leafroller larval counts and levels of fruit damage were significantly higher in most plots that were untreated or treated only with codling moth pheromone. Leafroller fruit damage levels in these plots were commonly between 10 and 15% at harvest. As summer larval counts were good predictors of fruit damage levels, larval sampling could be a useful tool for predicting leafroller outbreaks. Use of pheromone trapping for A. citrana to detect localized outbreaks within an orchard was not useful and failed to correlate with larval numbers, whereas adult monitoring for P. pyrusana appears more promising. Efforts to implement a codling moth mating-disruption program in California must include changes in strategies for monitoring and controlling leafroller species.

GENETIC DIVERGENCE IS DECOUPLED FROM ECOLOGICAL DIVERSIFICATION IN THE HAWAIIAN NESOSYDNE PLANTHOPPERS

Adaptive radiation involves ecological shifts coupled with isolation of gene pools. However, we know little about what drives the initial stages of divergence. We study a system in which ecological diversification is found within a chronologically well‐defined geological matrix to provide insight into this enigmatic phase of radiation. We tested the hypothesis that a period of geographic isolation precedes ecological specialization in an adaptive radiation of host‐specialized Hawaiian planthoppers. We examined population structure and history using mitochondrial and multiple independent microsatellite loci in a species whose geographic distribution on the island of Hawaii enabled us to observe the chronology of divergence in its very earliest stages. We found that genetic divergence is associated with geographic features but not different plant hosts and that divergence times are very recent and on the same timescales as the dynamic geology of the island. Our results suggest an important role for geography in the dynamics of the early stages of divergence.

Parasitism of Lygus hesperus (Miridae) by Anaphes iole (Mymaridae) and Leiophron uniformis (Braconidae) in California strawberry

Abstract Augmentative releases of two parasitoids, Anaphes iole Girault and Leiophron uniformis (Gahan), were evaluated for control of Lygus hesperus Knight populations on strawberry. Small cages were used to evaluate a range of parasitoid release rates on known densities of L. hesperus eggs or nymphs. In addition, the number of ovipositions per female L. uniformis and the distribution of ovipositions per nymph were determined for two densities of L. hesperus nymphs. Parasitism levels reached 80% for A. iole and nearly 100% for L. uniformis , indicating that these parasitoids will search for and parasitize Lygus in strawberry. A. iole was successfully reared from Lygus eggs within strawberry plants. Thus this host plant does not appear to be a barrier to the development of augmentative biological control. The distribution of L. uniformis ovipositions per host did not vary consistently from random in response to either host or parasitoid density. Ovipositions per parasitoid did not change in response to parasitoid release rate if high numbers of nymphs (300 per cage) were present. When half this number of nymphs were exposed to the same parasitoid release rates, the number of ovipositions per parasitoid declined as parasitoid densities increased. This indicates that for L. uniformis the level of mutual interference is influenced by both host and parasitoid density, not parasitoid density alone.