Robin J. Stuart

Ecology in the service of biological control: the case of entomopathogenic nematodes

Abstract Biological control manipulations of natural enemies to reduce pest populations represent large-scale ecological experiments that have both benefited from and contributed to various areas of modern ecology. Unfortunately, economic expediency and the need for rapid implementation often require that biological control programs be based more on trial and error than on sound ecological theory and testing. This approach has led to some remarkable successes but it has also produced dismal failures. This point is particularly well illustrated in the historical development and use of entomopathogenic nematodes for the biological control of insect pests. Intense effort has focused on developing these natural enemies as alternatives to chemical insecticides, in part because laboratory assays indicated that these nematodes possess a broad host range. This illusory attribute launched hundreds of field releases, many of which failed due to ecological barriers to infection that are not apparent from laboratory exposures, where conditions are optimal and host-parasite contact assured. For example, the entomopathogenic nematode Steinernema carpocapsae is a poor choice to control scarab larvae because this nematode uses an ambusher foraging strategy near the soil surface whereas the equally sedentary scarab remains within the soil profile, shows a weak host recognition response to scarabs, has difficulty overcoming the scarab immune response, and has low reproduction in this host. Conversely, two other nematodes, Heterorhabditis bacteriophora and S. glaseri, are highly adapted to parasitize scarabs: they use a cruising foraging strategy, respond strongly to scarabs, easily overcome the immune response, and reproduce well in these hosts. Increased understanding of the ecology of entomopathogenic nematodes has enabled better matches between parasites and hosts, and more accurate predictions of field performance. These results underline the importance of a strong partnership between basic and applied ecology in the area of biological control.

Selection alters the pattern of emergence from the host cadaver in the entomopathogenic nematode, Steinernema glaseri

We used selection to test for a genetic component to the pattern of emergence of infective juveniles from the host cadaver in the entomopathogenic nematode, Steinernema glaseri (Steiner), and whether other traits would respond to selection on this major and complex life-history character. We selected for early (‘ fast’) and late (‘ slow’) emerging lines by perpetuating nematodes that emerged on the first and after the seventh day of emergence respectively. After 12 cycles of selection, the pattern for the slow line but not the fast line differed significantly from the base population. Cumulative emergence for the slow line was less than the base population from Days 4 to 14 of the 18-day emergence period. The maximum difference occurred on the fourth day when 72·6% of emergence was complete for the base population but only 55·4% for the slow line. Decreases in infective juvenile size over the emergence period were consistent with the change in emergence pattern, but variation in sex ratios was not. No differences in infectivity were found. These results indicate that the emergence pattern has a genetic component, and that genetic variability for this trait occurs in natural populations. Furthermore, the asymmetric response to selection suggests that our field population is under strong selection for a highly skewed early emergence.

Antibiotic resistance and protease production by Photorhabdus luminescens and Xenorhabdus poinarii bacteria symbiotic with entomopathogenic nematodes: variation among species and strains

Abstract Bacteria in the genera Photorhabdus and Xenorhabdus are highly pathogenic to insects and are symbiotically associated with nematodes in the genera Heterorhabditis and Steinernema , respectively. We compared extracellular protease production and resistance to antibiotics (chloramphenicol, erythromycin, neomycin and tetracycline) for 32 isolates of P. luminescens and 11 isolates of X. poinarii taken from nematodes isolated from soil in southern New Jersey. P. luminescens produced greater amounts of protease, and was more resistant to erythromycin and less resistant to neomycin than X. poinarii . No interspecific differences in resistance to chloramphenicol or tetracycline were detected. Variability within species was not related to the site, habitat or soil core from which the isolates were obtained, and was not associated with variation in the color of the host cadaver for P. luminescens . Resistance to erythromycin was positively correlated with resistance to both neomycin and tetracycline for P. luminescens , but was negatively correlated with resistance to neomycin for X. poinarii . Antibiotic resistance profiles and extracellular protease production might be useful characteristics for distinguishing among species and strains of these bacteria, probably have ecological significance with respect to intra- and interspecific competition within host cadavers, and could have implications for the utility of these organisms for biological control.

Egg-Mass Variability and Differential Parasitism of Choristoneura parallela (Lepidoptera: Tortricidae) by Endemic Trichogramma minutum (Hymenoptera: Trichogrammatidae)

Abstract The fireworm Choristoneura parallela (Robinson) is a major pest in New Jersey cranberry bogs where it produces two generations each year. Eggs are laid in compact, single-layered masses of a few to >300 eggs on the leaves of various plant species, and are parasitized by the endemic generalist egg parasite, Trichogramma minutum Riley. In preparation for an augmentative biological control program using T. minutum, we assessed egg-mass variability and parasitism rates in a series of unmanipulated field populations. We examined 193,950 eggs from 1,789 egg masses on 17 plant species, which represented 12 samples taken from three bogs (one sample per generation per bog each year for 2 yr). Egg-mass size, shape, and density (number of eggs per unit area within masses) differed across samples and plant species. Egg masses on narrow-leafed species (e.g., redroot, swamp candles, and grasses) tended to be longer and narrower than those on broad-leafed species (e.g., brier, red maple, leatherleaf, marsh Saint John’s wort, and marsh fern). Relatively few eggs per mass on certain plant species (e.g., marsh fern) indicate possible host preferences, whereas unusually high (e.g., grasses, sweet pepperbush) or low (e.g., marsh fern) densities indicate additional host plant influences on egg mass structure. Overall, T. minutum parasitized 4,309 eggs (2.2%) from 271 egg masses (15.1%) on 12 plant species, which included the 11 most common fireworm host plants. Parasitism rates for egg masses varied from 1.6 to 44.9% across samples, and only 11 parasitized masses were completely parasitized (4.1%). Parasitized masses had fewer eggs and lower density than nonparasitized masses, but did not differ in length, width, area, or circumference. T. minutum exhibited an apparent preference for masses on sweet pepperbush and marsh Saint John’s wort over those on leatherleaf. This preference was not fully explained by egg number or density, and might be associated with other differences among egg masses or host plants. These results indicate potentially complex tritrophic interactions that could have important implications for the development, monitoring, and success of biological control programs.

Short Communication: On the Relationship Between the Ant, Acanthomyops claviger, and the Blueberry Mealybug, Dysmicoccus vaccinii

Many ant species in the subfamilies Myrmicinae, Dolichoderinae, and Formicinae associate with plant-feeding homopterans and obtain from them a carbohydrate-rich digestive product known as honeydew. Often the relationship between ants and homopterans appears to be a highly evolved symbiosis, and most myrmecophilous homopterans have various morphological and behavioral adaptations that appear to facilitate ant attendance. For example, in aphids these adaptations can include modified cornicles, cauda, wax filaments, and setae, as well as specialized postures and honeydew excretion mechanisms. In turn, ants also exhibit apparent behavioral adaptations for this association, with some species defending their homopterans against predators and parasites, building shelters around them, and transporting them among host plants. Some ant queens even carry homopterans on their nuptial flights as an apparent mechanism to perpetuate this association (see reviews by Way, 1963; Buckley, 1987; Hölldobler and Wilson, 1990). Although the relationship between ants and their tended homopterans generally appears to be mutualistic, the details of the relationships between particular species can be quite variable. Indeed, some homopterans appear to benefit more from associations with certain ant species than with others