Joseph S. Elkinton

Interactions Among Gypsy Moths, White‐footed Mice, and Acorns

Low-density populations of gypsy moth, Lymantria dispar, were studied over a 10-yr period in Massachusetts. Increases in gypsy moth density were associated with declines in density of the white-footed mouse, Peromyscus leucopus, a principal predator. Furthermore, changes in density of P. leucopus populations were positively correlated with the density of acorn crops, a dominant winter food source for these mice. To demonstrate these effects we used a novel bootstrap regression method that adjusts for spatial and temporal autocorrelation in the time series data. The findings are compatible with a dual equilibrium model of gypsy moth population dynamics, in which low densities are regulated by mice and high densities are regulated by other factors, notably a virus disease.

HOST HETEROGENEITY IN SUSCEPTIBILITY AND DISEASE DYNAMICS: TESTS OF A MATHEMATICAL MODEL

Most mathematical models of disease assume that transmission is linearly dependent on the densities of host and pathogen. Recent data for animal diseases, however, have cast doubt on this assumption, without assessing the usefulness of alternative models. In this article, we use a combination of laboratory dose‐response experiments, field transmission experiments, and observations of naturally occurring populations to show that virus transmission in gypsy moths is a nonlinear function of virus density, apparently because of heterogeneity among individual gypsy moth larvae in their susceptibility to the virus. Dose‐response experiments showed that larvae from a laboratory colony of gypsy moths are substantially less heterogeneous in their susceptibility to the virus than are larvae from feral populations, and field experiments showed that there is a more strongly nonlinear relationship between transmission and virus density for feral larvae than for lab larvae. This nonlinearity in transmission changes the dynamics of the virus in natural populations so that a model incorporating host heterogeneity in susceptibility to the virus gives a much better fit to data on virus dynamics from large‐scale field plots than does a classical model that ignores host heterogeneity. Our results suggest that heterogeneity among individuals has important effects on the dynamics of disease in insects at several spatial and temporal scales and that heterogeneity in susceptibility may be of general importance in the ecology of disease.

MEASURING AND TESTING FOR SPATIAL SYNCHRONY

Spatial synchrony in abundance among populations at different locations has been studied for many species. Different statistics have been used as measures of synchrony, and various techniques have been employed to test the hypothesis that there is no synchrony. In this paper we first describe and contrast various measures of synchrony and then discuss testing for no synchrony. Tests that ignore the serial correlation are commonly employed but are incorrect if there is serial correlation present, as is often the case with populations followed over time. Alternative approaches and their limitations are presented including tests based on residuals, adjusted degrees of freedom tests, and bootstrap procedures. We recommend tests based on residuals in a model-based setting. We also discuss some of the difficulties of finding model-free approaches and suggest some methods based on confidence intervals for future study.

What causes outbreaks of the gypsy moth in North America

Abstract The gypsy moth has been present in North America for more than 100 years, and in many of the areas where it has become established outbreaks occur with varying degrees of periodicity. There also exists extensive spatial synchrony in the onset of outbreaks over large geographic regions. Density-dependent mortality clearly limits high-density populations, but there is little evidence for strong regulation of low-density populations. Predation by small mammals appears to be the major source of mortality affecting low-density populations, but because these are generalist predators and gypsy moths are a less preferred food item, mammals do not appear to regulate populations in a density-dependent fashion. Instead, predation levels appear to be primarily determined by small mammal abundance, which is in turn closely linked to the production of acorns that are a major source of food for overwintering predator populations. Mast production by host oak trees is typically variable among years, but considerable spatial synchrony in masting exists over large geographic areas. Thus, it appears that the temporal and spatial patterns of mast production may be responsible for the episodic and spatially synchronous behavior of gypsy moth outbreaks in North America. This multitrophic relationship among mast, predators, and gypsy moths represents a very different explanation of forest insect outbreak dynamics than the more widely applied theories based upon predator–prey cycles or feedbacks with host foliage quality.

Using simple models to predict virus epizootics in gypsy moth populations

1. Biologists have made little use of recent advances in the mathematical theory of the dynamics of insect pathogens, because of difficulties with parameter estimation and misgivings about the simplicity of the models in question. 2. We use an existing simple model for the dynamics of insect pathogens, slightly modified both to provide greater accuracy and to allow for more straightforward parameter estimation. 3. Focusing on the nuclear polyhedrosis virus (NPV) of gypsy moth (Lymantria dispar (L.)), we estimated each of the model parameters independently, estimating three of the four model parameters from the literature

Observer bias and the detection of low-density populations

Monitoring programs increasingly are used to document the spread of invasive species in the hope of detecting and eradicating low-density infestations before they become established. However, interobserver variation in the detection and correct identification of low-density populations of invasive species remains largely unexplored. In this study, we compare the abilities of volunteer and experienced individuals to detect low-density populations of an actively spreading invasive species, and we explore how interobserver variation can bias estimates of the proportion of sites infested derived from occupancy models that allow for both false negative and false positive (misclassification) errors. We found that experienced individuals detected small infestations at sites where volunteers failed to find infestations. However, occupancy models erroneously suggested that experienced observers had a higher probability of falsely detecting the species as present than did volunteers. This unexpected finding is an artifact of the modeling framework and results from a failure of volunteers to detect low-density infestations rather than from false positive errors by experienced observers. Our findings reveal a potential issue with site occupancy models that can arise when volunteer and experienced observers are used together in surveys.

Pathogen‐Driven Outbreaks in Forest Defoliators Revisited: Building Models from Experimental Data

Models of outbreaks in forest‐defoliating insects are typically built from a priori considerations and tested only with long time series of abundances. We instead present a model built from experimental data on the gypsy moth and its nuclear polyhedrosis virus, which has been extensively tested with epidemic data. These data have identified key details of the gypsy moth–virus interaction that are missing from earlier models, including seasonality in host reproduction, delays between host infection and death, and heterogeneity among hosts in their susceptibility to the virus. Allowing for these details produces models in which annual epidemics are followed by bouts of reproduction among surviving hosts and leads to quite different conclusions than earlier models. First, these models suggest that pathogen‐driven outbreaks in forest defoliators occur partly because newly hatched insect larvae have higher average susceptibility than do older larvae. Second, the models show that a combination of seasonality and delays between infection and death can lead to unstable cycles in the absence of a stabilizing mechanism; these cycles, however, are stabilized by the levels of heterogeneity in susceptibility that we have observed in our experimental data. Moreover, our experimental estimates of virus transmission rates and levels of heterogeneity in susceptibility in gypsy moth populations give model dynamics that closely approximate the dynamics of real gypsy moth populations. Although we built our models from data for gypsy moth, our models are, nevertheless, quite general. Our conclusions are therefore likely to be true, not just for other defoliator‐pathogen interactions, but for many host‐pathogen interactions in which seasonality plays an important role. Our models thus give qualitative insight into the dynamics of host‐pathogen interactions, while providing a quantitative interpretation of our gypsy moth–virus data.

EFFECTS OF SYNCHRONY WITH HOST PLANT ON POPULATIONS OF A SPRING‐FEEDING LEPIDOPTERAN

Comparisons of traits of outbreaking and nonoutbreaking leaf-eating Lepi- doptera and Symphyta have shown that spring-feeding species are more likely to have outbreaks than are summer-feeding species. It has been suggested that variable synchrony with host budburst causes the population sizes of spring-feeding species to be more variable primarily because of the negative effects of older leaves on insects. While much evidence exists that leaf age can directly affect survival and reproduction of insects, few studies have looked at the population-level effects of variable phenology, and especially the po- tential for complex direct and indirect interactions with natural-enemy effects. To examine the consequences of variable phenology for population growth of an outbreaking insect, we manipulated the timing of gypsy moth ( Lymantria dispar) egg hatch in the field. We released large numbers of gypsy moth larvae into replicate plots in the field at three times relative to budburst. Survival of larvae in protective sleeves was high unless they were released very long before host budburst, and leaf age had a direct negative effect on fecundity: the later the release, the lower was the fecundity of insects reared on white oak and black oak. The later the release, however, the greater was the dispersal by ballooning, which had the effect of reducing local densities. Because the most important natural enemies impose density-dependent mortality, dispersal had the effect of raising survival rate for later release dates. The direct host-plant effect and natural-enemy effects exhibited opposing influences on population processes, because fecundity decreased with release date but sur- vival increased. The survival advantage of the late release outweighed the loss in fecundity, so that the expected population growth rate was highest for the latest release. The net effects of phenology on insect population growth thus depend largely on natural-enemy effects. Very different conclusions would have been drawn had we measured mortality only in protective sleeves and not in the presence of natural enemies. The strong natural-enemy effects may explain the large variability in outcome of plant-herbivore interactions and contribute to the high variability in population size of spring-feeding species.

Density-Dependent Suppression of Experimentally Created Gypsy Moth, Lymantria dispar (Lepidoptera: Lymantriidae), Populations by Natural Enemies

SUMMARY (1) Experimental manipulations of densities of gypsy moths revealed a strong, positive spatially density-dependent reduction in population size, a response not evident in past studies of natural populations in North America. (2) Positive density-dependent mortality occurred during the early and mid larval stages and was primarily due to Compsilura concinnata, a polyphagous parasitoid. (3) The oviposition rate of Parasetigena silvestris, an oligophagous parasitoid of gypsy moths, was initially inversely density-dependent but became positively density-dependent during the late larval period. (4) Phobocampe disparis showed an inversely density-dependent response, and predation by small mammals on pupae deployed in the litter was lower in plots with

Biomodal patterns of mortality from nuclear polyhedrosis virus in gypsy moth (Lymantria dispar) populations

Abstract A bimodal temporal pattern of mortality caused by the nuclear polyhedrosis virus (NPV) was observed in nine gypsy moth ( Lymantria dispar ) populations of varying densities. In all cases, peak mortality from NPV occurred during the second wave (late larval instars) and the highest mortality occurred in high density populations. Patterns of NPV mortality were established several weeks before being expressed. There was no discernible correlation between weekly mortality rates and temperature, rainfall, or total solar radiation. The bimodality was also apparent in NPV contamination on foliage which was measured by bioassay. A similar pattern was observed in the laboratory among larvae reared in groups from field-collected egg masses and from eggs artificially contaminated with NPV from a laboratory population. As in field populations, the period of low mortality from NPV between the two waves occurred when most larvae were late third and fourth instars. Larvae reared individually did not exhibit the second wave of mortality.