Long-distance dispersal of the gypsy moth (Lepidoptera: Lymantriidae) facilitated its initial invasion of Wisconsin

Gypsy moth (Lymantria dispar L.) spread is dominated by stratified dispersal, and, although spread rates are variable in space and time, the gypsy moth has invaded Wisconsin at a consistently higher rate than in other regions. Allee effects, which act on low-density populations ahead of the moving population that contribute to gypsy moth spread, have also been observed to be consistently weaker in Wisconsin. Because a major cause of an Allee effect in the gypsy moth is mate-finding failure at low densities, supplementing low-density populations with immigrants that arrive through dispersal may facilitate establishment and consequent spread. We used local indicator of spatial autocorrelation methods to examine space-time gypsy moth monitoring data from 1996 to 2006 and identify isolated, low-density colonies that arrived through dispersal. We measured the distance of these colonies from the moving population front to show that long-distance dispersal was markedly present in earlier years when Wisconsin was still mainly uninfested. Recently, however, immigrants arriving through long-distance dispersal may no longer be detected because instead of invading uninfested areas, they are now supplementing high-density colonies. In contrast, we observed no temporal pattern in the distance between low-density colonies and the population front in West Virginia and Virginia. We submit that long-distance dispersal, perhaps facilitated through meteorological mechanisms, played an important role in the spread dynamics of the initial Wisconsin gypsy moth invasion, but it currently plays a lesser role because the portion of Wisconsin most susceptible to long-distance immigrants from alternate sources is now heavily infested.     

Prey‐processing by avian predators enhances virus transmission in the gypsy moth

The Lymantria dispar nucleopolyhedrovirus (LdNPV) is one of the most important regulators of gypsy moth populations, but some aspects of its transmission remain poorly understood, particularly its high rate of spatial spread and ability to persist in low‐density populations. We tested the role of predatory birds in the transmission of this virus using experimental gypsy moth populations in an aviary. Predatory birds captured virus‐infected caterpillars and facilitated viral dispersal via two processes: 1) by ingesting infected caterpillars and passing viral occlusion bodies (OBs) through their guts, and 2) by scattering OBs during predator‐specific processing behaviors, a mechanism documented here for the first time. The relative importance of both pathways differed by predator species. After eating virus‐infected gypsy moth larvae, red‐eyed vireos and black‐capped chickadees passed more gypsy moth nucleopolyhedrovirus in feces than did gray catbirds. During prey‐processing, the repetitive beating of caterpillars by red‐eyed vireos, a behavior that was rarely utilized by chickadees and catbirds, resulted in the scattering of infectious virus. Due to the combination of efficient gut passage and virus spread from prey beating, higher rates of transmission occurred in experimental gypsy moth populations exposed to red‐eyed vireos than those exposed to catbirds or chickadees. Our results show that effective virus transmission was achieved when virus was vectored by predatory birds through a combination of both behavioral and physiological traits.     

Interpretation of gypsy moth frontal advance using meteorology in a conditional algorithm

The gypsy moth, Lymantria dispar, is a non-native species that continues to invade areas in North America. It spreads generally through stratified dispersal where local growth and diffusive spread are coupled with long-distance jumps ahead of the leading edge. Long-distance jumps due to anthropogenic movement of life stages is a well-documented spread mechanism. Another mechanism is the atmospheric transport of early instars and adult males, believed to occur over short distances. However, empirical gypsy moth population data continue to support the possibility of alternative methods of long-range dispersal. Such dispersal events seemed to have occurred in the mid- to late-1990s with spread across Lake Michigan to Wisconsin. Such dispersal would be against the prevailing wind flow for the area and would have crossed a significant physical barrier (Lake Michigan). The climatology of the region shows that vigorous cyclones can result in strong easterly winds in the area at the time when early instars are present. It is hypothesized that these storms would enable individuals to be blown across the Lake and explain the appearance of new population centers observed at several locations on the western shore of Lake Michigan nearly simultaneously. A synoptic climatology model coupled with population dynamics data from the area was parameterized to show an association between transport events and population spread from 1996 to 2007. This work highlights the importance of atmospheric transport events relative to the invasion dynamics of the gypsy moth, and serves as a model for understanding this mechanism of spread in other related biological invasions.     

Gypsy moth response to landscape structure differs from neutral model predictions: implications for invasion monitoring

Simulations of dispersal across computer-generated neutral landscapes have generated testable predictions about the relationship between dispersal success and landscape structure. Models predict a threshold response in dispersal success with increasing habitat fragmentation. A threshold is defined as an abrupt, disproportionate decline in dispersal success at a certain proportion of habitat in the landscape. To identify potential empirical threshold responses in invasion success to landscape structure, we quantified the relationship between progression of the gypsy moth (Lymantria dispar) invasion wavefront across Michigan (1985–1996) and the structure of the Michigan landscape using two indices of invasion success and six landscape metrics. We also examined the effect of scale of analysis and choice of land cover characterization on our results by repeating our analysis at three scales using two different land cover maps. Contrary to simulation model predictions, thresholds in invasion success did not correspond closely with thresholds in landscape structure metrics. Increased variation in invasion success indices at smaller scales of analysis also suggested that invasion success should be studied at larger spatial extents (≥75 km²) than would be appropriate for characterizing individual dispersal events. The predictions of individual dispersal models across neutral landscapes may have limited applications for the monitoring and management of vagile species with excellent dispersal capabilities such as the gypsy moth.     

Persistence of invading gypsy moth populations in the United States

Exotic invasive species are a mounting threat to native biodiversity, and their effects are gaining more public attention as each new species is detected. Equally important are the dynamics of exotic invasives that are previously well established. While the literature reports many examples of the ability of a newly arrived exotic invader to persist prior to detection and population growth, we focused on the persistence dynamics of an established invader, the European gypsy moth (Lymantria dispar) in the United States. The spread of gypsy moth is largely thought to be the result of the growth and coalescence of isolated colonies in a transition zone ahead of the generally infested area. One important question is thus the ability of these isolated colonies to persist when subject to Allee effects and inimical stochastic events. We analyzed the US gypsy moth survey data and identified isolated colonies of gypsy moth using the local indicator of spatial autocorrelation. We then determined region-specific probabilities of colony persistence given the population abundance in the previous year and its relationship to a suite of ecological factors. We observed that colonies in Wisconsin, US, were significantly more likely to persist in the following year than in other geographic regions of the transition zone, and in all regions, the abundance of preferred host tree species and land use category did not appear to influence persistence. We propose that differences in region-specific rates of persistence may be attributed to Allee effects that are differentially expressed in space, and that the inclusion of geographically varying Allee effects into colony-invasion models may provide an improved paradigm for addressing the establishment and spread of gypsy moth and other invasive exotic species.     

Anthropogenic drivers of gypsy moth spread

The gypsy moth, Lymantria dispar (L.), is a polyphagous defoliator introduced to Medford, Massachusetts in 1869. It has spread to over 860,000 km² in North America, but this still only represents ¼ of its susceptible host range in the United States. To delay defoliation in the remaining susceptible host range, the government maintains a barrier zone and a quarantine, reflecting a presumption that anthropogenic factors are important in the spread of gypsy moth. We develop a model framework that relates these factors along with biophysical characteristics to a county’s susceptibility to gypsy moth invasion. We then compile a dataset for counties within 200 km of the infested area and use trap catch data from 1999 to 2007 to estimate the probability of gypsy moth presence. As expected, gypsy moth is more likely to be found close to the population front and to traps that recorded moths in the previous year. However, when controlling for these factors, our most robust finding is that the use of wood for home heating and energy is consistently positively correlated with the presence of gypsy moth. In contrast, the movement of wood products by industry, which is actively regulated by state and federal governments, is rarely correlated with the presence of gypsy moth. This is consistent with effective regulation of the movement of goods by industry, but not by the public. Our findings provide empirical support for the importance and challenge of firewood as a vector for non-native forest insects.     

Effect of conidial dispersal of the fungal pathogen Entomophaga maimaiga (Zygomycetes: Entomophthorales) on survival of its gypsy moth (Lepidoptera: Lymantriidae) host

Several researchers have developed a one-generational computer model that simulates infection prevalence of gypsy moth, Lymantria dispar, caterpillars by its fungal pathogen, Entomophaga maimaiga. Inputs required are temperature, humidity, and rainfall records, a measure of fungus resting spore load in the soil, and an estimate of gypsy moth larval density. In a previous study, the model accurately tracked fungal-induced host mortality as long as airborne fungal conidia were allowed to disperse freely over a local area. In 2002, dispersal of conidia and its influence on the impact of the fungus on the gypsy moth was investigated. Gypsy moth densities and fungus resting spore loads were measured in 15 plots within a 3 km area. In 7 of the plots, prevalence of fungal disease was determined weekly by collecting and rearing gypsy moth larvae. Different strategies were used to disperse conidia within the model, and resulting simulated prevalence rates were compared to actual data. Model output was most accurate when airborne conidia were permitted to disperse equally to all plots. Thus, to accurately assess the impact of the fungus in one location, it is necessary to take into account fungal activity throughout the local area.     

Spatial analysis of harmonic oscillation of gypsy moth outbreak intensity

Outbreaks of many forest-defoliating insects are synchronous over broad geographic areas and occur with a period of approximately 10 years. Within the range of the gypsy moth in North America, however, there is considerable geographic heterogeneity in strength of periodicity and the frequency of outbreaks. Furthermore, gypsy moth outbreaks exhibit two significant periodicities: a dominant period of 8–10 years and a subdominant period of 4–5 years. In this study, we used a simulation model and spatially referenced time series of outbreak intensity data from the Northeastern United States to show that the bimodal periodicity in the intensity of gypsy moth outbreaks is largely a result of harmonic oscillations in gypsy moth abundance at and above a 4 km² scale of resolution. We also used geographically weighted regression models to explore the effects of gypsy moth host-tree abundance on the periodicity of gypsy moths. We found that the strength of 5-year cycles increased relative to the strength of 10-year cycles with increasing host tree abundance. We suggest that this pattern emerges because high host-tree availability enhances the growth rates of gypsy moth populations.     

Comparison of methods for estimating the spread of a non-indigenous species

Aim  To compare different quantitative approaches for estimating rates of spread in the exotic species gypsy moth, Lymantria dispar L., using county-level presence/absence data and spatially extensive trapping grids.
Location  USA
Methods  We used county-level presence/absence records of the gypsy moth's distribution in the USA, which are available beginning in 1900, and extensive grids of pheromone-baited traps, which are available in selected areas beginning in 1981. We compared a regression approach and a boundary displacement approach for estimating gypsy moth spread based on these sources of data.
Results  We observed relative congruence between methods and data sources in estimating overall rates of gypsy moth spread through time, and among regions.
Main conclusions  The ability to estimate spread in exotic invasive species is a primary concern in management programmes and one for which there is a lack of information on the reliability of methods. Also, in most invading species, there is generally a lack of data to explore methods of estimating spread. Extensive data available on gypsy moth in the USA allowed for such a comparison. We show that, even with spatially crude records of presence/absence, overall rates of spread do not differ substantially from estimates obtained from the more costly deployment of extensive trapping grids. Moreover, these methods can also be applied to the general study of species distributional changes, such as range expansion or retraction, in response to climate change or other environmental effects.     

Spatial analysis of gypsy moth populations in Sardinia using geostatistical and climate models

• 1 Spatial fluctuations of the Sardinian population of the gypsy moth Lymantria dispar (L.) (Lepidoptera: Lymantriidae) were characterized using geostatistical and climate models. Data on gypsy moth egg mass abundance recorded at 282 permanent monitoring sites from 1980 to 2004 were incorporated in a geographic information system with the vegetational, geomorphological and pedological features of the sites.
• 2 Statistical analyses revealed that the relative outbreak frequency was related to the predominant host tree, slope and elevation of the monitoring sites, whereas there was no correlation between outbreak frequency and exposure and soil type.
• 3 By using bioclimatic modelling, probability maps of gypsy moth outbreaks were generated. The model identified a probability surface with climatic conditions favourable to gypsy moth outbreaks and thus potentially subject to defoliation. The maps included 92 sites where outbreaks never occurred, suggesting that the Sardinian climate may not be a determinant factor for gypsy moth outbreaks.
• 4 The geostatistical method cokriging with outbreak frequency as a covariate was found to be the most suitable technique to estimate gypsy moth egg mass abundance. Semivariograms showed spatial correlation of egg mass abundance within the range 18.5–53 km. The results obtained were used to create regional gypsy moth distribution maps by cokriging, which demonstrated the outbreak foci and different infestation levels at each monitoring area. These results can help to delimit the treatment areas and develop rational gypsy moth management programmes.

     

Using mechanistic models to understand synchrony in forest insect populations: the North American gypsy moth as a case study

In many forest insects, subpopulations fluctuate concurrently across large geographical areas, a phenomenon known as population synchrony. Because of the large spatial scales involved, empirical tests to identify the causes of synchrony are often impractical. Simple models are, therefore, a useful aid to understanding, but data often seem to contradict model predictions. For instance, chaotic population dynamics and limited dispersal are not uncommon among synchronous forest defoliators, yet both make it difficult to achieve synchrony in simple models. To test whether this discrepancy can be explained by more realistic models, we introduced dispersal and spatially correlated stochasticity into a mechanistic population model for the North American gypsy moth Lymantria dispar. The resulting model shows both chaotic dynamics and spatial synchrony, suggesting that chaos and synchrony can be reconciled by the incorporation of realistic dynamics and spatial structure. By relating alterations in model structure to changes in synchrony levels, we show that the synchrony is due to a combination of spatial covariance in environmental stochasticity and the origins of chaos in our multispecies model.     

Competition between the gypsy moth, Lymantria dispar, and the northern tiger swallowtail, Papilio canadensis: interactions mediated by host plant chemistry, pathogens, and parasitoids

The gypsy moth, Lymantria dispar, and the northern tiger swallowtail, Papilio canadensis, overlap geographically as well as in their host ranges. Adult female swallowtails are incapable of distinguishing between damaged and undamaged leaves, and the opportunities for competition between these two species are numerous. We designed field and laboratory experiments to look for evidence of indirect competition between P. canadensis and L. dispar larvae. Swallowtail caterpillars were reared in the laboratory on leaves from gypsy-moth-defoliated and undefoliated trees to explore host-plant effects. We tested for pathogen-mediated interactions by rearing swallowtail larvae on both sterilized and unsterilized leaves from defoliated and undefoliated sources. In addition, we measured the effects of known gypsy moth pathogens, as well as gypsy moth body fluids, on the growth and survival of swallowtail larvae. Field experiments were designed to detect the presence of parasitoid-mediated competition, as well: we recorded parasitism of swallowtail caterpillars placed in the field either where there were no gypsy moth larvae present, or where we had artificially created dense gypsy moth populations. We found evidence that swallowtails were negatively affected by gypsy moths in several ways: defoliation by gypsy moths depressed swallowtail growth rate and survival, whether leaves were sterilized or not; sterilization significantly reduced the effect of defoliation, and gypsy moth body fluids proved lethal; and swallowtail caterpillars suffered significantly increased rates of parasitism when they were placed in the field near gypsy moth infestations.     

Dispersion in time and space affect mating success and Allee effects in invading gypsy moth populations

1. Understanding why invading populations sometimes fail to establish is of considerable relevance to the development of strategies for managing biological invasions. 2. Newly arriving populations tend to be sparse and are often influenced by Allee effects. Mating failure is a typical cause of Allee effects in low-density insect populations, and dispersion of individuals in space and time can exacerbate mate-location failure in invading populations. 3. Here we evaluate the relative importance of dispersal and sexual asynchrony as contributors to Allee effects in invading populations by adopting as a case study the gypsy moth (Lymantria dispar L.), an important insect defoliator for which considerable demographic information is available. 4. We used release-recapture experiments to parameterize a model that describes probabilities that males locate females along various spatial and temporal offsets between male and female adult emergence. 5. Based on these experimental results, we developed a generalized model of mating success that demonstrates the existence of an Allee threshold, below which introduced gypsy moth populations are likely to go extinct without any management intervention.     

Extensive gypsy moth defoliation in Southern New England characterized using Landsat satellite observations

Southern New England is currently experiencing the first major gypsy moth (Lymantria dispar) defoliation event in nearly 30 years. Using a novel approach based on time series of Landsat satellite observations, we generated consistent maps of gypsy moth defoliation for 2015 (first year of the outbreak), 2016 (second year of outbreak), and 2017 (third year of outbreak). Our mapped results demonstrate that the defoliation event continued through the 2017 growing season. Moreover, the affected area more than doubled in extent each year and expanded radially to encompass 4386 km² of forested area in Rhode Island, eastern Connecticut, and central Massachusetts. The current gypsy moth outbreak is believed to be the result of a series of unusually dry springs in 2014, 2015, and 2016, which suppressed Entomophaga maimaiga, a fungal mortality agent that has historically reduced gypsy moth impacts in this region. The continuation and marked expansion of the outbreak in 2017 despite average spring rainfall suggests that caterpillars were active early in the growing season, and mortality from the fungus likely peaked after significant defoliation had already occurred. Our Landsat time series approach represents an important new source of data on spatial and temporal patterns in gypsy moth defoliation, and continued satellite-based monitoring will be essential for tracking the progress of this and other gypsy moth outbreaks.     

Geographical variation in the spatial synchrony of a forest-defoliating insect: isolation of environmental and spatial drivers

Despite the pervasiveness of spatial synchrony of population fluctuations in virtually every taxon, it remains difficult to disentangle its underlying mechanisms, such as environmental perturbations and dispersal. We used multiple regression of distance matrices (MRMs) to statistically partition the importance of several factors potentially synchronizing the dynamics of the gypsy moth, an invasive species in North America, exhibiting outbreaks that are partially synchronized over long distances (approx. 900 km). The factors considered in the MRM were synchrony in weather conditions, spatial proximity and forest-type similarity. We found that the most likely driver of outbreak synchrony is synchronous precipitation. Proximity played no apparent role in influencing outbreak synchrony after accounting for precipitation, suggesting dispersal does not drive outbreak synchrony. Because a previous modelling study indicated weather might indirectly synchronize outbreaks through synchronization of oak masting and generalist predators that feed upon acorns, we also examined the influence of weather and proximity on synchrony of acorn production. As we found for outbreak synchrony, synchrony in oak masting increased with synchrony in precipitation, though it also increased with proximity. We conclude that precipitation could synchronize gypsy moth populations directly, as in a Moran effect, or indirectly, through effects on oak masting, generalist predators or diseases.     

The role of Allee effects in gypsy moth, <Emphasis Type="Italic">Lymantria dispar</Emphasis> (L.), invasions

Allee effects have been applied historically in efforts to understand the low-density population dynamics of rare and endangered species. Many biological invasions likewise experience the phenomenon of decreasing population growth rates at low population densities because most founding populations of introduced nonnative species occur at low densities. In range expansion of established species, the initial colonizers of habitat beyond the organism’s current range are usually at low density, and thus could be subject to Allee dynamics. There has been consistent empirical and theoretical evidence demonstrating, and in some cases quantifying, the role of Allee dynamics in the gypsy moth, Lymantria dispar (L.), invasion of North America. In this review, we examine the potential causes of the Allee effect in the gypsy moth and highlight the importance of mate-finding failure as a primary mechanism behind an Allee effect, while the degree to which generalist predators induce an Allee effect remains unclear. We then explore the role of Allee effects in the establishment and spread dynamics of the gypsy moth system, which conceptually could serve as a model system for understanding how Allee effects manifest themselves in the dynamics of biological invasions.     

Elevational gradient in the cyclicity of a forest-defoliating insect

Observed changes in the cyclicity of herbivore populations along latitudinal gradients and the hypothesis that shifts in the importance of generalist versus specialist predators explain such gradients has long been a matter of intense interest. In contrast, elevational gradients in population cyclicity are largely unexplored. We quantified the cyclicity of gypsy moth populations along an elevational gradient by applying wavelet analysis to spatially referenced 31-year records (1975–2005) of defoliation. Based on geographically weighted regression and nonlinear regression, we found either a hump-shaped or plateauing relationship between elevation and the cyclicity of gypsy moth populations and a positive relationship between cyclicity and the density of the gypsy moth’s preferred host-tree species. The potential effects of elevational gradients in the density of generalist predators and preferred host-tree species on the cyclicity of gypsy moth populations were evaluated with mechanistic simulation models. The models suggested that an elevational gradient in the densities of preferred host tree species could partially explain elevational patterns of gypsy moth cyclicity. Results from a model assuming a type-III functional response of generalist predators to changes in gypsy moth density were inconsistent with the observed elevational gradient in gypsy moth cyclicity. However, a model with a more realistic type-II functional response gave results roughly consistent with the empirical findings. In contrast to classical studies on the effects of generalist predators on prey population cycles, our model with a type-II functional response predicts a unimodal relationship between generalist-predator density and the cyclicity of gypsy moth populations.     

Influence of Diet and Density on Laboratory Cannibalism Behaviors in Gypsy Moth Larvae (Lymantria dispar L.)

The gypsy moth (Lymantria dispar) is an insect folivore that feeds on a broad range of hosts, and undergoes intermittent outbreaks that cause extensive tree mortality. Like many other herbivorous insects, gypsy moth larvae consume a substrate that is low in nitrogen. Gypsy moth larvae have been known to cannibalize under crowded conditions in the laboratory. In this study, we assessed the influence of nitrogen and density on cannibalism behavior in gypsy moth larvae. Cannibalism rates increased with decreased nitrogen and increased density. There was no interaction between these two parameters. Developmental experiments confirmed that low dietary nitrogen is detrimental, in agreement with previous studies. In a second experiment, we assessed the influence of previous cannibalism experiences on subsequent cannibalism behavior. Gypsy moth larvae that had previously cannibalized other larvae subsequently exhibited higher cannibalism rates than those larvae that had not cannibalized. In conclusion, low nitrogen, high larval density, and previous cannibalism experience are important factors contributing to gypsy moth larval cannibalism. Future studies are needed to estimate benefits to larvae, and to more closely approximate field conditions.     

Host tree influences on the dispersal of first instar gypsy moths, Lymantria dispar (L.)

Abstract. 1. In laboratory tests, first instar gypsy moths attempted dispersal more frequency when exposed to less acceptable foliage.
2. First instars from small eggs attempted dispersal less frequently than larvae from large eggs when exposed to foliage from highly acceptable or marginally acceptable hosts. Dispersal rates of larvae from medium sized eggs were intermediate.
3. These results (1–2) confirm and expand upon the findings of Capinera & Barbosa (1976).
4. In the field, data on the relative densities of larvae on different host species support the conclusion that the frequency of dispersal attempts is inversely related to host acceptability.
5. The implications of these findings for the population dynamics of the gypsy moth are discussed.     

Population cycles produce periodic range boundary pulses

Classical theories of biological invasions predict constant rates of spread that can be estimated from measurable life history parameters, but such outcomes depend strongly on assumptions that are often unmet in nature. Subsequent advances have demonstrated how relaxing assumptions of these foundational models results in other spread patterns seen in nature, including invasions that accelerate through time, or that alternate among periods of expansion, retraction, and stasis of range boundaries. In this paper, we examine how periodic population fluctuations affect temporal patterns of range expansion by coupling empirical data on the gypsy moth invasion in North America with insights from a model incorporating population cycles, Allee effects, and stratified diffusion. In an analysis of field data, we found that gypsy moth spread exhibits pulses with a period of 6 yr, which field data and model simulations suggest is the result of a 6‐yr population cycle in established populations near the invasion front. Model simulations show that the development of periodic behavior in range expansion depends primarily on the period length of population cycles. The period length of invasion pulses corresponded to the population cycle length, and the regularity of invasion pulses tended to decline with increases in population cycle length. A key insight of this research is that dynamics of established populations, behind the invasion front, can have strong effects on spread. Our findings suggest that coordination between separate management programs targeting low‐density spreading and established outbreaking populations, respectively, could increase the efficacy of efforts to mitigate gypsy moth impacts. Given the variety of species experiencing population fluctuations, Allee effects, and stratified diffusion, insights from this study are potentially important to understanding how the range boundaries of many species change.