Assessing drivers of localized invasive spread to inform large-scale management of a highly damaging insect pest.

Studies of biological invasions at the macroscale or across multiple scales can provide important insights for management, particularly when localized information about invasion dynamics or environmental contexts is unavailable. In this study, we performed a macroscale analysis of the roles of invasion drivers on the local scale dynamics of a high-profile pest, Lymantria dispar dispar L., with the purpose of improving the prioritization of vulnerable areas for treatment. Specifically, we assessed the relative effects of various anthropogenic and environmental variables on the establishment rate of 8010 quadrats at a localized scale (5 × 5 km) across the entire L. dispar transition zone (the area encompassing the leading population edge, currently from Minnesota to North Carolina). We calculated the number of years from first detection of L. dispar in a quadrat to the year when probability of establishment of L. dispar was greater than 99% (i.e., waiting time to establishment after first detection). To assess the effects of environmental and anthropogenic variables on each quadrat's waiting time to establishment, we performed linear mixed-effects regression models for the full transition zone and three subregions within the zone. Seasonal temperatures were found to be the primary drivers of local establishment rates. Winter temperatures had the strongest effects, especially in the northern parts of the transition zone. Furthermore, the effects of some factors on waiting times to establishment varied across subregions. Our findings contribute to identifying especially vulnerable areas to further L. dispar spread and informing region-specific criteria by invasion managers for the prioritization of areas for treatment.

Evolutionary genomics of gypsy moth populations sampled along a latitudinal gradient.

The European gypsy moth (Lymantria dispar L.) was first introduced to Massachusetts in 1869 and within 150 years has spread throughout eastern North America. This large-scale invasion across a heterogeneous landscape allows examination of the genetic signatures of adaptation potentially associated with rapid geographical spread. We tested the hypothesis that spatially divergent natural selection has driven observed changes in three developmental traits that were measured in a common garden for 165 adult moths sampled from six populations across a latitudinal gradient covering the entirety of the range. We generated genotype data for 91,468 single nucleotide polymorphisms based on double digest restriction-site associated DNA sequencing and used these data to discover genome-wide associations for each trait, as well as to test for signatures of selection on the discovered architectures. Genetic structure across the introduced range of gypsy moth was low in magnitude (FST  = 0.069), with signatures of bottlenecks and spatial expansion apparent in the rare portion of the allele frequency spectrum. Results from applications of Bayesian sparse linear mixed models were consistent with the presumed polygenic architectures of each trait. Further analyses indicated spatially divergent natural selection acting on larval development time and pupal mass, with the linkage disequilibrium component of this test acting as the main driver of observed patterns. The populations most important for these signals were two range-edge populations established less than 30 generations ago. We discuss the importance of rapid polygenic adaptation to the ability of non-native species to invade novel environments.

Novel insights on population and range edge dynamics using an unparalleled spatiotemporal record of species invasion.

Quantifying the complex spatial dynamics taking place at range edges is critical for understanding future distributions of species, yet very few systems have sufficient data or the spatial resolution to empirically test these dynamics. This paper reviews how data from a large-scale pest management programme have provided important contributions to the fields of population dynamics and invasion biology. The invasion of gypsy moth (Lymantria dispar) is well-documented from its introduction near Boston, Massachusetts USA in 1869 to its current extent of over 900,000 km2 in Eastern North America. Over the past two decades, the USDA Forest Service Slow the Spread (STS) programme for managing the future spread of gypsy moth has produced unrivalled spatiotemporal data across the invasion front. The STS programme annually deploys a grid of 60,000-100,000 pheromone-baited traps, currently extending from Minnesota to North Carolina. The data from this programme have provided the foundation for investigations of complex population dynamics and the ability to examine ecological hypotheses previously untestable outside of theoretical venues, particularly regarding invasive spread and Allee effects. This system provides empirical data on the importance of long-distance dispersal and time-lags on population establishment and spatial spread. Studies showing high rates of spatiotemporal variation of the range edge, from rapid spread to border stasis and even retraction, highlight future opportunities to test mechanisms that influence both invasive and native species ranges. The STS trap data have also created a unique opportunity to study low-density population dynamics and quantify Allee effects with empirical data. Notable contributions include evidence for spatiotemporal variation in Allee effects, demonstrating empirical links between Allee effects and spatial spread, and testing mechanisms of population persistence and growth rates at range edges. There remain several outstanding questions in spatial ecology and population biology that can be tested within this system, such as the scaling of local ecological processes to large-scale dynamics across landscapes. The gypsy moth is an ideal model of how important ecological questions can be answered by thinking more broadly about monitoring data.

Temporal variation in the synchrony of weather and its consequences for spatiotemporal population dynamics.

Over large areas, synchronous fluctuations in population density are often attributed to environmental stochasticity (e.g., weather) shared among local populations. This concept was first advanced by Patrick Moran who showed, based on several assumptions, that long-term population synchrony will equal the synchrony of environmental stochasticity among locations. We examine the consequences of violating one of Moran's assumptions, namely that environmental synchrony is constant through time. We demonstrate that the synchrony of weather conditions from regions across the United States varied considerably from 1895 to 2010. Using a simulation model modified from Moran's original study, we show that temporal variation in environmental synchrony can cause changes in population synchrony, which in turn can temporarily increase or decrease the amplitude of regional-scale population fluctuations. A case study using the gypsy moth (Lymantria dispar) provides empirical support for these predictions. This study provides theoretical and empirical evidence that temporal variation in environmental synchrony can be used to identify factors that synchronize population fluctuations and highlights a previously underappreciated cause of variability in population dynamics.

Long-term shifts in the cyclicity of outbreaks of a forest-defoliating insect.

Recent collapses of population cycles in several species highlight the mutable nature of population behavior as well as the potential role of human-induced environmental change in causing population dynamics to shift. We investigate changes in the cyclicity of gypsy moth (Lymantria dispar) outbreaks by applying wavelet analysis to an 86-year time series of forest defoliation in the northeastern United States. Gypsy moth population dynamics shifted on at least four occasions during the study period (1924-2009); strongly cyclical outbreaks were observed between ca. 1943-1965 and ca. 1978-1996, with noncyclical dynamics in the intervening years. During intervals of cyclical dynamics, harmonic oscillations at cycle lengths of 4-5 and 8-10 years co-occurred. Cross-correlation analyses indicated that the intensity of suppression efforts (area treated by insecticide application) did not significantly reduce the total area of defoliation across the region in subsequent years, and no relationship was found between insecticide use and the cyclicity of outbreaks. A gypsy moth population model incorporating empirically based trophic interactions produced shifting population dynamics similar to that observed in the defoliation data. Gypsy moth cycles were the result of a high-density limit cycle driven by a specialist pathogen. Though a generalist predator did not produce an alternative stable equilibrium, cyclical fluctuations in predator density did generate extended intervals of noncyclical behavior in the gypsy moth population. These results suggest that changes in gypsy moth population behavior are driven by trophic interactions, rather than by changes in climatic conditions frequently implicated in other systems.

Climatic warming disrupts recurrent Alpine insect outbreaks.

Climate change has been identified as a causal factor for diverse ecological changes worldwide. Warming trends over the last couple of decades have coincided with the collapse of long-term population cycles in a broad range of taxa, although causal mechanisms are not well-understood. Larch budmoth (LBM) population dynamics across the European Alps, a classic example of regular outbreaks, inexplicably changed sometime during the 1980s after 1,200 y of nearly uninterrupted periodic outbreak cycles. Herein, analysis of perhaps the most extensive spatiotemporal dataset of population dynamics and reconstructed Alpine-wide LBM defoliation records reveals elevational shifts in LBM outbreak epicenters that coincide with temperature fluctuations over two centuries. A population model supports the hypothesis that temperature-mediated shifting of the optimal elevation for LBM population growth is the mechanism for elevational epicenter changes. Increases in the optimal elevation for population growth over the warming period of the last century to near the distributional limit of host larch likely dampened population cycles, thereby causing the collapse of a millennium-long outbreak cycle. The threshold-like change in LBM outbreak pattern highlights how interacting species with differential response rates to climate change can result in dramatic ecological changes.

Spatiotemporal dynamics of forest insect populations under climate change.

Effects of climate on forest insect populations are complex, often involving drivers that are opposing, nonlinear, and nonadditive. Overall, climate change is driving an increase in outbreaks and range shifts. Links between climate and forest insect dynamics are becoming clearer; however, the underlying mechanisms remain less clear. Climate alters forest insect population dynamics directly through life history, physiology, and voltinism, and indirectly through effects on host trees and natural enemies. Climatic effects on bark beetles, wood-boring insects, and sap-suckers are often indirect, through effects on host-tree susceptibility, whereas climatic effects on defoliators are comparatively more direct. We recommend process-based approaches to global distribution mapping and population models to identify the underlying mechanisms and enable effective management of forest insects.

Allee effects and pulsed invasion by the gypsy moth.

Biological invasions pose considerable threats to the world's ecosystems and cause substantial economic losses. A prime example is the invasion of the gypsy moth in the United States, for which more than $194 million was spent on management and monitoring between 1985 and 2004 alone. The spread of the gypsy moth across eastern North America is, perhaps, the most thoroughly studied biological invasion in the world, providing a unique opportunity to explore spatiotemporal variability in rates of spread. Here we describe evidence for periodic pulsed invasions, defined as regularly punctuated range expansions interspersed among periods of range stasis. We use a theoretical model with parameter values estimated from long-term monitoring data to show how an interaction between strong Allee effects (negative population growth at low densities) and stratified diffusion (most individuals disperse locally, but a few seed new colonies by long-range movement) can explain the invasion pulses. Our results indicate that suppressing population peaks along range borders might greatly slow invasion.

Evaluating the success of treatments that slow spread of an invasive insect pest.

BACKGROUND: Treatments for the suppression and eradication of insect populations undergo substantial testing to ascertain their efficacy and safety, but the generally limited spatial and temporal scope of such studies limit knowledge of how contextual factors encountered in operational contexts shape the relative success of pest management treatments. These contextual factors potentially include ecological characteristics of the treated area, or the timing of treatments relative to pest phenology and weather events. We used an extensive database on over 1000 treatments of nascent populations of Lymantria dispar (L.) (gypsy moth) to examine how place-based and time-varying conditions shape the success of management treatments. RESULTS: We found treatment success to vary across states and years, and to be highest in small treatment blocks that are isolated from other populations. In addition, treatment success tended to be lower in treatment blocks with open forest canopies, possibly owing to challenges of effectively distributing treatments in these areas. CONCLUSIONS: Our findings emphasize the importance of monitoring for early detection of nascent gypsy moth colonies in order to successfully slow the spread of the invasion. Additionally, operations research should address best practices for effectively treating with patchy and open forest canopies. © 2021 Society of Chemical Industry.

Spatial synchrony propagates through a forest food web via consumer-resource interactions.

In many study systems, populations fluctuate synchronously across large regions. Several mechanisms have been advanced to explain this, but their importance in nature is often uncertain. Theoretical studies suggest that spatial synchrony initiated in one species through Moran effects may propagate among trophically linked species, but evidence for this in nature is lacking. By applying the nonparametric spatial correlation function to time series data, we discover that densities of the gypsy moth, the moth's chief predator (the white-footed mouse), and the mouse's winter food source (red oak acorns) fluctuate synchronously over similar distances (approximately1000 km) and with similar levels of synchrony. In addition, we investigate the importance of consumer-resource interactions in propagating synchrony among species using an empirically informed simulation model of interactions between acorns, the white-footed mouse, the gypsy moth, and a viral pathogen of the gypsy moth. Our results reveal that regional stochasticity acting directly on populations of the mouse, moth, or pathogen likely has little effect on levels of the synchrony displayed by these species. In contrast, synchrony in mast seeding can propagate across trophic levels, thus explaining observed levels of synchrony in both white-footed mouse and gypsy moth populations. This work suggests that the transfer of synchrony among trophically linked species may be a major factor causing interspecific synchrony.

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 km(2) 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.

Invasion speed is affected by geographical variation in the strength of Allee effects.

Allee effects can play a critical role in slowing or preventing the establishment of low density founder populations of non-indigenous species. Similarly, the spread of established invaders into new habitats can be influenced by the degree to which small founder populations ahead of the invasion front are suppressed through Allee effects. We develop an approach to use empirical data on the gypsy moth, a non-indigenous invader in North America, to quantify the Allee threshold across geographical regions, and we report that the strength of the Allee effect is subject to spatial and temporal variability. Moreover, we present what is to our knowledge the first empirical evidence that geographical regions with higher Allee thresholds are associated with slower speeds of invasion.

Closing the gaps for animal seed dispersal: Separating the effects of habitat loss on dispersal distances and seed aggregation.

Habitat loss can alter animal movements and disrupt animal seed dispersal mutualisms; however, its effects on spatial patterns of seed dispersal are not well understood. To explore the effects of habitat loss on seed dispersal distances and seed dispersion (aggregation), we created a spatially explicit, individual-based model of an animal dispersing seeds (SEADS-Spatially Explicit Animal Dispersal of Seeds) in a theoretical landscape of 0%-90% habitat loss based on three animal traits: movement distance, gut retention time, and time between movements. Our model design had three objectives: to determine the effects of (1) animal traits and (2) habitat loss on seed dispersal distances and dispersion and (3) determine how animal traits could mitigate the negative effects of habitat loss on these variables. SEADS results revealed a complex interaction involving all animal traits and habitat loss on dispersal distances and dispersion, driven by a novel underlying mechanism of fragment entrapment. Unexpectedly, intermediate habitat loss could increase dispersal distances and dispersion relative to low and high habitat loss for some combinations of animal traits. At intermediate habitat loss, movement between patches was common, and increased dispersal distances and dispersion compared to continuous habitats because animals did not stop in spaces between fragments. However, movement between patches was reduced at higher habitat loss as animals became trapped in fragments, often near the parent plant, and dispersed seeds in aggregated patterns. As movement distance increased, low time between movements and high gut retention time combinations permitted more movement to adjacent patches than other combinations of animal traits. Because habitat loss affects movement in a nonlinear fashion under some conditions, future empirical tests would benefit from comparisons across landscapes with more than two levels of fragmentation.

Performance of Wild and Laboratory-Reared Gypsy Moth (Lepidoptera: Erebidae): A Comparison between Foliage and Artificial Diet.

The effects of long-term mass rearing of laboratory insects on ecologically relevant traits is an important consideration when applying research conclusions to wild populations or developing management strategies. Laboratory strains of the gypsy moth, Lymantria dispar (L.), an invasive forest pest in North America, have been continuously reared since 1967. Selection on these strains has enhanced a variety of traits, resulting in faster development, shorter diapause, and greater fecundity. As in many mass-reared insects, laboratory strains of the gypsy moth are also reared exclusively on artificial diets that lack much of the phytochemical and nutritional complexity associated with natural foliage. We tested for differences in growth and development of wild gypsy moth populations from across the invasive range in comparison to laboratory strains when reared on artificial diet and a preferred foliage host species, northern red oak (Quercus rubra L.). Overall, caterpillars reared on foliage had higher survival and faster development rates, with smaller differences among populations. When reared on artificial diet, laboratory strains had the highest performance as expected. The response from the wild populations was mixed, with two populations performing poorly on artificial diet and another performing nearly as well as the laboratory strains. Performance on diet was enhanced when larvae received cubed portions changed regularly, as opposed to filled cups. Understanding these relationships between food source and population performance is important for informing studies that examine population comparisons using wild and laboratory-reared strains.

Dynamics of discrete-time larch budmoth population models.

The larch budmoth (LBM) population in the Swiss Alps is well known for its periodic outbreaks and regular oscillations over several centuries. The ecological mechanisms that drive these oscillations, however, have not been unambiguously identified, although a number of hypotheses have been proposed. In this article, we investigate several LBM resulting from these different ecological hypotheses. We first study a leaf quality-moth population model and then two moth-parasitoid models. Existence and stability of equilibria are investigated and sufficient conditions for which populations can persist are derived. We then provide conclusions based on our analysis.

Landscape mosaic induces traveling waves of insect outbreaks.

The effect of landscape mosaic on recurrent traveling waves in spatial population dynamics was studied via simulation modeling across a theoretical landscape with varying levels of connectivity. Phase angle analysis was used to identify locations of wave epicenters on patchy landscapes. Simulations of a tri-trophic model of the larch budmoth (Zeiraphera diniana) with cyclic population dynamics on landscapes with a single focus of high-density habitat produced traveling waves generally radiating outwardly from single and multiple foci and spreading to isolated habitats. We have proposed two hypotheses for this result: (1) immigration subsidies inflate population growth rates in the high connectivity habitat and, thus, reduce the time from valleys to peaks in population cycles; (2) populations in the high connectivity habitat crash from peaks to valleys faster than in an isolated habitat due to over-compensatory density dependence. While population growth rates in the high connectivity habitat benefitted from immigration subsidies, times from population valleys to peaks were greater in high connectivity habitat due to a greater magnitude of fluctuations. Conversely, the mean time of the crash from population peaks to valleys was shorter in high connectivity habitat, supporting the second hypothesis. Results of this study suggest over-compensatory density dependence as an underlying mechanism for recurrent traveling waves originating in high connectivity habitats aggregated around a single focus.