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.

Advances in understanding the drivers of population spatial synchrony.

The causes of spatial synchrony in population dynamics are often elusive. We review how recent advances have enhanced understanding of the causes of the spatial synchrony of insect populations and revealed previously underappreciated complexities in patterns of synchrony. We highlight how regional-scale studies of population genetic structure have helped elucidate the role of dispersal in population synchronization and how novel data-analytic approaches have revealed variation in spatial synchrony across timescales and geographies and the underlying drivers. We also stress the limited current understanding of the impacts of climate change on the spatial synchrony of insect populations and the potential ramifications of these effects for pest management as well as species conservation.

Climate affects the outbreaks of a forest defoliator indirectly through its tree hosts.

Although spatial variation in climate can directly affect the survival and reproduction of forest insects and the tree species compositions of forests, little is known about the indirect effects of climate on outbreaks of forest insects through its effects on forest composition. In this study, we use structural equation modeling to examine the direct and indirect effects of climate, water capacity of the soil, host tree density, and non-host density on the spatial extent of Lymantria dispar outbreaks in the Eastern USA over a period of 44 years (1975-2018). Host species were subdivided into four taxonomic and ecologically distinct groups: red oaks (Lobatae), white oaks (Lepidobalanus), other preferred hosts, and intermediate (less preferred) hosts. We found that mean annual temperature had stronger effects than mean annual precipitation on the spatial extent of outbreaks, and that indirect effects of temperature (via its effects on oak density) on defoliation were stronger than direct effects. The density of non-host trees increased with increasing precipitation and, consistent with the 'associational resistance hypothesis', defoliation decreased with increasing density of non-host trees. This study offers quantitative evidence that geographic variation in climate can indirectly affect outbreaks of a forest insect through its effects on tree species composition.

A transdisciplinary research agenda for understanding insect responses to ecological light pollution informed by evolutionary trap theory.

Evolutionary traps are phenomena in which rapid environmental change causes environmental cues that historically guided adaptive behavioral or life-history decisions to become poor predictors of the consequences of such decisions for an organism's fitness. Evolutionary trap theory offers an ideal framework for understanding and mitigating the effects of ecological light pollution (ELP) on insects. We emphasize the utility of an evolutionary trap perspective in demonstrating the importance of an integrated understanding of the sensory, behavioral, evolutionary, and demographic mechanisms underlying insect responses to ELP. We also highlight neglected areas of research where greater focus can help enhance understanding of how ELP affects the persistence, evolutionary trajectory, and population dynamics of insects across space and time.

Interactions between artificial light at night, soil moisture, and plant density affect the growth of a perennial wildflower.

Artificial light at night (ALAN) has been shown to alter aspects of plant growth, but we are not aware of any studies that have examined whether the effects of ALAN on plants depend upon the backdrop of variation in other abiotic factors that plants encounter in field populations. We conducted a field experiment to investigate whether ALAN affects the growth and anti-herbivore defenses of common milkweed, Asclepias syriaca, and whether the effects of ALAN are influenced by plant density or soil moisture content. Artificial light at night, soil moisture, and plant density were manipulated according to a split-plot factorial design. Although increasing soil moisture by watering had no significant effects on latex exudation, attributes of plant growth generally responded positively to watering. The basal stem diameter (BSD) and height of plants were affected by ALAN × soil moisture interactions. For both of these variables, the positive effects of ALAN were greater for plants that were not watered than for plants that were. Basal stem diameter was also affected by an ALAN × plant density interaction, and the positive effect of ALAN on BSD was greater in the low-density treatment than in the high-density treatment. Our results demonstrate that the effects of ALAN on plant growth can be altered by soil moisture and plant density. Consequently, the effects of ALAN on plants in nature may not be consistent with existing frameworks that do not account for critical abiotic variables such as water availability or biotic interactions between plants such as competition.

Population spatial synchrony enhanced by periodicity and low detuning with environmental forcing.

Explaining why fluctuations in abundances of spatially disjunct populations often are correlated through time is a major goal of population ecologists. We address two hypotheses receiving little to no testing in wild populations: (i) that population cycling facilitates synchronization given weak coupling among populations, and (ii) that the ability of periodic external forces to synchronize oscillating populations is a function of the mismatch in timescales (detuning) between the force and the population. Here, we apply new analytical methods to field survey data on gypsy moth outbreaks. We report that at timescales associated with gypsy moth outbreaks, spatial synchrony increased with population periodicity via phase locking. The extent to which synchrony in temperature and precipitation influenced population synchrony was associated with the degree of mismatch in dominant timescales of oscillation. Our study provides new empirical methods and rare empirical evidence that population cycling and low detuning can promote population spatial synchrony.

Invasion in patchy landscapes is affected by dispersal mortality and mate-finding failure.

Range expansions are a function of population growth and dispersal, and nascent populations often must overcome demographic Allee effects (positive density dependence at low population densities) driven by factors such as mate-finding failure. Given the importance of individual movement to mate finding, links between landscape structure and movement may be critical to range expansion; however, landscape effects on other factors including mortality may be equally or more important. In one of the most comprehensive investigations of the interactions of these processes to date, we combined field experiments, simulation modeling, and analysis of empirical spread patterns to investigate how landscape structure affected the spread of the gypsy moth in Virginia and West Virginia. In experiments designed to assess how landscape attributes affect mate finding, we found adult males resisted leaving forest patches and the probability of locating a pheromone source declined more rapidly over distance in non-forest matrix than in forest. We used these findings to develop individual-based simulation models of gypsy moth population dynamics and spread in complex patch-matrix landscapes. The models produced an Allee effect that strengthened with reductions in forested area, but owing more so to dispersal mortality than to effects on mate location. Predicted maximum rates of population spread grew with increases in forest area due to increasing success of long-distance transport events. Evaluations of empirical data showed relationships between spread rates and landscape structure largely consistent with model predictions. We conclude rates of spread were largely driven by long-distance dispersal events, the success of which was influenced primarily by dispersal mortality of larvae in unsuitable matrix, and that landscape effects on mate location played a secondary role. Though influences of landscape structure on mate location appear to be unimportant to the spread of the gypsy moth, we predict they would have stronger effects on more dispersive species.

Experimental tests of light-pollution impacts on nocturnal insect courtship and dispersal.

Though a number of effects of artificial light pollution on behavior and physiology have been described, there is little understanding of their consequences for the growth and distribution of populations. Here, we document impacts of light pollution on aspects of firefly population ecology and underlying mating behaviors. Many firefly species have a unique communication system whereby bioluminescent flashes are used in courtship displays to find and attract mates. We performed a series of manipulative field experiments in which we quantified the effects of adding artificial nighttime lighting on abundances and total flashing activity of fireflies, courtship behaviors and mating between tethered females and free-flying males, and dispersal distances of marked individuals. We show that light pollution reduces flashing activities in a dark-active firefly species (Photuris versicolor) by 69.69 % and courtship behavior and mating success in a twilight-active species (Photinus pyralis). Though courtship behavior and mating success of Photinus pyralis was reduced by light pollution, we found no effects of light pollution on male dispersal in this species. Our findings suggest that light pollution is likely to adversely impact firefly populations, and contribute to wider discussions about the ecological consequences of sensory pollution.

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.

Replacement of a dominant viral pathogen by a fungal pathogen does not alter the collapse of a regional forest insect outbreak.

Natural enemies and environmental factors likely both influence the population cycles of many forest-defoliating insect species. Previous work suggests precipitation influences the spatiotemporal patterns of gypsy moth outbreaks in North America, and it has been hypothesized that precipitation could act indirectly through effects on pathogens. We investigated the potential role of climatic and environmental factors in driving pathogen epizootics and parasitism at 57 sites over an area of ≈72,300 km(2) in four US mid-Atlantic states during the final year (2009) of a gypsy moth outbreak. Prior work has largely reported that the Lymantria dispar nucleopolyhedrovirus (LdNPV) was the principal mortality agent responsible for regional collapses of gypsy moth outbreaks. However, in the gypsy moth outbreak-prone US mid-Atlantic region, the fungal pathogen Entomophaga maimaiga has replaced the virus as the dominant source of mortality in dense host populations. The severity of the gypsy moth population crash, measured as the decline in egg mass densities from 2009 to 2010, tended to increase with the prevalence of E. maimaiga and larval parasitoids, but not LdNPV. A significantly negative spatial association was detected between rates of fungal mortality and parasitism, potentially indicating displacement of parasitoids by E. maimaiga. Fungal, viral, and parasitoid mortality agents differed in their associations with local abiotic and biotic conditions, but precipitation significantly influenced both fungal and viral prevalence. This study provides the first spatially robust evidence of the dominance of E. maimaiga during the collapse of a gypsy moth outbreak and highlights the important role played by microclimatic conditions.

How topography induces reproductive asynchrony and alters gypsy moth invasion dynamics.

Reproductive asynchrony, a temporal mismatch in reproductive maturation between an individual and potential mates, may contribute to mate-finding failure and Allee effects that influence the establishment and spread of invasive species. Variation in elevation is likely to promote variability in maturation times for species with temperature-dependent development, but it is not known how strongly this influences reproductive asynchrony or the population growth of invasive species. We examined whether spatial variation in reproductive asynchrony, due to differences in elevation and local heterogeneity in elevation (hilliness), can explain spatial heterogeneity in the population growth rate of the gypsy moth, Lymantria dispar (L.), along its invasion front in Virginia and West Virginia, USA. We used a spatially explicit model of the effects of reproductive asynchrony on mating success to develop predictions of the influences of elevation and elevational heterogeneity on local population growth rates. Population growth rates declined with increased elevation and more modestly with increased elevational heterogeneity. As in earlier work, we found a positive relationship between the population growth rate and the number of introduced egg masses, indicating a demographic Allee effect. At high elevations and high heterogeneity in elevation, the population growth rate was lowest and the density at which the population tended to replace itself (i.e. the Allee threshold) was highest. An analysis of 22 years of field data also showed decreases in population growth rates with elevation and heterogeneity in elevation that were largely consistent with the model predictions. These results highlight how topographic characteristics can affect reproductive asynchrony and influence mate-finding Allee effects in an invading non-native insect population. Given the dependence of developmental rates on temperature in poikilotherms, topographic effects on reproductive success could potentially be important to the population dynamics of many organisms.

Forest defoliator outbreaks under climate change: effects on the frequency and severity of outbreaks of five pine insect pests.

To identify general patterns in the effects of climate change on the outbreak dynamics of forest-defoliating insect species, we examined a 212-year record (1800-2011) of outbreaks of five pine-defoliating species (Bupalus piniarius, Panolis flammea, Lymantria monacha, Dendrolimus pini, and Diprion pini) in Bavaria, Germany for the evidence of climate-driven changes in the severity, cyclicity, and frequency of outbreaks. We also accounted for historical changes in forestry practices and examined effects of past insecticide use to suppress outbreaks. Analysis of relationships between severity or occurrence of outbreaks and detrended measures of temperature and precipitation revealed a mixture of positive and negative relationships between temperature and outbreak activity. Two moth species (P. flammea and Dendrolimus pini) exhibited lower outbreak activity following years or decades of unusually warm temperatures, whereas a sawfly (Diprion pini), for which voltinism is influenced by temperature, displayed increased outbreak occurrence in years of high summer temperatures. We detected only one apparent effect of precipitation, which showed Dendrolimus pini outbreaks tending to follow drought. Wavelet analysis of outbreak time series suggested climate change may be associated with collapse of L. monacha and Dendrolimus pini outbreak cycles (loss of cyclicity and discontinuation of outbreaks, respectively), but high-frequency cycles for B. piniarius and P. flammea in the late 1900s. Regional outbreak severity was generally not related to past suppression efforts (area treated with insecticides). Recent shifts in forestry practices affecting tree species composition roughly coincided with high-frequency outbreak cycles in B. piniarius and P. flammea but are unlikely to explain the detected relationships between climate and outbreak severity or collapses of outbreak cycles. Our results highlight both individualistic responses of different pine-defoliating species to climate changes and some patterns that are consistent across defoliator species in this and other forest systems, including collapsing of population cycles.

Induced plant defenses, host-pathogen interactions, and forest insect outbreaks.

Cyclic outbreaks of defoliating insects devastate forests, but their causes are poorly understood. Outbreak cycles are often assumed to be driven by density-dependent mortality due to natural enemies, because pathogens and predators cause high mortality and because natural-enemy models reproduce fluctuations in defoliation data. The role of induced defenses is in contrast often dismissed, because toxic effects of defenses are often weak and because induced-defense models explain defoliation data no better than natural-enemy models. Natural-enemy models, however, fail to explain gypsy moth outbreaks in North America, in which outbreaks in forests with a higher percentage of oaks have alternated between severe and mild, whereas outbreaks in forests with a lower percentage of oaks have been uniformly moderate. Here we show that this pattern can be explained by an interaction between induced defenses and a natural enemy. We experimentally induced hydrolyzable-tannin defenses in red oak, to show that induction reduces variability in a gypsy moth's risk of baculovirus infection. Because this effect can modulate outbreak severity and because oaks are the only genus of gypsy moth host tree that can be induced, we extended a natural-enemy model to allow for spatial variability in inducibility. Our model shows alternating outbreaks in forests with a high frequency of oaks, and uniform outbreaks in forests with a low frequency of oaks, matching the data. The complexity of this effect suggests that detecting effects of induced defenses on defoliator cycles requires a combination of experiments and models.

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.

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.

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.

Diffusion models for animals in complex landscapes: incorporating heterogeneity among substrates, individuals and edge behaviours.

1. Animals move commonly through a variety of landscape elements and edges in search of food, mates and other resources. We developed a diffusion model for the movement of an insect herbivore, the planthopper Prokelisia crocea, that inhabits a landscape composed of patches of its host plant, prairie cordgrass Spartina pectinata, embedded in a matrix of mudflat or smooth brome Bromus inermis. 2. We used mark-release-resight experiments to quantify planthopper movements within cordgrass-brome and cordgrass-mudflat arenas. A diffusion model was then fitted that included varying diffusion rates for cordgrass and matrix, edge behaviour in the form of a biased random walk and heterogeneity among planthoppers (sessile vs. mobile). The model parameters were estimated by maximum likelihood using the numerical solution of the diffusion model as a probability density. Akaike's information criterion (AIC) values were used to compare models with different subsets of features. 3. There was clear support for models incorporating edge behaviour and both sessile and mobile insects. The most striking difference between the cordgrass-brome and cordgrass-mudflat experiments involved edge behaviour. Planthoppers crossed the cordgrass-brome edge readily in either direction, but traversed the cordgrass-mudflat edge primarily in one direction (mudflat to cordgrass). Diffusion rates were also significantly higher on mudflat than for cordgrass and brome. 4. The differences in behaviour for cordgrass-brome vs. cordgrass-mudflat edges have implications for the connectivity of cordgrass patches as well as their persistence. Higher dispersal rates are expected between cordgrass patches separated by brome relative to mudflat, but patches surrounded by mudflat appear more likely to persist through time. 5. The experimental design and diffusion models used here could potentially be extended to any organism where mass mark-recapture experiments are feasible, as well as complex natural landscapes.