Phylogenetic risk assessment is robust for forecasting the impact of European insects on North American conifers.

Some introduced species cause severe damage, although the majority have little impact. Robust predictions of which species are most likely to cause substantial impacts could focus efforts to mitigate those impacts or prevent certain invasions entirely. Introduced herbivorous insects can reduce crop yield, fundamentally alter natural and managed forest ecosystems, and are unique among invasive species in that they require certain host plants to succeed. Recent studies have demonstrated that understanding the evolutionary history of introduced herbivores and their host plants can provide robust predictions of impact. Specifically, divergence times between hosts in the native and introduced ranges of a nonnative insect can be used to predict the potential impact of the insect should it establish in a novel ecosystem. However, divergence time estimates vary among published phylogenetic datasets, making it crucial to understand if and how the choice of phylogeny affects prediction of impact. Here, we tested the robustness of impact prediction to variation in host phylogeny by using insects that feed on conifers and predicting the likelihood of high impact using four different published phylogenies. Our analyses ranked 62 insects that are not established in North America and 47 North American conifer species according to overall risk and vulnerability, respectively. We found that results were robust to the choice of phylogeny. Although published vascular plant phylogenies continue to be refined, our analysis indicates that those differences are not substantial enough to alter the predictions of invader impact. Our results can assist in focusing biosecurity programs for conifer pests and can be more generally applied to nonnative insects and their potential hosts by prioritizing surveillance for those insects most likely to be damaging invaders.

Bacterial and Fungal Symbionts in Pollen Provisions of a Native Solitary Bee in Urban and Rural Environments.

Among insects, symbionts such as bacteria and fungi can be linked to their physiology and immature development, and in some cases are part of a defense system against parasites and diseases. Current bacterial and fungal symbiont associations in solitary bees are understudied, especially in the Pacific Northwest region of the USA. We collected pollen provisions from the native spring-foraging solitary bee, Osmia lignaria Say, across two distinct foraging periods over 2 years at 22 sites along an urban-to-rural gradient in western Washington. We then used next-generation sequencing to identify bacterial and fungi within pollen provisions and assessed the effect of their richness and diversity on O. lignaria larval development success and adult emergence. We detected a significantly positive relationship between bacterial diversity in pollen with O. lignaria larval developmental success, and higher bacterial richness and diversity during the later foraging period. Fungal generic richness and diversity decreased with increasing plant richness. Although neither was associated with O. lignaria developmental success, we did detect Ascosphaera spp. known to be pathogenic to O. lignaria and other bee species. Neither bacterial or fungal richness or diversity was affected by site type when classified as urban or rural. This study provides new information on bacterial and fungal symbionts present in pollen provisions of a native solitary bee when foraging across urban and rural areas of the Pacific Northwest.

Native solitary bee reproductive success depends on early season precipitation and host plant richness.

Spring-emerging bees depend upon the synchronized bloom times of angiosperms that provide pollen and nectar for offspring. The emergence of such bees and bloom times are linked to weather but can be phenologically mismatched, which could limit bee developmental success. However, it remains unclear how such phenologically asynchrony could affect spring-emerging pollinators, and especially for those that forage over a relatively short time period. We examined the relationship between weather and host plant selection on the native spring-foraging solitary bee, Osmia lignaria, across 3 years at urban and rural sites in and around Seattle, Washington, USA. We used community science weather data to test the effects of precipitation, wind, and temperature on O. lignaria oviposition and developmental success. We also collected pollen data over two distinct foraging periods, early and late spring, and used Next-Generation Sequencing to identify plant genera from pollen. Among the weather variables, precipitation during the early foraging period adversely affected larval developmental success and adult bee emergence success, but not oviposition. Using DNA metabarcoding, we observed that increases in the number of plant genera in pollen increased adult emergence in both foraging periods, but not oviposition or larval development. We also observed that foraging bees consistently visited certain genera during each foraging period, especially Acer, Salix, and Rubus. However, pollen collected by O. lignaria over different years varied in the number of total genera visited, highlighting the importance of multi-year studies to ascertain bee foraging preferences and its link to developmental success.

Evolution of Disease Severity and Susceptibility in the Asteraceae to the Powdery Mildew Golovinomyces latisporus: Major Phylogenetic Structure Coupled With Highly Variable Disease Severity at Fine Scales.

Pathogen host range and pathogen severity are dependent on interactions with their hosts and are hypothesized to have evolved as products of a coevolutionary arms race. An understanding of the factors that affect host range and pathogen severity is especially crucial in introduced pathogens that infect evolutionarily naïve hosts and cause substantial damage to ecosystems. Powdery mildews are detrimental pathogens found worldwide in managed and natural systems. Golovinomyces latisporus is a powdery mildew species that is especially damaging to plants within Asteraceae and to plants within the genus Helianthus in particular. In this study, we evaluated 126 species within Asteraceae to measure the role of host plant morphophysiological traits and evolutionary history on susceptibility to G. latisporus and disease severity. We observed phylogenetic signal in both susceptibility and severity within and among major clades of the Asteraceae. In general, there was a major phylogenetic structure of host severity to G. latisporus; however, there was some fine-scale phylogenetic variability. Phylogenetic statistical methods showed that chlorophyll content, biomass, stomatal index, and trichome density were not associated with disease severity, thus providing evidence that phylogenetic structure, rather than observed plant morphophysiological traits, is the most reliable predictor of pathogen severity. This work sheds light on the role that evolutionary history plays in plant susceptibility and severity to disease and underscores the relative unimportance of commonly assessed host plant traits in powdery mildew severity.

Comparison of Pollen Grain Treatments Without Mechanical Fracturation Prior to Protein Quantification.

Protein and amino acids in pollen are important nutritional components for larval development in several insect species, especially in Apoidea. The Bradford assay is a widely used method to measure relative protein content of pollen, which can shed light on pollen quality and consequences to fitness. Prior to using the Bradford assay, protein must be released from pollen grains, often using a mixture of chemical and mechanical fracturation methods. In this study, we tested the efficacy of protein extraction without using mechanical fracturation. We used pollen collected by the solitary bee Osmia lignaria Say to compare two known buffers associated with pollen protein analysis: phosphate-buffered saline and sodium hydroxide, and deionized water, and with different pollen weights from which we quantified protein using the Bradford assay. While all buffers and deionized water were useful in releasing protein from pollen grains collected by O. lignaria, the use of sodium hydroxide resulted in significantly higher protein quantification across all pollen weights. This methodological study can inform future studies of pollen nutrition in pollen-foraging species.

Sequencing Herbarium Specimens of a Common Detrimental Plant Disease (Powdery Mildew).

Powdery mildew (Erysiphaceae) is a detrimental plant disease that occurs on a variety of economically important crops. Powdery mildew consists of over 873 species of fungal pathogens that affect over 10,000 plant species. Genetic identification of powdery mildew is accomplished using the internal transcribed spacer (ITS) and large subunit (LSU) regions of the nuclear ribosomal RNA gene cluster. The ITS and LSU regions of powdery mildews can be useful in ecological, epidemiological, phylogenetic, and taxonomic investigations. However, sequencing these regions is not without its challenges. For example, powdery mildew sequences are often contaminated with plant and/or fungal DNA. Also, there tends to be a limited amount and older specimens' DNA can fragment over time. The success of sequencing powdery mildew often depends on the primers used for running polymerase chain reaction (PCR). The primers need to be broad enough that they match the majority of powdery mildew DNA yet specific enough that they do not align with other organisms. A review of the taxonomy and phylogeny of the powdery mildews is presented with an emphasis on sequencing the ITS + LSU genomic regions. Additionally, we introduce a new nested primer protocol for sequencing powdery mildew herbarium samples that includes six new powdery mildew-specific primers. The new sequencing protocol presented allows specimens up to 130 years old to be sequenced consistently. Sequencing herbarium specimens can be extremely useful for addressing many ecological, epidemiological, phylogenetic, and taxonomic problems in multiple plant pathogenic systems including the powdery mildews.

Biodiversity influences plant productivity through niche-efficiency.

The loss of biodiversity is threatening ecosystem productivity and services worldwide, spurring efforts to quantify its effects on the functioning of natural ecosystems. Previous research has focused on the positive role of biodiversity on resource acquisition (i.e., niche complementarity), but a lack of study on resource utilization efficiency, a link between resource and productivity, has rendered it difficult to quantify the biodiversity-ecosystem functioning relationship. Here we demonstrate that biodiversity loss reduces plant productivity, other things held constant, through theory, empirical evidence, and simulations under gradually relaxed assumptions. We developed a theoretical model named niche-efficiency to integrate niche complementarity and a heretofore-ignored mechanism of diminishing marginal productivity in quantifying the effects of biodiversity loss on plant productivity. Based on niche-efficiency, we created a relative productivity metric and a productivity impact index (PII) to assist in biological conservation and resource management. Relative productivity provides a standardized measure of the influence of biodiversity on individual productivity, and PII is a functionally based taxonomic index to assess individual species' inherent value in maintaining current ecosystem productivity. Empirical evidence from the Alaska boreal forest suggests that every 1% reduction in overall plant diversity could render an average of 0.23% decline in individual tree productivity. Out of the 283 plant species of the region, we found that large woody plants generally have greater PII values than other species. This theoretical model would facilitate the integration of biological conservation in the international campaign against several pressing global issues involving energy use, climate change, and poverty.

Eradication of Invading Insect Populations: From Concepts to Applications.

Eradication is the deliberate elimination of a species from an area. Given that international quarantine measures can never be 100% effective, surveillance for newly arrived populations of nonnative species coupled with their eradication represents an important strategy for excluding potentially damaging insect species. Historically, eradication efforts have not always been successful and have sometimes been met with public opposition. But new developments in our understanding of the dynamics of low-density populations, the availability of highly effective treatment tactics, and bioeconomic analyses of eradication strategies offer new opportunities for developing more effective surveillance and eradication programs. A key component that connects these new developments is the harnessing of Allee effects, which naturally promote localized species extinction. Here we review these developments and suggest how research might enhance eradication strategies.

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.

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.

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.

The effect of male and female age on Lymantria dispar (Lepidoptera: Lymantriidae) fecundity.

Insects that reproduce sexually must locate a suitable mate, and many species have evolved efficient communication mechanisms to find each other. The number of reproductively viable individuals in a population can be an important constraint in the growth of populations. One factor that can affect insect fecundity is the age of mating adults, as fecundity tends to decline with age. Field observations collected annually on Lymantria dispar (L.) from 2001 to 2007 and 2009 consistently revealed a small proportion of egg masses (generally < 10% in each year) in which > 0 but < 5% of eggs were fertilized in an egg mass consisting of approximately 200-500 eggs. In these studies, male age was unknown but female age was fixed at < 24 h, which, according to previous studies on the effect of female L. dispar age on reproductive success, should have been optimal for fertilization. In this article, we analyzed field data (2001-2007 and 2009) to explore patterns in the occurrence of low-fertilized egg masses. We supplemented these data with laboratory experiments that examined the interacting role of male and female age, and multiple male matings. We observed that increases in male and female age reduce the rate of fertilization, which is furthermore reduced, as males mate multiple times as they age. This article highlights the importance of both female and male age at the time of mating in an invading species, with ramifications to low-density populations in this and other sexually reproducing insect species.

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.

Combining tactics to exploit Allee effects for eradication of alien insect populations.

Invasive species increasingly threaten ecosystems, food production, and human welfare worldwide. Hundreds of eradication programs have targeted a wide range of nonnative insect species to mitigate the economic and ecological impacts of biological invasions. Many such programs used multiple tactics to achieve this goal, but interactions between tactics have received little formal consideration, specifically as they interact with Allee dynamics. If a population can be driven below an Allee threshold, extinction becomes more probable because of factors such as the failure to find mates, satiate natural enemies, or successfully exploit food resources, as well as demographic and environmental stochasticity. A key implication of an Allee threshold is that the population can be eradicated without the need and expense of killing the last individuals. Some combinations of control tactics could interact with Allee dynamics to increase the probability of successful eradication. Combinations of tactics can be considered to have synergistic (greater efficiency in achieving extinction from the combination), additive (no improvement over single tactics alone), or antagonistic (reduced efficiency from the combination) effects on Allee dynamics. We highlight examples of combinations of tactics likely to act synergistically, additively, or antagonistically on pest populations. By exploiting the interacting effects of multiple tactics on Allee dynamics, the success and cost-effectiveness of eradication programs can be enhanced.

Advances in understanding and predicting the spread of invading insect populations.

Understanding and predicting the spread of invading insects is a critical challenge in management programs that aim to minimize ecological and economic harm to native ecosystems. Although efforts to quantify spread rates have been well studied over the past several decades, opportunities to improve our ability to estimate rates of spread, and identify the factors, such as habitat suitability and climate, that influence spread, remain. We review emerging sources of data that can be used to delineate distributional boundaries through time and thus serve as a basis for quantifying spread rates. We then address advances in modeling methods that facilitate our understanding of factors that drive invasive insect spread. We conclude by highlighting some remaining challenges in understanding and predicting invasive insect spread, such as the role of climate change and biotic similarity between the native and introduced ranges, particularly as it applies to decision-making in management programs.

Development of Azalea Lace Bug, Stephanitis pyrioides, on Susceptible and Resistant Rhododendron species in Western Washington.

The invasive azalea lace bug, Stephanitis pyrioides (Scott) (Tingidae: Hemiptera), is an important pest of Rhododendron (L.) (Ericales: Ericaceae). Feeding by nymphs and adults removes chlorophyll, reduces rates of photosynthesis and transpiration, and causes leaf stippling, which reduces the aesthetic value of infested plants. Rhododendron spp. are a major component of landscapes in the Pacific Northwest. Previous studies on the seasonality of S. pyrioides in North America are largely from the southeastern United States, which could have limited applicability in the Pacific Northwest. To quantify S. pyrioides seasonality in western Washington, we sampled ~200 leaves from 18 Rhododendron plants 1-2 times per wk from April to October over 2 yr, and microscopically counted the number of eggs, early instars, late instars, and adults. We developed a degree-day model for first generation S. pyrioides, which we used to estimate that S. pyrioides undergoes two full and a partial third generation in western Washington. Our model estimates 5 and 50% early instar occurrence, after hatching from overwintering eggs, at 69 and 171 accumulated degree-days from 1 January, respectively, when using a base threshold of 10.2°, which can be used to optimize the timing of management decisions. We also observed faster development and adult emergence when S. pyrioides nymphs feed on susceptible host plants relative to more resistant host plants, which may influence the timing of management decisions and potentially increase the probability of a full third generation. This research enhances our knowledge of an emerging invasive species in the Pacific Northwest.

Exploiting Allee effects for managing biological invasions.

Biological invasions are a global and increasing threat to the function and diversity of ecosystems. Allee effects (positive density dependence) have been shown to play an important role in the establishment and spread of non-native species. Although Allee effects can be considered a bane in conservation efforts, they can be a benefit in attempts to manage non-native species. Many biological invaders are subject to some form of an Allee effect, whether due to a need to locate mates, cooperatively feed or reproduce or avoid becoming a meal, yet attempts to highlight the specific exploitation of Allee effects in biological invasions are surprisingly unprecedented. In this review, we highlight current strategies that effectively exploit an Allee effect, and propose novel means by which Allee effects can be manipulated to the detriment of biological invaders. We also illustrate how the concept of Allee effects can be integral in risk assessments and in the prioritization of resources allocated to manage non-native species, as some species beset by strong Allee effects could be less successful as invaders. We describe how tactics that strengthen an existing Allee effect or create new ones could be used to manage biological invasions more effectively.

Introduced pathogens follow the invasion front of a spreading alien host.

1. When an invasive species first colonizes an area, there is an interval before any host-specific natural enemies arrive at the new location. Population densities of newly invading species are low, and the spatial and temporal interactions between spreading invasive species and specific natural enemies that follow are poorly understood. 2. We measured infection rates of two introduced host-specific pathogens, the entomophthoralean fungus Entomophaga maimaiga and the baculovirus Lymantria dispar nucleopolyhedrovirus (LdNPV), occurring in spreading populations of an invasive forest defoliator, L. dispar (gypsy moth), in central Wisconsin. 3. Over 3 years, we found that host density was closely associated with the presence and prevalence of both pathogens. The fungal and viral pathogens differed in the sensitivity of their response as E. maimaiga was present in lower-density host population than LdNPV. 4. We examined the relationship between weather conditions and infection prevalence and found that activity of both the fungus and virus was strongly seasonally influenced by temperature and rainfall or temperature alone, respectively. 5. Purposeful releases of pathogens (median distances of study sites from release sites were 65·2 km for E. maimaiga and 25·6 km for LdNPV) were not associated with pathogen prevalence. 6. A generalist fly parasitoid, Compsilura concinnata, also killed L. dispar larvae collected from the study sites, and parasitism was greater when infection by pathogens was lower. 7. Our results demonstrated that although infection levels were low in newly established host populations, host-specific pathogens had already moved into host populations close behind advancing populations of an invasive host; thus, spreading hosts were released from these enemies for only a relatively short time.

Field evaluation of effect of temperature on release of disparlure from a pheromone-baited trapping system used to monitor gypsy moth (Lepidoptera: Lymantriidae).

Traps baited with disparlure, the synthetic form of the gypsy moth, Lymantria dispar (L.) (Lepidoptera: Lymantriidae), sex pheromone are used to detect newly founded populations and estimate population density across the United States. The lures used in trapping devices are exposed to field conditions with varying climates, which can affect the rate of disparlure release. We evaluated the release rate of disparlure from delta traps baited with disparlure string dispenser from 1 to 3 yr across a broad geographic gradient, from northern Minnesota to southern North Carolina. Traps were deployed over approximately 12 wk that coincided with the period of male moth flight and the deployment schedule of traps under gypsy moth management programs. We measured a uniform rate of release across all locations when considered over the accumulation of degree-days; however, due to differences in degree-day accumulation across locations, there were significant differences in release rates over time among locations. The initial lure load seemed to be sufficient regardless of climate, although rapid release of the pheromone in warmer climates could affect trap efficacy in late season. Daily rates of release in colder climates, such as Minnesota and northern Wisconsin, may not be optimal in detection efforts. This work highlights the importance of local temperatures when deploying pheromone-baited traps for monitoring a species across a large and climatically diverse landscape.

Evaluation of Trapping Schemes to Detect Emerald Ash Borer (Coleoptera: Buprestidae).

Management responses to invasive forest insects are facilitated by the use of detection traps ideally baited with species-specific semiochemicals. Emerald ash borer, Agrilus planipennis Fairmaire, is currently invading North American forests, and since its detection in 2002, development of monitoring tools has been a primary research objective. We compared six trapping schemes for A. planipennis over 2 yr at sites in four U.S. states and one Canadian province that represented a range of background A. planipennis densities, canopy coverage, and ash basal area. We also developed a region-wide phenology model. Across all sites and both years, the 10th, 50th, and 90th percentile of adult flight occurred at 428, 587, and 837 accumulated degree-days, respectively, using a base temperature threshold of 10°C and a start date of 1 January. Most trapping schemes captured comparable numbers of beetles with the exception of purple prism traps (USDA APHIS PPQ), which captured significantly fewer adults. Trapping schemes varied in their trap catch across the gradient of ash basal area, although when considering trap catch as a binary response variable, trapping schemes were more likely to detect A. planipennis in areas with a higher ash component. Results could assist managers in optimizing trap selection, placement, and timing of deployment given local weather conditions, forest composition, and A. planipennis density.