Identifying the generalizable controls on insect associations of native and non-native trees.

Trees growing outside their native geographic ranges often exhibit exceptional growth and survival due in part to the lack of co-evolved natural enemies that may limit their spread and suppress population growth. While most non-native trees tend to accumulate natural enemies over time, it remains uncertain which host and insect characteristics affect these novel associations and whether novel associations follow patterns of assembly similar to those of native hosts. Here, we used a dataset of insect-host tree associations in Europe to model which native insect species are paired with which native tree species, and then tested the model on its ability to predict which native insects are paired with which non-native trees. We show that native and non-native tree species closely related to known hosts are more likely to be hosts themselves, but that native host geographic range size, insect feeding guild, and sampling effort similarly affect insect associations. Our model had a strong ability to predict which insect species utilize non-native trees as hosts, but evolutionarily isolated tree species posed the greatest challenge to the model. These results demonstrate that insect-host associations can be reliably predicted, regardless of whether insect and host trees have co-evolved, and provide a framework for predicting future pest threats using a select number of easily attainable tree and insect characteristics.

A mechanistic statistical approach to infer invasion characteristics of human-dispersed species with complex life cycle.

The rising introduction of invasive species through trade networks threatens biodiversity and ecosystem services. Yet, we have a limited understanding of how transportation networks determine patterns of range expansion. This is partly because current analytical models fail to integrate the invader's life-history dynamics with heterogeneity in human-mediated dispersal patterns. And partly because classical statistical methods often fail to provide reliable estimates of model parameters due to spatial biases in the presence-only records and lack of informative demographic data. To address these gaps, we first formulate an age-structured metapopulation model that uses a probability matrix to emulate human-mediated dispersal patterns. The model reveals that an invader spreads along the shortest network path, such that the inter-patch network distances decrease with increasing traffic volume and reproductive value of hitchhikers. Next, we propose a Bayesian statistical method to estimate model parameters using presence-only data and prior demographic knowledge. To show the utility of the statistical approach, we analyze zebra mussel (Dreissena polymorpha) expansion in North America through the commercial shipping network. Our analysis underscores the importance of correcting spatial biases and leveraging priors to answer questions, such as where and when the zebra mussels were introduced and what life-history characteristics make these mollusks successful invaders.

Optimal allocation of resources among general and species-specific tools for plant pest biosecurity surveillance.

This paper proposes a surveillance model for plant pests that can optimally allocate resources among survey tools with varying properties. While some survey tools are highly specific for the detection of a single pest species, others are more generalized. There is considerable variation in the cost and sensitivity of these tools, but there are no guidelines or frameworks for identifying which tools are most cost-effective when used in surveillance programs that target the detection of newly invaded populations. To address this gap, we applied our model to design a trapping surveillance program in New Zealand for bark- and wood-boring insects, some of the most serious forest pests worldwide. Our findings show that exclusively utilizing generalized traps (GTs) proves to be highly cost-effective across a wide range of scenarios, particularly when they are capable of capturing all pest species. Implementing surveillance programs that only employ specialized traps (ST) is cost-effective only when these traps can detect highly damaging pests. However, even in such cases, they significantly lag in cost-effectiveness compared to GT-only programs due to their restricted coverage. When both GTs and STs are used in an integrated surveillance program, the total expected cost (TEC) generally diminishes when compared to programs relying on a single type of trap. However, this relative reduction in TEC is only marginally larger than that achieved with GT-only programs, as long as highly damaging species can be detected by GTs. The proportion of STs among the optimal required traps fluctuates based on several factors, including the relative pricing of GTs and STs, pest arrival rates, potential damage, and, more prominently, the coverage capacity of GTs. Our analysis suggests that deploying GTs extensively across landscapes appears to be more cost-effective in areas with either very high or very low levels of relative risk density, potential damage, and arrival rate. Finally, STs are less likely to be required when the pests that are detected by those tools have a higher likelihood of successful eradication because delaying detection becomes less costly for these species.

Variation in Avian Predation Pressure as a Driver for the Diversification of Periodical Cicada Broods.

AbstractPeriodical cicadas live 13 or 17 years underground as nymphs, then emerge in synchrony as adults to reproduce. Developmentally synchronized populations called broods rarely coexist, with one dominant brood locally excluding those that emerge in off years. Twelve modern 17-year cicada broods are believed to have descended from only three ancestral broods following the last glaciation. The mechanisms by which these daughter broods overcame exclusion by the ancestral brood to synchronously emerge in a different year, however, are elusive. Here, we demonstrate that temporal variation in the population density of generalist predators can allow intermittent opportunities for new broods to invade, even though a single brood remains dominant most of the time. We show that this mechanism is consistent, in terms of the type and frequency of brood replacements, with the distribution of periodical cicada broods throughout North America today. Although we investigate one particularly charismatic case study, the mechanisms involved (competitive exclusion, Allee effects, trait variation, predation, and temporal variability) are ubiquitous and could contribute to patterns of species diversity in a range of systems.

The spongy moth, Lymantria dispar.

Rindos and Leibhold introduce the invasive pest, the spongy moth.

Historical plant introductions predict current insect invasions.

Thousands of insect species have been introduced outside of their native ranges, and some of them strongly impact ecosystems and human societies. Because a large fraction of insects feed on or are associated with plants, nonnative plants provide habitat and resources for invading insects, thereby facilitating their establishment. Furthermore, plant imports represent one of the main pathways for accidental nonnative insect introductions. Here, we tested the hypothesis that plant invasions precede and promote insect invasions. We found that geographical variation in current nonnative insect flows was best explained by nonnative plant flows dating back to 1900 rather than by more recent plant flows. Interestingly, nonnative plant flows were a better predictor of insect invasions than potentially confounding socioeconomic variables. Based on the observed time lag between plant and insect invasions, we estimated that the global insect invasion debt consists of 3,442 region-level introductions, representing a potential increase of 35% of insect invasions. This debt was most important in the Afrotropics, the Neotropics, and Indomalaya, where we expect a 10 to 20-fold increase in discoveries of new nonnative insect species. Overall, our results highlight the strong link between plant and insect invasions and show that limiting the spread of nonnative plants might be key to preventing future invasions of both plants and insects.

Periodical Cicada Emergences Affect Masting Behavior of Oaks.

AbstractOaks (Quercus spp.) are masting species exhibiting highly variable and synchronized acorn production. We investigated the hypothesis that periodical cicadas (Magicada spp.), well known to have strong effects on the ecosystems in which they occur, affect acorn production of oaks through their xylem feeding habits as nymphs, the oviposition damage they inflict as adults during emergences, or the nutrient pulse resulting from the decomposition of their bodies following breeding. We found negative effects on acorn production during emergence years and the year following emergences and enhanced acorn production 2 years after emergence. We also found evidence indicating a significant effect of cicada emergences on spatial synchrony of acorn production by trees growing within the range of the same cicada brood compared with different broods. These results demonstrate that periodical cicadas act as a trophic environmental "veto" depressing acorn production during and immediately following emergences, after which the nutrient pulse associated with the cicada's demise enhances oak reproduction.

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.

Optimizing the use of suppression zones for containment of invasive species.

Despite efforts to prevent their establishment, many invasive species continue to spread and threaten food production, human health, and natural biodiversity. Slowing the spread of established species is often a preferred strategy; however, it is also expensive and necessitates treatment over large areas. Therefore, it is critical to examine how to distribute management efforts over space cost-effectively. Here we consider a continuous-space bioeconomic model and we develop a novel algorithm to find the most cost-effective allocation of treatment efforts throughout a landscape. We show that the optimal strategy often comprises eradication in the yet-uninvaded area, and under certain conditions, it also comprises maintaining a "suppression zone," an area between the invaded and the uninvaded areas, where treatment reduces the invading population but without eliminating it. We examine how the optimal strategy depends on the demographic characteristics of the species and reveal general criteria for deciding when a suppression zone is cost effective.

Alien insect dispersal mediated by the global movement of commodities.

Globalization and economic growth are recognized as key drivers of biological invasions. Alien species have become a feature of almost every biological community worldwide, and rates of new introductions continue to rise as the movement of people and goods accelerates. Insects are among the most numerous and problematic alien organisms, and are mainly introduced unintentionally with imported cargo or arriving passengers. However, the processes occurring prior to insect introductions remain poorly understood. We used a unique dataset of 1,902,392 border interception records from inspections at air, land, and maritime ports in Australia, New Zealand, Europe, Japan, USA, and Canada to identify key commodities associated with insect movement through trade and travel. In total, 8939 species were intercepted, and commodity association data were available for 1242 species recorded between 1960 and 2019. We used rarefaction and extrapolation methods to estimate the total species richness and diversity associated with different commodity types. Plant and wood products were the main commodities associated with insect movement across cargo, passenger baggage, and international mail. Furthermore, certain species were mainly associated with specific commodities within these, and other broad categories. More closely related species tended to share similar commodity associations, but this occurred largely at the genus level rather than within orders or families. These similarities within genera can potentially inform pathway management of new alien species. Combining interception records across regions provides a unique window into the unintentional movement of insects, and provides valuable information on establishment risks associated with different commodity types and pathways.

Forest Insect Biosecurity: Processes, Patterns, Predictions, Pitfalls.

The economic and environmental threats posed by non-native forest insects are ever increasing with the continuing globalization of trade and travel; thus, the need for mitigation through effective biosecurity is greater than ever. However, despite decades of research and implementation of preborder, border, and postborder preventative measures, insect invasions continue to occur, with no evidence of saturation, and are even predicted to accelerate. In this article, we review biosecurity measures used to mitigate the arrival, establishment, spread, and impacts of non-native forest insects and possible impediments to the successful implementation of these measures. Biosecurity successes are likely under-recognized because they are difficult to detect and quantify, whereas failures are more evident in the continued establishment of additional non-native species. There are limitations in existing biosecurity systems at global and country scales (for example, inspecting all imports is impossible, no phytosanitary measures are perfect, knownunknowns cannot be regulated against, and noncompliance is an ongoing problem). Biosecurity should be a shared responsibility across countries, governments, stakeholders, and individuals.

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.

Hidden patterns of insect establishment risk revealed from two centuries of alien species discoveries.

Understanding the socioeconomic drivers of biological invasion informs policy development for curtailing future invasions. While early 20th-century plant trade expansions preceded increased establishments of plant pests in Northern America, increased establishments did not follow accelerating imports later that century. To explore this puzzle, we estimate the historical establishment of plant-feeding Hemiptera in Northern America as a function of historical U.S. imports of live plants from seven world regions. Delays between establishment and discovery are modeled using a previously unused proxy for dynamic discovery effort. By recovering the timing of pest arrivals from their historical discoveries, we disentangle the joint establishment-discovery process. We estimate long delays to discovery, which are partially attributable to the low detectability of less economically important insect species. We estimate that many introduced species remain undiscovered, ranging from around one-fifth for Eurasian regions to two-fifths for Central and South America.

Worldwide border interceptions provide a window into human-mediated global insect movement.

As part of national biosecurity programs, cargo imports, passenger baggage, and international mail are inspected at ports of entry to verify compliance with phytosanitary regulations and to intercept potentially damaging nonnative species to prevent their introduction. Detection of organisms during inspections may also provide crucial information about the species composition and relative arrival rates in invasion pathways that can inform the implementation of other biosecurity practices such as quarantines and surveillance. In most regions, insects are the main taxonomic group encountered during inspections. We gathered insect interception data from nine world regions collected from 1995 to 2019 to compare the composition of species arriving at ports in these regions. Collectively, 8,716 insect species were intercepted in these regions over the last 25 yr, with the combined international data set comprising 1,899,573 interception events, of which 863,972 were identified to species level. Rarefaction analysis indicated that interceptions comprise only a small fraction of species present in invasion pathways. Despite differences in inspection methodologies, as well as differences in the composition of import source regions and imported commodities, we found strong positive correlations in species interception frequencies between regions, particularly within the Hemiptera and Thysanoptera. There were also significant differences in species frequencies among insects intercepted in different regions. Nevertheless, integrating interception data among multiple regions would be valuable for estimating invasion risks for insect species with high likelihoods of introduction as well as for identifying rare but potentially damaging species.

Inoculative Releases and Natural Spread of the Fungal Pathogen Entomophaga maimaiga (Entomophthorales: Entomophthoraceae) into U.S. Populations of Gypsy Moth, Lymantria dispar (Lepidoptera: Erebidae).

While emphasis with entomopathogens has often been on inundative releases, we describe here historic widespread inoculative releases of a fungal entomopathogen. Several U.S. states and municipalities conducted inoculative releases of the gypsy moth, Lymantria dispar (L.) (Lepidoptera: Erebidae), pathogen Entomophaga maimaiga Humber, Shimazu et Soper (Entomophthorales: Entomophthoraceae) after 1993, as gypsy moth populations spread into the Midwest and North Carolina. This Japanese pathogen first caused epizootics in northeastern North America in 1989 and methods for its inoculative release were tested and proven to be effective from 1991 to 1993. After 1993, spores in soil or in late instar cadavers were collected during or after epizootics and were released inoculatively into newly established populations of this spreading invasive; the goal was that spores would overwinter and germinate the next spring to infect larvae, thus speeding pathogen spread and hastening the development of epizootics in newly established populations. The fungus was released in gypsy moth populations that were separated from areas where the fungus was already established. In particular, extensive releases by natural resource managers in Wisconsin and Michigan aided the spread of E. maimaiga throughout these states. Where it has become established, this acute pathogen has become the dominant natural enemy and has exerted considerable influence in reducing gypsy moth damage. While this pathogen most likely would have invaded these new regions eventually, releases accelerated the spread of E. maimaiga and helped to reduce impacts of initial outbreaks, while further outbreaks were reduced by the pathogen's subsequent persistence and activity in those areas.

Approaches for estimating benefits and costs of interventions in plant biosecurity across invasion phases.

Nonnative plant pests cause billions of dollars in damages. It is critical to prevent or reduce these losses by intervening at various stages of the invasion process, including pathway risk management (to prevent pest arrival), surveillance and eradication (to counter establishment), and management of established pests (to limit damages). Quantifying benefits and costs of these interventions is important to justify and prioritize investments and to inform biosecurity policy. However, approaches for these estimations differ in (1) the assumed relationship between supply, demand, and prices, and (2) the ability to assess different types of direct and indirect costs at invasion stages, for a given arrival or establishment probability. Here we review economic approaches available to estimate benefits and costs of biosecurity interventions to inform the appropriate selection of approaches. In doing so, we complement previous studies and reviews on estimates of damages from invasive species by considering the influence of economic and methodological assumptions. Cost accounting is suitable for rapid decisions, specific impacts, and simple methodological assumptions but fails to account for feedbacks, such as market adjustments, and may overestimate long-term economic impacts. Partial equilibrium models consider changes in consumer and producer surplus due to pest impacts or interventions and can account for feedbacks in affected sectors but require specialized economic models, comprehensive data sets, and estimates of commodity supply and demand curves. More intensive computable general equilibrium models can account for feedbacks across entire economies, including capital and labor, and linkages among these. The two major considerations in choosing an approach are (1) the goals of the analysis (e.g., consideration of a single pest or intervention with a limited range of impacts vs. multiple interventions, pests or sectors), and (2) the resources available for analysis such as knowledge, budget and time.

Sharp boundary formation and invasion between spatially adjacent periodical cicada broods.

Periodical cicadas, Magicicada spp., are a useful model system for understanding the population processes that influence range boundaries. Unlike most insects, these species typically exist at very high densities (occasionally >1000/ m2) and have unusually long life-spans (13 or 17 years). They spend most of their lives underground feeding on plant roots. After the underground period, adults emerge from the ground to mate and oviposit over a period of just a few days. Collections of populations that are developmentally synchronized across large areas are known as "broods". There are usually sharp boundaries between spatially adjacent broods and regions of brood overlap are generally small. The exact mechanism behind this developmental synchronization and the sharp boundary between broods remain unknown: previous studies have focused on the impacts of predator-driven Allee-effects, competition among nymphs, and their impacts on the persistence of off-synchronized emergence events. Here, we present a nonlinear Leslie-type matrix model to additionally consider cicada movement between spatially separated broods, and examine its role in maintaining brood boundaries and within-brood developmental synchrony that is seen in nature. We successfully identify ranges of competition and dispersal that lead to stable coexistence of broods that differ between spatial patches.

Combining multiple tactics over time for cost-effective eradication of invading insect populations.

Because of the profound ecological and economic impacts of many non-native insect species, early detection and eradication of newly founded, isolated populations is a high priority for preventing damages. Though successful eradication is often challenging, the effectiveness of several treatment methods/tactics is enhanced by the existence of Allee dynamics in target populations. Historically, successful eradication has often relied on the application of two or more tactics. Here, we examine how to combine three treatment tactics in the most cost-effective manner, either simultaneously or sequentially in a multiple-annum process. We show that each tactic is most efficient across a specific range of population densities. Furthermore, we show that certain tactics inhibit the efficiency of other tactics and should therefore not be used simultaneously; but since each tactic is effective at specific densities, different combinations of tactics should be applied sequentially through time when a multiple-annum eradication programme is needed.