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.

Pathways for accidental biocontrol: The human-mediated dispersal of insect predators and parasitoids.

Introductions of insect predators and parasitoids for biological control are a key method for pest management. Yet in recent decades, biological control has become more strictly regulated and less frequent. Conversely, the rate of unintentional insect introductions through human activities is rising. While accidental introductions of insect natural enemies can potentially have serious ecological consequences, they are challenging to quantify as their movements go largely unobserved. We used historical border interception records collected by the US Department of Agriculture from 1913 to 2018 to describe the diversity of entomophagous insects transported unintentionally, their main introduction pathways, and trends in host specificity. There were 35,312 interceptions of insect predators and parasitoids during this period, representing 93 families from 11 orders, and 196 species from these families. Commodity associations varied, but imported plants and plant products were the main introduction pathway. Most interceptions originated with commodities imported from the Neotropical, Panamaian, and Western Palearctic regions. Among the intercepted species, 27% were found in material originating from more than one country. Two thirds of species were polyphagous host generalists. Furthermore, 25% of species had already been introduced intentionally as biological control agents internationally, and 4.6% have documented negative impacts on native biodiversity or human society. Most of the intercepted species that have not established in the United States are host generalists or have at least one known host species available. The unintentional transport of diverse natural enemy insects has the potential to cause substantial ecological impacts, both in terms of controlling pests through accidental biocontrol and disrupting native communities. Characterizing the insects being transported and their introduction pathways can inform biosecurity practices and management.

Invasiveness is linked to greater commercial success in the global pet trade.

The pet trade has become a multibillion-dollar global business, with tens of millions of animals traded annually. Pets are sometimes released by their owners or escape, and can become introduced outside of their native range, threatening biodiversity, agriculture, and health. So far, a comprehensive analysis of invasive species traded as pets is lacking. Here, using a unique dataset of 7,522 traded vertebrate species, we show that invasive species are strongly overrepresented in trade across mammals, birds, reptiles, amphibians, and fish. However, it is unclear whether this occurs because, over time, pet species had more opportunities to become invasive, or because invasive species have a greater commercial success. To test this, we focused on the emergent pet trade in ants, which is too recent to be responsible for any invasions so far. Nevertheless, invasive ants were similarly overrepresented, demonstrating that the pet trade specifically favors invasive species. We show that ant species with the greatest commercial success tend to have larger spatial distributions and more generalist habitat requirements, both of which are also associated with invasiveness. Our findings call for an increased risk awareness regarding the international trade of wildlife species as pets.

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.

Reliability of social media data in monitoring the global pet trade in ants.

The global pet trade is a major risk to biodiversity and humans and has become increasingly globalized, diversified, digitalized, and extremely difficult to control. With billions of internet users posting online daily, social media could be a powerful surveillance tool. But it is unknown how reliably social media can track the global pet trade. We tested whether Instagram data predicted the geographic distribution of pet stores and the taxonomic composition of traded species in the emerging pet trade in ants (Hymenoptera, Formicidae). We visited 138 online stores selling ants as pets worldwide and recorded the species traded. We scraped ∼38,000 Instagram posts from ∼6300 users referencing ants as pets and analyzed comments on post and geolocation (available for ∼1800 users). We tested whether the number of Instagram users predicted the number of ant sellers per country and whether the species referenced as pets on Instagram matched the species offered in online stores, with a particular focus on invasive species. The location of Instagram users referencing ants as pets predicted the location of ant sellers across the globe (R2  = 0.87). Instagram data detected 439 of the 631 ant species traded in online stores (70%), including 59 of the 68 invasive species traded (87%). The number of Instagram users referencing a species was a good predictor of the number of sellers offering the species (R2  = 0.77). Overall, Instagram data provided affordable and reliable data for monitoring the emerging pet trade in ants. Easier access to these data would facilitate monitoring of the global pet trade and help implement relevant regulations in a timely manner.

El mercado global de mascotas es una amenaza importante para la biodiversidad y los humanos y cada vez está más globalizado, diversificado, digitalizado y muy difícil de controlar. Con miles de millones de usuarios publicando a diario en línea, las redes sociales podrían ser una herramienta poderosa de vigilancia, aunque no se sabe cuán confiable puede ser su rastreo del mercado global de mascotas. Analizamos si los datos de Instagram pronosticaban la distribución geográfica de las tiendas de mascotas y la composición taxonómica de las especies comercializadas en el mercado emergente de hormigas mascotas (Hymenoptera, Formicidae). Visitamos 138 tiendas virtuales dedicadas al comercio de hormigas como mascotas a nivel mundial y registramos las especies comercializadas. Reunimos ∼38,000 publicaciones de Instagram de ∼6,300 usuarios que mencionaban a las hormigas como mascotas y analizamos los comentarios en las publicaciones y la geolocalización (disponible para ∼1,800 usuarios). Analizamos si el número de usuarios de Instagram pronosticaba el número de vendedores de hormigas por país y si las especies mencionadas como mascotas en Instagram eran las mismas que aquellas ofrecidas en las tiendas en línea, con foco particular sobre las especies invasoras. La ubicación de los usuarios de Instagram que mencionaban a las hormigas como mascotas pronosticó la ubicación de los vendedores de hormigas alrededor del mundo (R2 = 0.87). La información de Instagram detectó 439 de las 631 especies de hormigas comercializadas en las tiendas virtuales (70%), incluidas 59 de las 68 especies invasoras comercializadas (87%). El número de usuarios de Instagram que mencionaba a una especie fue un buen indicador del número de vendedores que ofrecían esa eespecie (R2 = 0.77). En general, la información de Instagram proporcionó datos accesibles y confiables para el monitoreo del mercado emergente de hormigas mascotas. Un acceso más sencillo a estos datos facilitaría el monitoreo del mercado global de mascotas y ayudaría a implementar regulaciones relevantes de manera oportuna.

Insect and plant invasions follow two waves of globalisation.

Globalisation has facilitated the spread of alien species, and some of them have significant impacts on biodiversity and human societies. It is commonly thought that biological invasions have accelerated continuously over the last centuries, following increasing global trade. However, the world experienced two distinct waves of globalisation (~1820-1914, 1960-present), and it remains unclear whether these two waves have influenced invasion dynamics of many species. To test this, we built a statistical model that accounted for temporal variations in sampling effort. We found that insect and plant invasion rates did not continuously increase over the past centuries but greatly fluctuated following the two globalisation waves. Our findings challenge the idea of a continuous acceleration of alien species introductions and highlight the association between temporal variations in trade openness and biological invasion dynamics. More generally, this emphasises the urgency of better understanding the subtleties of socio-economic drivers to improve predictions of future invasions.

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.

Increased acclimation ability accompanies a thermal niche shift of a recent invasion.

Globalization is removing dispersal barriers for the establishment of invasive species and enabling their spread to novel climates. New thermal environments in the invaded range will be particularly challenging for ectotherms, as their metabolism directly depends on environmental temperature. However, we know little about the role climatic niche shifts play in the invasion process, and the underlining physiological mechanisms. We tested if a thermal niche shift accompanies an invasion, and if native and introduced populations differ in their ability to acclimate thermal limits. We used an alien ant species-Tapinoma magnum-which recently started to spread across Europe. Using occurrence data and accompanying climatic variables, we measured the amount of overlap between thermal niches in the native and invaded range. We then experimentally tested the acclimation ability in native and introduced populations by incubating T. magnum at 18, 25 and 30°C. We measured upper and lower critical thermal limits after 7 and 21 days. We found that T. magnum occupies a distinct thermal niche in its introduced range, which is on average 3.5°C colder than its native range. Critical thermal minimum did not differ between populations from the two ranges when colonies were maintained at 25 or 30°C, but did differ after colony acclimation at a lower temperature. We found twofold greater acclimation ability of introduced populations to lower temperatures, after prolonged incubation at 18°C. Increased acclimation ability of lower thermal limits could explain the expansion of the realized thermal niche in the invaded range, and likely contributed to the spread of this species to cooler climates. Such thermal plasticity could be an important, yet so far understudied, factor underlying the expansion of invasive insects into novel climates.

Recurrent bridgehead effects accelerate global alien ant spread.

Biological invasions are a major threat to biological diversity, agriculture, and human health. To predict and prevent new invasions, it is crucial to develop a better understanding of the drivers of the invasion process. The analysis of 4,533 border interception events revealed that at least 51 different alien ant species were intercepted at US ports over a period of 70 years (1914-1984), and 45 alien species were intercepted entering New Zealand over a period of 68 years (1955-2013). Most of the interceptions did not originate from species' native ranges but instead came from invaded areas. In the United States, 75.7% of the interceptions came from a country where the intercepted ant species had been previously introduced. In New Zealand, this value was even higher, at 87.8%. There was an overrepresentation of interceptions from nearby locations (Latin America for species intercepted in the United States and Oceania for species intercepted in New Zealand). The probability of a species' successful establishment in both the United States and New Zealand was positively related to the number of interceptions of the species in these countries. Moreover, species that have spread to more continents are also more likely to be intercepted and to make secondary introductions. This creates a positive feedback loop between the introduction and establishment stages of the invasion process, in which initial establishments promote secondary introductions. Overall, these results reveal that secondary introductions act as a critical driver of increasing global rates of invasions.

How complex should models be? Comparing correlative and mechanistic range dynamics models.

Criticism has been levelled at climate-change-induced forecasts of species range shifts that do not account explicitly for complex population dynamics. The relative importance of such dynamics under climate change is, however, undetermined because direct tests comparing the performance of demographic models vs. simpler ecological niche models are still lacking owing to difficulties in evaluating forecasts using real-world data. We provide the first comparison of the skill of coupled ecological-niche-population models and ecological niche models in predicting documented shifts in the ranges of 20 British breeding bird species across a 40-year period. Forecasts from models calibrated with data centred on 1970 were evaluated using data centred on 2010. We found that more complex coupled ecological-niche-population models (that account for dispersal and metapopulation dynamics) tend to have higher predictive accuracy in forecasting species range shifts than structurally simpler models that only account for variation in climate. However, these better forecasts are achieved only if ecological responses to climate change are simulated without static snapshots of historic land use, taken at a single point in time. In contrast, including both static land use and dynamic climate variables in simpler ecological niche models improve forecasts of observed range shifts. Despite being less skilful at predicting range changes at the grid-cell level, ecological niche models do as well, or better, than more complex models at predicting the magnitude of relative change in range size. Therefore, ecological niche models can provide a reasonable first approximation of the magnitude of species' potential range shifts, especially when more detailed data are lacking on dispersal dynamics, demographic processes underpinning population performance, and change in land cover.

Insects in temperate urban parks face stronger selection pressure from the cold than the heat.

Urban areas experience higher temperatures compared to rural areas and as such, are increasingly considered places of acclimatization and adaptation to warming. Small ectotherms, such as insects, whose body temperature rises with habitat temperature, are directly affected by temperature changes. Thus, warming could have a profound effect on insect behavior and physiology. To test if the urban heat island effect drives higher thermal tolerance and activity changes, we used globally distributed and abundant insects-ants. We measured the heat and cold tolerance of 14 ant species distributed across urban and peri-urban areas. As thermal traits are often correlated with ant foraging, we measured foraging activity during three consecutive years across eight sites. Contrary to our prediction, ants exposed to the urban heat island effect did not have a higher heat tolerance than peri-urban ants. Instead, cold tolerance varied across habitats, with ants from the cooler, peri-urban habitats being able to tolerate lower temperatures. We recorded the same pattern of invariant heat and higher cold tolerance for ants in the canopy, compared to ground nesting ants. Ant activity was almost 10 times higher in urban sites and best predicted by cold, not heat tolerance. These unexpected results suggest that we need to rethink predictions about urban heat islands increasing insect heat tolerance in urban habitats, as cold tolerance might be a more plastic or adaptable trait, particularly in the temperate zone.

Non-native ants are breaking down biogeographic boundaries and homogenizing community assemblages.

As geographic distance increases, species assemblages become more distinct, defining global biogeographic realms with abrupt biogeographic boundaries. Yet, it remains largely unknown to what extent these realms may change because of human-mediated dispersal of species. Focusing on the distributions of 309 non-native ant species, we show that historical biogeographic patterns have already broken down into tropical versus non-tropical regions. Importantly, we demonstrate that these profound changes are not limited to the distribution patterns of non-native ants but fundamentally alter biogeographic boundaries of all ant biodiversity (13,774 species). In total, 52% of ant assemblages have become more similar, supporting a global trend of biotic homogenization. Strikingly, this trend was strongest on islands and in the tropics, which harbor some of the most vulnerable ecosystems. Overall, we show that the pervasive anthropogenic impacts on biodiversity override biogeographic patterns resulting from millions of years of evolution, and disproportionally affect particular regions.

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.

Increase in quantity and quality of suitable areas for invasive species as climate changes.

As climatically suitable range projections become increasingly used to assess distributions of species, we recommend systematic assessments of the quality of habitat in addition to the classical binary classification of habitat. We devised a method to assess occurrence probability, captured by a climatic suitability index, through which we could determine variations in the quality of potential habitat. This relative risk assessment circumvents the use of an arbitrary suitability threshold. We illustrated our method with 2 case studies on invasive ant species. We estimated invasion potential of the destroyer ant (Monomorium destructor) and the European fire ant (Myrmica rubra) on a global scale currently and by 2080 with climate change. We found that 21.1% of the world's landmass currently has a suitable climate for the destroyer ant and 16% has a suitable climate for European fire ant. Our climatic suitability index showed that both ant species would benefit from climate change, but in different ways. The size of the potential distribution increased by 35.8% for the destroyer ant. Meanwhile, the total area of potential distribution remained the same for the European fire ant (>0.05%), but the level of climatic suitability within this range increased greatly and led to an improvement in habitat quality (i.e., of invasive species' establishment likelihood). Either through quantity or quality of suitable areas, both invasive ant species are likely to increase the extent of their invasion in the future, following global climate change. Our results show that species may increase their range if either more areas become suitable or if the available areas present improved suitability. Studies in which an arbitrary suitability threshold was used may overlook changes in area quality within climatically suitable areas and as a result reach incorrect predictions. Incremento de la Cantidad y Calidad de Áreas Idóneas para Especies Invasoras a Medida que Cambia el Clima.

Biological invasions: The secret domination of alien ants.

Globalization has contributed to the spread of thousands of species, yet only a few harmful ones have attracted most attention. New evidence shows that introduced ants are a particularly important group of global invaders that can dominate native insect communities.

The global risk of infectious disease emergence from giant land snail invasion and pet trade.

BACKGROUND: Pathogen outbreaks mostly originate from animals, but some species are more likely to trigger epidemics. The giant land snail (Lissachatina fulica) is a widespread invader, a popular exotic pet, and a notorious vector of the rat lungworm, causing eosinophilic meningitis in humans. However, a comprehensive assessment of the risks of disease outbreak associated with this species is lacking. METHODS: We assessed and mapped the risk of disease transmission associated with the invasion and pet trade of L. fulica. First, we conducted a review of the scientific literature to list all known L. fulica parasites and pathogens and query host-pathogen databases to identify their potential mammalian hosts. Then, to assess the potential for L. fulica to spread globally, we modelled its suitable climatic conditions and tested whether, within climatically suitable areas, the species tended to occur near humans or not. Finally, we used social media data to map L. fulica possession as an exotic pet and to identify human behaviours associated with increased risk of disease transmission. RESULTS: Lissachatina fulica can carry at least 36 pathogen species, including two-thirds that can infect humans. The global invasion of L. fulica is climatically limited to tropical areas, but the species is strongly associated with densely populated areas where snails are more likely to enter in contact with humans. In temperate countries, however, climatic conditions should prevent L. fulica's spread. However, we show that in Europe, giant snails are popular exotic pets and are often handled with direct skin contact, likely increasing the risk of pathogen transmission to their owners. CONCLUSIONS: It is urgent to raise public awareness of the health risks associated with L. fulica in both tropical countries and Europe and to regulate its trade and ownership internationally. Our results highlight the importance of accounting for multiple types of human-wildlife interactions when assessing risks of infectious disease emergence. Furthermore, by targeting the species most likely to spread pathogens, we show that it is possible to rapidly identify emerging disease risks on a global scale, thus guiding timely and appropriate responses.

Impacts of climate change on the future of biodiversity.

Many studies in recent years have investigated the effects of climate change on the future of biodiversity. In this review, we first examine the different possible effects of climate change that can operate at individual, population, species, community, ecosystem and biome scales, notably showing that species can respond to climate change challenges by shifting their climatic niche along three non-exclusive axes: time (e.g. phenology), space (e.g. range) and self (e.g. physiology). Then, we present the principal specificities and caveats of the most common approaches used to estimate future biodiversity at global and sub-continental scales and we synthesise their results. Finally, we highlight several challenges for future research both in theoretical and applied realms. Overall, our review shows that current estimates are very variable, depending on the method, taxonomic group, biodiversity loss metrics, spatial scales and time periods considered. Yet, the majority of models indicate alarming consequences for biodiversity, with the worst-case scenarios leading to extinction rates that would qualify as the sixth mass extinction in the history of the earth.

Globalization and the anthropogenic spread of invasive social insects.

Social insects are among the worst invasive species and a better understanding of their anthropogenic spread is needed. I highlight recent research demonstrating that social insects have been dispersed since the early beginnings of globalized trade and in particular after the Industrial Revolution, following two waves of globalization. Many species have complex invasion histories, with multiple independent introduction events and frequent secondary spread. The major source and recipient regions differ markedly across ants, wasps, termites and bees, probably linked to their different introduction pathways. At a more local scale, anthropogenic factors such as irrigation, urbanization or the presence of railways facilitate invasions. In the future, social insect invasions could further accelerate due to intensifying global trade and novel introduction pathways.

Climatic niche shifts in introduced species.

Predictions of future biological invasions often rely on the assumption that introduced species establish only under climatic conditions similar to those in their native range. To date, 135 studies have tested this assumption of 'niche conservatism', yielding contradictory results. Here we revisit this literature, consider the evidence for niche shifts, critically assess the methods used, and discuss the authors' interpretations of niche shifts. We find that the true frequency of niche shifts remains unknown because of diverging interpretations of similar metrics, conceptual issues biasing conclusions towards niche conservatism, and the use of climatic data that may not be biologically meaningful. We argue that these issues could be largely addressed by focussing on trends or relative degrees of niche change instead of dichotomous classifications (shift versus no shift), consistently and transparently including non-analogous climates, and conducting experimental studies on mismatches between macroclimates and microclimates experienced by the study organism. Furthermore, an observed niche shift may result either from species filling a greater part of their fundamental niche during the invasion (a 'realised niche shift') or from rapid evolution of traits adapting species to novel climates in the introduced range (a 'fundamental niche shift'). Currently, there is no conclusive evidence distinguishing between these potential mechanisms of niche shifts. We outline how these questions may be addressed by combining computational analyses and experimental evidence.