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.

When insect pests build their own thermal niche: The hot nest of the pine processionary moth.

Temperature strongly drives physiological and ecological processes in ectotherms. While many species rely on behavioural thermoregulation to avoid thermal extremes, others build structures (nests) that confer a shelter against climate variability and extremes. However, the microclimate inside nests remains unknown for most insects. We investigated the thermal environment inside the nest of a temperate winter-developing insect species, the pine processionary moth (PPM), Thaumetopoea pityocampa. Gregarious larvae collectively build a silken nest at the beginning of the cold season. We tested the hypothesis that it provides a warmer microenvironment to larvae. First, we monitored temperature inside different types of nests varying in the number of larvae inside. Overall, nest temperature was positively correlated to global radiation and air temperature. At noon, when global radiation was maximal, nest temperature exceeded air temperature by up to 11.2-16.5 °C depending on nest type. In addition, thermal gradients of amplitude from 6.85 to 15.5 °C were observed within nests, the upper part being the warmest. Second, we developed a biophysical model to predict temperature inside PPM nests based on heat transfer equations and to explain this important temperature excess. A simple model version accurately predicted experimental measurements, confirming that nest temperature is driven mainly by radiation load. Finally, the model showed that nest temperature increases at the same rate as air temperature change. We conclude that some pest insects already live in warm microclimates by building their own sheltering nest. This effect should be considered when studying the impact of climate change on phenology and distribution.

Modelling for risk and biosecurity related to forest health.

Modelling the invasion and emergence of forest pests and pathogens (PnPs) is necessary to quantify the risk levels for forest health and provide key information for policy makers. Here, we make a short review of the models used to quantify the invasion risk of exotic species and the emergence risk of native species. Regarding the invasion process, models tackle each invasion phase, e.g. pathway models to describe the risk of entry, species distribution models to describe potential establishment, and dispersal models to describe (human-assisted) spread. Concerning the emergence process, models tackle each process: spread or outbreak. Only a few spread models describe jointly dispersal, growth, and establishment capabilities of native species while some mechanistic models describe the population temporal dynamics and inference models describe the probability of outbreak. We also discuss the ways to quantify uncertainty and the role of machine learning. Overall, promising directions are to increase the models' genericity by parameterization based on meta-analysis techniques to combine the effect of species traits and various environmental drivers. Further perspectives consist in considering the models' interconnection, including the assessment of the economic impact and risk mitigation options, as well as the possibility of having multi-risks and the reduction in uncertainty by collecting larger fit-for-purpose datasets.

Altitudinal Barrier to the Spread of an Invasive Species: Could the Pyrenean Chain Slow the Natural Spread of the Pinewood Nematode?

Mountain ranges may delimit the distribution of native species as well as constitute potential barriers to the spread of invasive species. The invasive pinewood nematode, Bursaphelenchus xylophilus, is a severe forest pest inducing pine wilt disease. It is vectored in Europe by a native long-horned beetle, Monochamus galloprovincialis. This study explored the potential of the Pyrenean chain to slow or prevent the natural spread of nematode-infested beetles from the Iberian Peninsula, where the nematode is established and is expanding its range, towards France and the rest of Europe. An analysis of the genetic structure and migration patterns of the beetle populations throughout the Pyrenean mountain range was combined with a spread model simulating the potential movements of nematode-infested beetles across it. The central part of the Pyrenees, which corresponds to the highest elevation zone, was shown to prevent gene flow between the French and Spanish populations of M. galloprovincialis on each side of the mountains. Conversely, strong admixture was detected between populations located on both sides of low elevation hills, and especially at the east and west extremities of the mountain range. Simulations of the spread of nematode-infested beetles under various thresholds of beetle survival and pine wilt disease expression gave results consistent with the variation in genetic make-up, suggesting that western and eastern hillsides may represent corridors favoring natural spread of the nematode from the Iberian Peninsula to France. Simulations also showed that temperature rise due to climate change may significantly reduce the extent of the barrier formed by highest elevations. Our results support the hypothesis that the Pyrenean chain represents a partial barrier to the natural spread of nematode-infested beetles. These results, which have to be considered together with potential human-assisted long-distance spread of the nematode, highlight priority zones for future pest monitoring and management programs. More generally, such an integrated approach could be used to assess the role of mountain chains in the potential spread of other invasive pests.

Are heat waves susceptible to mitigate the expansion of a species progressing with global warming?

A number of organisms, especially insects, are extending their range in response of the increasing trend of warmer temperatures. However, the effects of more frequent climatic anomalies on these species are not clearly known. The pine processionary moth, Thaumetopoea pityocampa, is a forest pest that is currently extending its geographical distribution in Europe in response to climate warming. However, its population density largely decreased in its northern expansion range (near Paris, France) the year following the 2003 heat wave. In this study, we tested whether the 2003 heat wave could have killed a large part of egg masses. First, the local heat wave intensity was determined. Then, an outdoor experiment was conducted to measure the deviation between the temperatures recorded by weather stations and those observed within sun-exposed egg masses. A second experiment was conducted under laboratory conditions to simulate heat wave conditions (with night/day temperatures of 20/32°C and 20/40°C compared to the control treatment 13/20°C) and measure the potential effects of this heat wave on egg masses. No effects were noticed on egg development. Then, larvae hatched from these egg masses were reared under mild conditions until the third instar and no delayed effects on the development of larvae were found. Instead of eggs, the 2003 heat wave had probably affected directly or indirectly the young larvae that were already hatched when it occurred. Our results suggest that the effects of extreme climatic anomalies occurring over narrow time windows are difficult to determine because they strongly depend on the life stage of the species exposed to these anomalies. However, these effects could potentially reduce or enhance the average warming effects. As extreme weather conditions are predicted to become more frequent in the future, it is necessary to disentangle the effects of the warming trend from the effects of climatic anomalies when predicting the response of a species to climate change.

Assessing species distribution using Google Street View: a pilot study with the Pine Processionary Moth.

Mapping species spatial distribution using spatial inference and prediction requires a lot of data. Occurrence data are generally not easily available from the literature and are very time-consuming to collect in the field. For that reason, we designed a survey to explore to which extent large-scale databases such as Google maps and Google Street View could be used to derive valid occurrence data. We worked with the Pine Processionary Moth (PPM) Thaumetopoea pityocampa because the larvae of that moth build silk nests that are easily visible. The presence of the species at one location can therefore be inferred from visual records derived from the panoramic views available from Google Street View. We designed a standardized procedure allowing evaluating the presence of the PPM on a sampling grid covering the landscape under study. The outputs were compared to field data. We investigated two landscapes using grids of different extent and mesh size. Data derived from Google Street View were highly similar to field data in the large-scale analysis based on a square grid with a mesh of 16 km (96% of matching records). Using a 2 km mesh size led to a strong divergence between field and Google-derived data (46% of matching records). We conclude that Google database might provide useful occurrence data for mapping the distribution of species which presence can be visually evaluated such as the PPM. However, the accuracy of the output strongly depends on the spatial scales considered and on the sampling grid used. Other factors such as the coverage of Google Street View network with regards to sampling grid size and the spatial distribution of host trees with regards to road network may also be determinant.

An improved method to extract DNA from 1 ml of uncultured amniotic fluid from patients at less than 16 weeks' gestation.

The aim of this study was to develop an improved technique for DNA extraction from 1 ml of uncultured AF from patients with a gestational age less than 16 weeks and to allow the use of array-CGH without DNA amplification. The DNA extraction protocol was tested in a series of 90 samples including 41 of uncultured AF at less than 16 weeks of gestation. Statistical analyses were performed using linear regression. To evaluate the sensitivity and the specificity of array-CGH on 1 ml of uncultured AF, five samples with an abnormal karyotype (three with aneuploidy, two with structural abnormalities) and five with a normal karyotype were studied. This protocol was reproducible and we were able to show a great improvement with higher yield of DNA obtained from all patients, including those with a gestational age less than 16 weeks (p = 0.003). All chromosomal abnormalities were detected and characterized by array-CGH and normal samples showed normal profiles. This new DNA extraction protocol associated with array-CGH analysis could be used in prenatal testing even when gestational age is less than 16 weeks, especially in cases with abnormal ultrasound findings.

Framework for modelling economic impacts of invasive species, applied to pine wood nematode in Europe.

BACKGROUND: Economic impact assessment of invasive species requires integration of information on pest entry, establishment and spread, valuation of assets at risk and market consequences at large spatial scales. Here we develop such a framework and demonstrate its application to the pinewood nematode, Bursaphelenchus xylophilus, which threatens the European forestry industry. The effect of spatial resolution on the assessment result is analysed. METHODOLOGY/PRINCIPAL FINDINGS: Direct economic impacts resulting from wood loss are computed using partial budgeting at regional scale, while impacts on social welfare are computed by a partial equilibrium analysis of the round wood market at EU scale. Substantial impacts in terms of infested stock are expected in Portugal, Spain, Southern France, and North West Italy but not elsewhere in EU in the near future. The cumulative value of lost forestry stock over a period of 22 years (2008-2030), assuming no regulatory control measures, is estimated at €22 billion. The greatest yearly loss of stock is expected to occur in the period 2014-2019, with a peak of three billion euros in 2016, but stabilizing afterwards at 300-800 million euros/year. The reduction in social welfare follows the loss of stock with considerable delay because the yearly harvest from the forest is only 1.8%. The reduction in social welfare for the downstream round wood market is estimated at €218 million in 2030, whereby consumers incur a welfare loss of €357 million, while producers experience a €139 million increase, due to higher wood prices. The societal impact is expected to extend to well beyond the time horizon of the analysis, and long after the invasion has stopped. CONCLUSIONS/SIGNIFICANCE: Pinewood nematode has large economic consequences for the conifer forestry industry in the EU. A change in spatial resolution affected the calculated directed losses by 24%, but did not critically affect conclusions.

A suite of models to support the quantitative assessment of spread in pest risk analysis.

Pest Risk Analyses (PRAs) are conducted worldwide to decide whether and how exotic plant pests should be regulated to prevent invasion. There is an increasing demand for science-based risk mapping in PRA. Spread plays a key role in determining the potential distribution of pests, but there is no suitable spread modelling tool available for pest risk analysts. Existing models are species specific, biologically and technically complex, and data hungry. Here we present a set of four simple and generic spread models that can be parameterised with limited data. Simulations with these models generate maps of the potential expansion of an invasive species at continental scale. The models have one to three biological parameters. They differ in whether they treat spatial processes implicitly or explicitly, and in whether they consider pest density or pest presence/absence only. The four models represent four complementary perspectives on the process of invasion and, because they have different initial conditions, they can be considered as alternative scenarios. All models take into account habitat distribution and climate. We present an application of each of the four models to the western corn rootworm, Diabrotica virgifera virgifera, using historic data on its spread in Europe. Further tests as proof of concept were conducted with a broad range of taxa (insects, nematodes, plants, and plant pathogens). Pest risk analysts, the intended model users, found the model outputs to be generally credible and useful. The estimation of parameters from data requires insights into population dynamics theory, and this requires guidance. If used appropriately, these generic spread models provide a transparent and objective tool for evaluating the potential spread of pests in PRAs. Further work is needed to validate models, build familiarity in the user community and create a database of species parameters to help realize their potential in PRA practice.

Geographic variation in North American gypsy moth cycles: subharmonics, generalist predators, and spatial coupling.

Many defoliating forest lepidopterans cause predictable periodic deforestation. Several of these species exhibit geographical variation in both the strength of periodic behavior and the frequency of cycles. The mathematical models used to describe the population dynamics of such species commonly predict that gradual variation in the underlying ecological mechanisms may lead to punctuated (subharmonic) variation in outbreak cycles through period-doubling cascades. Gypsy moth, Lymantria dispar, in its recently established range in the northeastern United States may represent an unusually clear natural manifestation of this phenomenon. In this study we introduce a new statistical spatial-smoothing method for estimating outbreak periodicity from space-time defoliation data collected with spatial error. The method statistically confirms the existence of subharmonic variation in cyclicity among different forest types. Some xeric forest types exhibit a statistical 4-5 year period in outbreak dynamics, some mesic forest types a 9-10 year period, and some intermediate forest types a dominant 9-10 year period with a 4-5 year subdominant superharmonic. We then use a theoretical model involving gypsy moth, pathogens, and predators to investigate the possible role of geographical variation in generalist predator populations as the cause of this variation in dynamics. The model predicts that the period of gypsy moth oscillations should be positively associated with predator carrying capacity and that variation in the carrying capacity provides a parsimonious explanation of previous reports of geographical variation in gypsy moth periodicity. Furthermore, a two-patch spatial extension of the model shows that, in the presence of spatial coupling, subharmonic attractors can coexist whereas nonharmonic attractors (i.e., where the cycle lengths are not integer multiples of one another) cannot.

Direct impacts of recent climate warming on insect populations.

Effects of recent climate change have already been detected in many species, and, in particular, in insects. The present paper reviews the key impacts of global warming on insect development and dispersal. The effects of climate change appear to be much more complex than a simple linear response to an average increase in temperature. They can differ between seasons and bioclimatic regions. Earlier flight periods, enhanced winter survival and acceleration of development rates are the major insect responses. Differential response of insects and hosts to warming up might also lead to disruption of their phenological synchrony, but adaptive genetic processes are likely to quickly restore this synchrony. In a number of cases, warming results in removing or relocating the barriers that limit present species' ranges. It is also likely to facilitate the establishment and spread of invasive alien species. Finally, knowledge gaps are identified and future research interests are suggested.

Dispersal polymorphism in an invasive forest pest affects its ability to establish.

Given the increasing number of biological invasions, there is a crucial need to identify life history traits that promote invasion. Invasiveness reflects capabilities for both establishment after introduction and spread following establishment. In this paper, we explore, via simulation, the interacting effects of dispersal and Allee effects on both invasion processes. Dispersal capability is a trait that has been widely recognized to facilitate invasions. However, dispersal dilutes local population densities in isolated populations and this could strengthen Allee effects, ultimately promoting extinction of invading populations. A spatially explicit, stochastic individual-based model was used to simulate dispersal, mating, and growth in isolated, newly arrived invading populations. We used the invasion of North America by the gypsy moth, Lymantria dispar, as a case study because: (1) a great amount of biological data on the species is available; (2) Allee effects caused by mate location failure are known to play an important role in its establishment and spread; and (3) a dispersal polymorphism has previously been identified (i.e., in some populations adult females are fully capable of flight, but in other populations females are not able to fly). We considered the introduction of a hypothetical number of eggs at a single location, originating from populations with varying female dispersal capabilities, and we then used simulation models to evaluate the population growth rate over two generations as well as spread distance. Nondispersing populations had the highest growth rates and inclusion of even limited dispersal capabilities caused population growth rates to be greatly diminished. The Allee threshold was 700 eggs for nondispersing populations and 1400 eggs for the long-distance dispersing populations. Thus, for an intermediate number of eggs initially introduced, nondispersing populations would most likely establish, whereas dispersing populations would likely become extinct. Spread distance increased linearly with the number of eggs initially introduced in both dispersing and nondispersing populations but rapidly reached a limit for nondispersing populations. Though species capable of long-distance dispersal may invade a larger area than nondispersing species, their growth rates are likely to be considerably lower, and eradication should be easier. Following these results, strategies for managing invasions should be adjusted for the interactions between Allee effects and dispersal.

Alien species in a warmer world: risks and opportunities.

Climate change and biological invasions are key processes affecting global biodiversity, yet their effects have usually been considered separately. Here, we emphasise that global warming has enabled alien species to expand into regions in which they previously could not survive and reproduce. Based on a review of climate-mediated biological invasions of plants, invertebrates, fishes and birds, we discuss the ways in which climate change influences biological invasions. We emphasise the role of alien species in a more dynamic context of shifting species' ranges and changing communities. Under these circumstances, management practices regarding the occurrence of 'new' species could range from complete eradication to tolerance and even consideration of the 'new' species as an enrichment of local biodiversity and key elements to maintain ecosystem services.

Role of human-mediated dispersal in the spread of the pinewood nematode in China.

BACKGROUND: Intensification of world trade is responsible for an increase in the number of alien species introductions. Human-mediated dispersal promotes not only introductions but also expansion of the species distribution via long-distance dispersal. Thus, understanding the role of anthropogenic pathways in the spread of invading species has become one of the most important challenges nowadays. METHODOLOGY/PRINCIPAL FINDINGS: We analysed the invasion pattern of the pinewood nematode in China based on invasion data from 1982 to 2005 and monitoring data on 7 locations over 15 years. Short distance spread mediated by long-horned beetles was estimated at 7.5 km per year. Infested sites located further away represented more than 90% of observations and the mean long distance spread was estimated at 111-339 km. Railways, river ports, and lakes had significant effects on the spread pattern. Human population density levels explained 87% of the variation in the invasion probability (P<0.05). Since 2001, the number of new records of the nematode was multiplied by a factor of 5 and the spread distance by a factor of 2. We combined a diffusion model to describe the short distance spread with a stochastic, individual based model to describe the long distance jumps. This combined model generated an error of only 13% when used to predict the presence of the nematode. Under two climate scenarios (stable climate or moderate warming), projections of the invasion probability suggest that this pest could expand its distribution 40-55% by 2025. CONCLUSIONS/SIGNIFICANCE: This study provides evidence that human-induced dispersal plays a fundamental role in the spread of the pinewood nematode, and appropriate control measures should be taken to stop or slow its expansion. This model can be applied to Europe, where the nematode had been introduced later, and is currently expanding its distribution. Similar models could also be derived for other species that could be accidentally transported by humans.