Alain Roques

EXPANSION OF GEOGRAPHIC RANGE IN THE PINE PROCESSIONARY MOTH CAUSED BY INCREASED WINTER TEMPERATURES

Global warming is predicted to cause distributional changes in organisms whose geographic ranges are controlled by temperature. We report a recent latitudinal and altitudinal expansion of the pine processionary moth, Thaumetopoea pityocampa, whose larvae build silk nests and feed on pine foliage in the winter. In north-central France (Paris Basin), its range boundary has shifted by 87 km northwards between 1972 and 2004; in northern Italy (Alps), an altitudinal shift of 110–230 m upwards occurred between 1975 and 2004. By experimentally linking winter temperature, feeding activity, and survival of T. pityocampa larvae, we attribute the expansions to increased winter survival due to a warming trend over the past three decades. In the laboratory we determined the minimum nest and night air temperatures required for larval feeding and developed a mechanistic model based on these temperature thresholds. We tested the model in a translocation experiment that employed natural temperature gradients as spatial an...

Disentangling the role of environmental and human pressures on biological invasions across Europe

The accelerating rates of international trade, travel, and transport in the latter half of the twentieth century have led to the progressive mixing of biota from across the world and the number of species introduced to new regions continues to increase. The importance of biogeographic, climatic, economic, and demographic factors as drivers of this trend is increasingly being realized but as yet there is no consensus regarding their relative importance. Whereas little may be done to mitigate the effects of geography and climate on invasions, a wider range of options may exist to moderate the impacts of economic and demographic drivers. Here we use the most recent data available from Europe to partition between macroecological, economic, and demographic variables the variation in alien species richness of bryophytes, fungi, vascular plants, terrestrial insects, aquatic invertebrates, fish, amphibians, reptiles, birds, and mammals. Only national wealth and human population density were statistically significant predictors in the majority of models when analyzed jointly with climate, geography, and land cover. The economic and demographic variables reflect the intensity of human activities and integrate the effect of factors that directly determine the outcome of invasion such as propagule pressure, pathways of introduction, eutrophication, and the intensity of anthropogenic disturbance. The strong influence of economic and demographic variables on the levels of invasion by alien species demonstrates that future solutions to the problem of biological invasions at a national scale lie in mitigating the negative environmental consequences of human activities that generate wealth and by promoting more sustainable population growth.

Socioeconomic legacy yields an invasion debt

Globalization and economic growth are widely recognized as important drivers of biological invasions. Consequently, there is an increasing need for governments to address the role of international trade in their strategies to prevent species introductions. However, many of the most problematic alien species are not recent arrivals but were introduced several decades ago. Hence, current patterns of alien-species richness may better reflect historical rather than contemporary human activities, a phenomenon which might be called “invasion debt.” Here, we show that across 10 taxonomic groups (vascular plants, bryophytes, fungi, birds, mammals, reptiles, amphibians, fish, terrestrial insects, and aquatic invertebrates) in 28 European countries, current numbers of alien species established in the wild are indeed more closely related to indicators of socioeconomic activity from the year 1900 than to those from 2000, although the majority of species introductions occurred during the second half of the 20th century. The strength of the historical signal varies among taxonomic groups, with those possessing good capabilities for dispersal (birds, insects) more strongly associated with recent socioeconomic drivers. Nevertheless, our results suggest a considerable historical legacy for the majority of the taxa analyzed. The consequences of the current high levels of socioeconomic activity on the extent of biological invasions will thus probably not be completely realized until several decades into the future.

No saturation in the accumulation of alien species worldwide

Although research on human-mediated exchanges of species has substantially intensified during the last centuries, we know surprisingly little about temporal dynamics of alien species accumulations across regions and taxa. Using a novel database of 45,813 first records of 16,926 established alien species, we show that the annual rate of first records worldwide has increased during the last 200 years, with 37% of all first records reported most recently (1970–2014). Inter-continental and inter-taxonomic variation can be largely attributed to the diaspora of European settlers in the nineteenth century and to the acceleration in trade in the twentieth century. For all taxonomic groups, the increase in numbers of alien species does not show any sign of saturation and most taxa even show increases in the rate of first records over time. This highlights that past efforts to mitigate invasions have not been effective enough to keep up with increasing globalization.

Mitochondrial and microsatellite DNA markers reveal a Balkan origin for the highly invasive horse‐chestnut leaf miner Cameraria ohridella (Lepidoptera, Gracillariidae)

Biological invasions usually start with a small number of founder individuals. These founders are likely to represent a small fraction of the total genetic diversity found in the source population. Our study set out to trace genetically the geographical origin of the horse‐chestnut leafminer, Cameraria ohridella, an invasive microlepidopteran whose area of origin is still unkown. Since its discovery in Macedonia 25 years ago, this insect has experienced an explosive westward range expansion, progressively colonizing all of Central and Western Europe. We used cytochrome oxidase I sequences (DNA barcode fragment) and a set of six polymorphic microsatellites to assess the genetic variability of C. ohridella populations, and to test the hypothesis that C. ohridella derives from the southern Balkans (Albania, Macedonia and Greece). Analysis of mtDNA of 486 individuals from 88 localities allowed us to identify 25 geographically structured haplotypes. In addition, 480 individuals from 16 populations from Europe and the southern Balkans were genotyped for 6 polymorphic microsatellite loci. High haplotype diversity and low measures of nucleotide diversities including a significantly negative Tajima’s D indicate that C. ohridella has experienced rapid population expansion during its dispersal across Europe. Both mtDNA and microsatellites show a reduction in genetic diversity of C. ohridella populations sampled from artificial habitats (e.g. planted trees in public parks, gardens, along roads in urban or sub‐urban areas) across Europe compared with C. ohridella sampled in natural stands of horse‐chestnuts in the southern Balkans. These findings suggest that European populations of C. ohridella may indeed derive from the southern Balkans.

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.

Phylogeography of the pine processionary moth Thaumetopoea wilkinsoni in the Near East

Phylogeographic structure of the eastern pine processionary moth Thaumetopoea wilkinsoni was explored in this study by means of nested clade phylogeographic analyses of COI and COII sequences of mitochondrial DNA and Bayesian estimates of divergence times. Intraspecific relationships were inferred and hypotheses tested to understand historical spread patterns and spatial distribution of genetic variation. Analyses revealed that all T. wilkinsoni sequences were structured in three clades, which were associated with two major biogeographic events, the colonization of the island of Cyprus and the separation of southwestern and southeastern Anatolia during the Pleistocene. Genetic variation in populations of T. wilkinsoni was also investigated using amplified fragment length polymorphisms and four microsatellite loci. Contrasting nuclear with mitochondrial data revealed recurrent gene flow between Cyprus and the mainland, related to the long‐distance male dispersal. In addition, a reduction in genetic variability was observed at both mitochondrial and nuclear markers at the expanding boundary of the range, consistent with a recent origin of these populations, founded by few individuals expanding from nearby localities. In contrast, several populations fixed for one single mitochondrial haplotype showed no reduction in nuclear variability, a pattern that can be explained by recurrent male gene flow or selective sweeps at the mitochondrial level. The use of both mitochondrial and nuclear markers was essential in understanding the spread patterns and the population genetic structure of T. wilkinsoni, and is recommended to study colonizing species characterized by sex‐biased dispersal.

Temporal and interspecific variation in rates of spread for insect species invading Europe during the last 200 years

Globalization is triggering an increase in the establishment of alien insects in Europe, with several species having substantial ecological and economic impacts. We investigated long-term changes in rates of species spread following establishment. We used the total area of countries invaded by 1171 insect species for which the date of first record in Europe is known, to estimate their current range radius (calculated as [invaded area]0.5/π). We estimated initial rates of radial spread and compared them among different groups of insects for all years (1800–2014) and for a subset of more recent decades (1950–2014). Accidentally introduced species spread faster than intentionally introduced species. Considering the whole period 1800–2014, spread patterns also differ between feeding guilds, with decreasing spread rates over residence time in herbivores but not in detritivores or parasitic species. These decreases for herbivorous species appeared mainly in those associated with herbaceous plants and crops rather than woody plants. Initial spread rate was significantly greater for species detected after 1990, roughly 3–4 times higher than for species that arrived earlier. We hypothesize that the political changes in Europe following the collapse of the Iron Curtain in 1989, and the further dismantling of customs checkpoints within an enlarged European Union (EU) have facilitated the faster spread of alien insect species. Also, the number of species first recorded in the Eastern Bloc of the politically-divided Europe before 1989 was lower than for the rest of Europe. A detailed analysis of six recent invaders indicated a dominant role of long-distance translocations related to human activities, especially with the plant trade, in determining rates of spread.

Human-mediated long-distance jumps of the pine processionary moth in Europe

Although climate change is currently affecting the distribution of many species, insects are particularly impacted because of their high sensitivity to temperature. The pine processionary moth, Thaumetopoea pityocampa, is a forest insect extending its distribution in response to climate warming. Some pioneer colonies were recently detected far beyond the main range, near Paris and in eastern France. This study tracked the origin and pathways of these pioneer colonies through a combined use of genetic markers, measurement of female flight capabilities, and comparative analyses of the natural enemy complexes. This study also aimed to determine the establishment capability beyond the main range, considering the survival rate during two recent cold periods. The larval survival rate was higher in pioneer colonies (which behave like urban heat islands) than in main range. The flight capacity of females would not have allowed them to come from the main range or the nearest established colonies, and molecular tools further showed that individuals from at least three pioneer colonies were not assigned or similar to individuals at the edge of the main range. Egg parasitoids were absent while pupal parasitoids were present in the pioneer colonies suggesting an introduction at the pupal stage. These approaches provided strong evidence that this species has been accidentally moved near Paris and to eastern France, supporting the hypothesis of human-mediated transportation over natural dispersal. This type of dispersal was unexpected because of risks from urticating hairs and the easy detection of the species.

Oviposition strategies of conifer seed chalcids in relation to host phenology

Insects are considered the most important predators of seed cones, the female reproductive structures of conifers, prior to seed dispersal. Slightly more than 100 genera of insects are known to parasitize conifer seed cones. The most diverse (i.e., number of species) of these genera is Megastigmus (Hymenoptera: Torymidae), which comprises many important seed pests of native and exotic conifers. Seed chalcids, Megastigmus spp., lay eggs inside the developing ovules of host conifers and, until recently, oviposition was believed to occur only in fertilized ovules. Ovule development begins just after pollination, but stops if cells are not fertilized. The morphological stage of cone development at the time of oviposition by seed chalcids has been established for many species; however, knowledge of ovule development at that time has been documented for only one species, M. spermotrophus. Megastigmus spermotrophus oviposits in Douglas-fir ovules after pollination but before fertilization. Unlike the unfertilized ovules, those containing a M. spermotrophus larva continue to develop, whether fertilized or not, stressing the need to broaden our understanding of the insect–plant interactions for this entire genus. To achieve this task, we reviewed the scientific literature and assembled information pertaining to the timing of oviposition and to the pollination and fertilization periods of their respective host(s). More specifically, we were searching for circumstantial evidence that other species of Megastigmus associated with conifers could behave (i.e., oviposit before ovule fertilization) and impact on female gametophyte (i.e., prevent abortion) like M. spermotrophus. The evidence from our compilation suggests that seed chalcids infesting Pinaceae may also oviposit before ovule fertilization, just like M. spermotrophus, whereas those infesting Cupressaceae seemingly oviposit after ovule fertilization. Based on this evidence, we hypothesize that all species of Megastigmus associated with Pinaceae can oviposit in unfertilized ovules, whereas those exploiting Cupressaceae cannot, and thus oviposit only in already fully developed fertilized seeds. Furthermore, we predict that the presence of a larva in unfertilized ovules of all Pinaceae will influence the development of the female gametophyte by preventing its abortion. This influence on the Pinaceae can be interpreted as an ability to parasitize any of the potential seeds present in a seed cone, and as such represents a much more efficient oviposition strategy than searching and locating only fertilized seeds. Concomitantly, this ability has likely led to an overestimation of the impact of the species of seed chalcid infesting Pinaceae on seed production.