Lin Op de Beeck

Urbanisation shapes behavioural responses to a pesticide

The degree of urbanisation is rapidly increasing worldwide. Due to anthropogenic impact, urban populations are exposed to higher levels of contaminants and higher temperatures. Despite this, urbanisation is a largely overlooked spatial component in ecotoxicology. We tested in a common garden rearing experiment whether replicated urban and rural populations of the damselfly Coenagrion puella differ in their vulnerability to sublethal levels of a widespread pesticide, chlorpyrifos, in terms of ecologically relevant behaviours (exploration behaviour, activity, boldness and food intake), and to what extent these patterns are affected by temperature (20 and 24°C). Except boldness, all behaviours were affected by previous pesticide exposure. While the pesticide did not affect exploration behaviour at 20°C, it was associated with increased exploration at 24°C, which may reflect an increased toxicity of chlorpyrifos at higher temperatures. Importantly, rural and urban larvae showed consistently different, sometimes even opposite behavioural responses to pesticide exposure. When exposed to the pesticide, rural larvae decreased activity and food intake at both temperatures; urban larvae instead increased activity at both temperatures and only reduced food intake at the high temperature. This suggests that urban larvae were less affected by the pesticide, which would be consistent with a scenario of local adaptation to higher contaminant levels. Our results highlight that urbanisation may be an important factor to arrive at a spatially explicit ecological risk assessment, and may be an ignored reason why studies on the same species may generate widely different vulnerabilities to pesticides.

Microgeographic differentiation in thermal performance curves between rural and urban populations of an aquatic insect

The rapidly increasing rate of urbanization has a major impact on the ecology and evolution of species. While increased temperatures are a key aspect of urbanization (“urban heat islands”), we have very limited knowledge whether this generates differentiation in thermal responses between rural and urban populations. In a common garden experiment, we compared the thermal performance curves (TPCs) for growth rate and mortality in larvae of the damselfly Coenagrion puella from three urban and three rural populations. TPCs for growth rate shifted vertically, consistent with the faster–slower theoretical model whereby the cold‐adapted rural larvae grew faster than the warm‐adapted urban larvae across temperatures. In line with costs of rapid growth, rural larvae showed lower survival than urban larvae across temperatures. The relatively lower temperatures hence expected shorter growing seasons in rural populations compared to the populations in the urban heat islands likely impose stronger time constraints to reach a certain developmental stage before winter, thereby selecting for faster growth rates. In addition, higher predation rates at higher temperature may have contributed to the growth rate differences between urban and rural ponds. A faster–slower differentiation in TPCs may be a widespread pattern along the urbanization gradient. The observed microgeographic differentiation in TPCs supports the view that urbanization may drive life‐history evolution. Moreover, because of the urban heat island effect, urban environments have the potential to aid in developing predictions on the impact of climate change on rural populations.

Sexual selection reinforces a higher flight endurance in urban damselflies

Urbanization is among the most important and globally rapidly increasing anthropogenic processes and is known to drive rapid evolution. Habitats in urbanized areas typically consist of small, fragmented and isolated patches, which are expected to select for a better locomotor performance, along with its underlying morphological traits. This, in turn, is expected to cause differentiation in selection regimes, as populations with different frequency distributions for a given trait will span different parts of the species’ fitness function. Yet, very few studies considered differentiation in phenotypic traits associated with patterns in habitat fragmentation and isolation along urbanization gradients, and none considered differentiation in sexual selection regimes. We investigated differentiation in flight performance and flight‐related traits and sexual selection on these traits across replicated urban and rural populations of the scrambling damselfly Coenagrion puella. To disentangle direct and indirect paths going from phenotypic traits over performance to mating success, we applied a path analysis approach. We report for the first time direct evidence for the expected better locomotor performance in urban compared to rural populations. This matches a scenario of spatial sorting, whereby only the individuals with the best locomotor abilities colonize the isolated urban populations. The covariation patterns and causal relationships among the phenotypic traits, performance and mating success strongly depended on the urbanization level. Notably, we detected sexual selection for a higher flight endurance only in urban populations, indicating that the higher flight performance of urban males was reinforced by sexual selection. Taken together, our results provide a unique proof of the interplay between sexual selection and adaptation to human‐altered environments.

Evolution determines how global warming and pesticide exposure will shape predator–prey interactions with vector mosquitoes

How evolution may mitigate the effects of global warming and pesticide exposure on predator–prey interactions is directly relevant for vector control. Using a space‐for‐time substitution approach, we addressed how 4°C warming and exposure to the pesticide endosulfan shape the predation on Culex pipiens mosquitoes by damselfly predators from replicated low‐ and high‐latitude populations. Although warming was only lethal for the mosquitoes, it reduced predation rates on these prey. Possibly, under warming escape speeds of the mosquitoes increased more than the attack efficiency of the predators. Endosulfan imposed mortality and induced behavioral changes (including increased filtering and thrashing and a positional shift away from the bottom) in mosquito larvae. Although the pesticide was only lethal for the mosquitoes, it reduced predation rates by the low‐latitude predators. This can be explained by the combination of the evolution of a faster life history and associated higher vulnerabilities to the pesticide (in terms of growth rate and lowered foraging activity) in the low‐latitude predators and pesticide‐induced survival selection in the mosquitoes. Our results suggest that predation rates on mosquitoes at the high latitude will be reduced under warming unless predators evolve toward the current low‐latitude phenotype or low‐latitude predators move poleward.

Synthetic predator cues impair immune function and make the biological pesticide Bti more lethal for vector mosquitoes

The control of vector mosquitoes is one of the biggest challenges facing humankind with the use of chemical pesticides often leading to environmental impact and the evolution of resistance. Although to a lesser extent, this also holds for Bacillus thuringiensis israelensis (Bti), the most widely used biological pesticide to control mosquito populations. This raises the need for the development of integrated pest management strategies that allow the reduction of Bti concentrations without loss of the mosquito control efficiency. To this end, we tested in a laboratory experiment the combined effects of larval exposure to a sublethal Bti concentration and predation risk cues on life history and physiology of larval and adult Culex pipiens mosquitoes. Besides natural predator kairomones and prey alarm cues, we also tested synthetic kairomones of Notonecta predators. Neither Bti nor predation risk cues affected mortality, yet when both stressors were combined mortality increased on average by 133% compared to the treatment with only predation risk cues. This synergistic interaction was also present when Bti was combined with synthetic kairomones. This was further reflected in changes of the composite index of population performance, which suggested lowered per capita growth rates in mosquitoes exposed to Bti but only when Bti was combined with synthetic kairomones. Furthermore, predation risk cues shortened larval development time, reduced mass at metamorphosis in males, and had an immunosuppressive effect in larval and adult mosquitoes which may affect the mosquito vector competence. We provide the first demonstration that synthetic kairomones may generate similar effects on prey as natural kairomones. The identified immunosuppressive effect of synthetic kairomones and the novel lethal synergism type between a biological pesticide and synthetic predator kairomones provide an important proof of principle illustrating the potential of this combination for integrated mosquito control and should in a next step be evaluated under more natural conditions. It may guide novel integrated pest management programs with Bti that incorporate synthetic kairomones and thereby can reduce environmental impact and evolution of resistance creating more efficient and sustainable mosquito control.

Warming under seminatural outdoor conditions in the larval stage negatively affects insect flight performance

Laboratory studies indicate global warming may cause changes in locomotor performance directly relevant for fitness and dispersal. Yet, this remains to be tested under seminatural settings, and the connection with warming-induced alterations in the underlying traits has been rarely studied. In an outdoor mesocosm experiment with the damselfly Ischnura elegans, 4°C warming in the larval stage decreased the flight muscle mass, which correlated with a lower flight endurance. Warming did not affect body mass, size or wing morphology. This illustrates how carry-over effects of warming under seminatural conditions during early development bridge metamorphosis and negatively impact locomotor performance through changes in a key flight-related trait.