Nedim Tüzün

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.

Daily temperature variation and extreme high temperatures drive performance and biotic interactions in a warming world

We review the major patterns on the effects of daily temperature variation (DTV) and extreme high temperatures (EXT) on performance traits and the resulting outcome of biotic interactions in insects. EXT profoundly affects the outcome of all types of biotic interactions: competitive, predator-prey, herbivore-plant, host-pathogen/parasitoid and symbiotic interactions. Studies investigating effects of DTV on biotic interactions are few but also show strong effects on competitive and host-pathogen/parasitoid interactions. EXT typically reduces predation, and is expected to reduce parasitoid success. The effects of EXT and DTV on the outcome of the other interaction types are highly variable, yet can be predicted based on comparisons of the TPCs of the interacting species, and challenges the formulation of general predictions about the change in biotic interactions in a warming world.

Within-season variation in sexual selection on flight performance and flight-related traits in a damselfly

While selection is a key mechanism of evolution, our understanding of within-season variation in sexual selection remains limited. Here, we studied within-season sexual selection on two key performance traits, flight speed and flight endurance, and a set of morphological and physiological phenotypic traits in a natural population of the territorial damselfly Chalcolestes viridis. We applied a path analysis approach to address whether the flight-related traits affected mating success directly or indirectly through their effect on the flight performance traits, and whether these selection patterns differed between the first and second half of the reproductive season. While some trait means did not differ between both parts of the season (flight speed, wing loading and non-allometric wing shape), most traits showed within-season differences (flight endurance, fat content, flight muscle ratio, wing centroid size, body mass and the allometric wing shape). Despite the within-season temporal differences in flight endurance, sexual selection consistently favoured males with a higher flight endurance. None of the detected patterns of sexual selection on the flight-related traits were consistently significant in both periods: while we detected selection on wing loading and wing centroid size in the first half of the season, we detected selection on body mass in the second half of the season. More studies focusing on understudied traits such as performance traits are needed to refine our knowledge of the temporal dynamics of selection patterns in nature. This is important to arrive at a better understanding of the adaptive evolutionary dynamics of traits in natural populations.

Carry-Over Effects Across Metamorphosis of a Pesticide on Female Lifetime Fitness Strongly Depend on Egg Hatching Phenology: A Longitudinal Study under Seminatural Conditions

Current ecological risk assessment of pesticides fails to protect aquatic biodiversity. For the first time, we tested two potential reasons for this failure with regard to carry-over effects across metamorphosis: their dependence on hatching period, and the lack of studies quantifying adult fitness under seminatural conditions. Using the damselfly Coenagrion puella sampled from six populations, we designed an outdoor longitudinal one-year study starting from the egg stage. We exposed the aquatic larvae to the pesticide esfenvalerate (0.11 μg/L) during the initial microcosm part. Next, we monitored the lifetime fitness of the terrestrial adults in an insectary. Exposure to the pesticide negatively impacted not only larval traits, but also drastically reduced lifetime mating success of adult females. The impact of this postmetamorphic effect of the pesticide on the population level was three times more important than the effects in the larval stage. Importantly, this carry-over effect was only present in females that hatched early in the season, and was not mediated by metamorphic traits (age and mass at emergence). We provide proof-of-principle under seminatural conditions for two potential pitfalls that need to be considered when improving risk assessment: carry-over effects on adult fitness can (i) be much more important than effects during the larval stage and may not be captured by metamorphic traits, and (ii) be strongly modulated by egg hatching dates.

Pesticide-induced changes in personality depend on the urbanization level

Globally increasing urbanization causes major anthropogenic changes in ecosystems, drastically altering phenotypes of organisms. Increased contamination is a well-known result of urbanization, and its effect on behaviour has been extensively studied. Yet, animal personality, consistent behavioural variation between individuals, has rarely been investigated in the context of anthropogenic contaminants. Changes in personalities may affect the viability of populations, and even alter community dynamics. We investigated the effects of exposure to a sublethal dose of the commonly used pesticide esfenvalerate on two personality traits, activity and boldness, and compared these effects between replicated rural and urban populations using larvae of the damselfly Coenagrion puella. We tested for effects on behaviour at three distinct levels: the average levels of behaviours, the consistency of behaviours (repeatability), and the structure of the behavioural correlations (behavioural syndrome). We found that the pesticide treatment changed the average activity and the behavioural covariation (activity and boldness), but not the behavioural repeatability. Importantly, these pesticide-induced patterns depended strongly on urbanization level. The average activity reduction due to pesticide exposure was only present in urban individuals. Moreover, while a behavioural correlation between activity and boldness in rural larvae appeared only after the pesticide treatment, this activity–boldness syndrome was consistently present in the urban larvae. These differential responses of urban and rural populations may be explained by the apparently more efficient coping mechanism with contaminants of urban populations, as well as the generally more stressful urban habitats. These results highlight the importance of measuring behavioural expressions at various levels when assessing contaminant effects, and not just the means. Further, we suggest that pollution may play an important role in understanding the evolution and maintenance of animal personalities in natural populations.

Evolution of geographic variation in thermal performance curves in the face of climate change and implications for biotic interactions

We review the recent literature on geographic variation in insect thermal performance curves (TPCs). Despite strong thermal differences, there is often no change in TPCs across geographic gradients. When shifts occur, these are mostly vertical (indicating an overall shift in performance across temperatures, that is, countergradient or cogradient variation) and less horizontal (reflecting thermal adaptation). Based on this, using a space-for-time substitution approach, we generated likely evolutionary scenarios of TPC evolution to simulate the outcome of biotic interactions under future warming. We illustrate how taking evolution of the TPCs into account may strongly impact the predicted outcome of biotic interactions under climate warming. Importantly, both the type and the magnitude of the TPC shift was identified to be crucial to determine who will be winners and losers of biotic interactions.

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.