Sara Debecker

Integrating the pace‐of‐life syndrome across species, sexes and individuals: covariation of life history and personality under pesticide exposure

The pace-of-life syndrome (POLS) hypothesis integrates covariation of life-history traits along a fast-slow continuum and covariation of behavioural traits along a proactive-reactive personality continuum. Few studies have investigated these predicted life-history/personality associations among species and between sexes. Furthermore, whether and how contaminants interfere with POLS patterns remains unexplored. We tested for covariation patterns in life history and in behaviour, and for life-history/personality covariation among species, among individuals within species and between sexes. Moreover, we investigated whether pesticide exposure affects covariation between life history and behaviour and whether species and sexes with a faster POLS strategy have a higher sensitivity to pesticides. We reared larvae of four species of Ischnura damselflies in a common garden experiment with an insecticide treatment (chlorpyrifos absent/present) in the final instar. We measured four life-history traits (larval growth rate during the pesticide treatment, larval development time, adult mass and life span) and two behavioural traits (larval feeding activity and boldness, each before and after the pesticide treatment). At the individual level, life-history traits and behavioural traits aligned along a fast-slow and a proactive-reactive continuum, respectively. Species-specific differences in life history, with fast-lived species having a faster larval growth and development, a lower mass at emergence and a shorter life span, suggested that time constraints in the larval stage were predictably driving life-history evolution both in the larval stage and across metamorphosis in the adult stage. Across species, females were consistently more slow-lived than males, reflecting that a large body size and a long life span are generally more important for females. In contrast to the POLS hypothesis, there was only little evidence for the expected positive coupling between life-history pace and proactivity. Pesticide exposure decreased larval growth rate and affected life-history/personality covariation in the most fast-lived species. Our study supports the existence of life-history and behavioural continua with limited support for life-history/personality covariation. Variation in digestive physiology may explain this decoupling of life history and behaviour and provide valuable mechanistic insights to understand and predict the occurrence of life-history/personality covariation patterns.

Larval UV exposure impairs adult immune function through a trade‐off with larval investment in cuticular melanin

Summary Despite the strong impact of ultraviolet (UV) radiation on invertebrates, it is unknown whether it affects immune function across metamorphosis. More generally, the mechanisms on how larval stressors bridge metamorphosis and shape adult fitness in animals with a complex life cycle remain poorly understood. We studied whether cuticular melanin content is upregulated under UV exposure in the larval stage of the damselfly Coenagrion puella and whether this is traded off across metamorphosis against a key component of the invertebrate immune response, the melanotic encapsulation response, in the adult stage. Larvae exposed to UV increased the melanin content in their exoskeleton and metamorphosed later and at a smaller mass than animals reared without UV. Across metamorphosis, this was associated with a reduced melanotic encapsulation response, thereby constituting the first proof for a UV-driven impaired immune response in an invertebrate. The demonstrated costs of UV exposure in terms of age and mass at metamorphosis and reduced adult immune response likely translate into reduced adult fitness. Path analysis indicated that the immunosuppressive property of larval UV exposure was not mediated by age and mass at metamorphosis, but instead that the adult immune response was traded off against larval cuticular melanin investment. Melanin-based trade-off across metamorphosis provides a new pathway by which effects of larval stressors are carried over to the adult stage and thereby advances our understanding of the still largely enigmatic mechanisms of carryover effects of larval stressors across metamorphosis. Given the mechanistic basis, this carryover effect of larval UV exposure on adult immune function is expected to be general and may constitute a widespread and important cost of UV exposure in invertebrates.

Integrating ecology and evolution in aquatic toxicology: insights from damselflies

Current legislation and ecological risk assessment fails to protect aquatic biodiversity at low levels of contaminants. We addressed 3 topics embedded in general stress ecology and evolutionary ecology that are relevant to arrive at a better evaluation of the risk of low contaminant levels in aquatic systems: 1) delayed effects of contaminants, 2) interactions between contaminants and biotic interactors, and 3) vulnerability to contaminants under global warming. We developed these topics by capitalizing on the key insights obtained using damselflies as model organisms. First, delayed contaminant effects on important fitness-related effects exist during the larval stage and after metamorphosis in the adult stage. Second, synergistic interactions of contaminants with bacteria and predation risk have been demonstrated, and we present advances in the mechanistic understanding of these synergisms with biotic interactors. Third, we illustrate the strength of assessing the effect of contaminants under global warming using a space-for-time substitution approach and the need to consider temperature extremes. These studies using damselflies as model organisms highlight the relevance of considering contaminant effects after the exposure period and in the presence of natural stressors, such as predation risk and higher temperatures. They further highlight the need for spatially explicit risk-assessment and conservation tools. These insights are relevant for most aquatic taxa. Indeed most aquatic taxa have a complex life cycle, are strongly affected by predation risk and by warming, and show latitudinal gradients. Better integration of these topics in ecological risk assessment will be a major challenge for both scientists and policy makers, but of crucial importance to preserve aquatic biodiversity.

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.

Warming increases chlorpyrifos effects on predator but not anti-predator behaviours

Recent insights indicate that negative effects of pesticides on aquatic biota occur at concentrations that current legislation considers environmentally protective. We here address two, potentially interacting, mechanisms that may contribute to the underestimation of the impact of sublethal pesticide effects in single species tests at room temperature: the impairment of predator and antipredator behaviours and the stronger impact of organophosphate pesticides at higher temperatures. To address these issues we assessed the effects of chlorpyrifos on the predator and antipredator behaviours of larvae of the damselfly Ischnura elegans, important intermediate predators in aquatic food webs, in a common-garden warming experiment with replicated low- and high-latitude populations along the latitudinal gradient of this species in Europe. Chlorpyrifos reduced the levels of predator behavioural endpoints, and this reduction was stronger at the higher temperature for head orientations and feeding strikes. Chlorpyrifos also impaired two key antipredator behavioural endpoints, activity reductions in response to predator cues were smaller in the presence of chlorpyrifos, and chlorpyrifos caused a lower escape swimming speed; these effects were independent of temperature. This suggests chlorpyrifos may impact food web interactions by changing predator-prey interactions both with higher (predators) and lower trophic levels (food). Given that only the interaction with the lower trophic level was more impaired at higher temperatures, the overall pesticide-induced changes in food web dynamics may be strongly temperature-dependent. These findings were consistent in damselflies from low- and high-latitude populations, illustrating that thermal adaptation will not mitigate the increased toxicity of pesticides at higher temperatures. Our study not only underscores the relevance of including temperature and prey-predator interactions in ecological risk assessment but also their potential interplay and thereby highlights the complexity of contaminant effects on predator-prey interactions being differentially temperature-dependent pending on the trophic level.

Local adaptation and the potential effects of a contaminant on predator avoidance and antipredator responses under global warming: a space-for-time substitution approach

The ability to deal with temperature‐induced changes in interactions with contaminants and predators under global warming is one of the outstanding, applied evolutionary questions. For this, it is crucial to understand how contaminants will affect activity levels, predator avoidance and antipredator responses under global warming and to what extent gradual thermal evolution may mitigate these effects. Using a space‐for‐time substitution approach, we assessed the potential for gradual thermal evolution shaping activity (mobility and foraging), predator avoidance and antipredator responses when Ischnura elegans damselfly larvae were exposed to zinc in a common‐garden warming experiment at the mean summer water temperatures of shallow water bodies at southern and northern latitudes (24 and 20°C, respectively). Zinc reduced mobility and foraging, predator avoidance and escape swimming speed. Importantly, high‐latitude populations showed stronger zinc‐induced reductions in escape swimming speed at both temperatures, and in activity levels at the high temperature. The latter indicates that local thermal adaptation may strongly change the ecological impact of contaminants under global warming. Our study underscores the critical importance of considering local adaptation along natural gradients when integrating biotic interactions in ecological risk assessment, and the potential of gradual thermal evolution mitigating the effects of warming on the vulnerability to contaminants.

Integrating trait multidimensionality, predation and autotomy to explain the maintenance of boldness

There is an ongoing debate on how personality types are maintained within populations. We tested, for the first time, the potential of trait multidimensionality and trait compensation, where prey compensate for the costs of one trait by relying more on another one, in maintaining variation in boldness within a population. We studied how four boldness-related traits and swimming escape performance covary and shape the probability of survival and autotomy of Ischnura pumilio damselfly larvae in an experiment with predatory dragonfly larvae. Our results did not support the common belief that bold individuals are selected against in terms of survival selection by predation. Instead, we found survival selection favouring individuals combining being bold for two boldness-related traits. The four boldness-related traits did not covary frequently, supporting the multidimensionality of boldness. Moreover, animals bolder for one trait (activity in the presence of predator cues) were shyer for another trait (response to predator cues), which indicated trait compensation. However, the support for trait compensation was limited. The only other case of trait compensation was that bold larvae compensated for their increased risk-taking behaviour in the presence of a predator with a higher probability of autotomy. These patterns may contribute to maintaining variation in boldness in damselfly populations. Just as boldness-related traits are multidimensional, the mechanisms underlying their persistence in natural populations are also likely to be multifaceted.