Predation risk versus pesticide exposure: effects of fear and loathing on aquatic invertebrates

Aquatic species rely on plastic traits to defend themselves against predators. The induction of these antipredator defences is mediated by water-borne chemical cues. These induced defences have associated costs which can include decreased tolerance to future environmental change such as pesticide contamination. The effects of pesticides in natural systems can be a result not only of their direct toxicity but also of their indirect effects on predator-prey interactions. Despite their relevance for risk assessment, the interactive effects of pesticide contamination and predation stress are poorly understood because the underlying behavioural and physiological mechanisms are largely unstudied. The main objective of this thesis was therefore to assess the toxic effects of imidacloprid, a widely-used insecticide, on different invertebrate species under different levels of predation risk. First, the effects of Imidacloprid on freshwater communities were assessed using field-deployed mesocosms and organism level bioassays. Pulses of environmentally-relevant concentrations of imidacloprid were highly toxic to non-target aquatic insects. Feeding and metabolic responses of a stonefly species Pteronarcys comsctocki, proved to be a good early warning indicator of pesticide detrimental effects. Using a clone of Daphnia magna, the relative importance of alarm cues and fish kairomones (Salmo trutta) were studied as initiators of Daphnia antipredator defences. Although behavioural responses could be triggered by single cues, a combination of alarm cues and predator-specific compounds induced stronger responses and were necessary to induce complete antipredator responses (behavioural, physiological and in the life-history) of daphnids. A combination of both types of chemical cues could thus be used as surrogate for the effects of intimidation posed by predators. Using standardized laboratory toxicological methodologies different responses of D. magna, Chironomus riparius and Sericostoma vittatum d to sublethal concentrations of imidacloprid were assessed under different levels of predation risk. Significant effects of environmentally-relevant concentrations of imidacloprid were observed on insect behaviour and physiology. Higher concentrations of imidacloprid were necessary to elicit effects on D. magna, relative to the other species tested. Considering the ecotoxicological mode of action of imidacloprid and perceived predation risk, the effects of simultaneous exposure to both stressors were assessed using different approaches with additive reference models and analysis of variance. Both stressors acted additively for most responses tested in the different insect species with exposure to sublethal concentrations of imidacloprid also inhibiting antipredator responses with potential negative consequences in terms of mortality from predation in the field. For D. magna, exposure to both stressors showed significant deviations from the reference models results including synergism for same endpoints tested. The results obtained provide insight into the conditions under which interactions between these stressors are likely to occur: invertebrates such as daphnids, midges and caddisflies living under fish predation stress will be more affected by sub-lethal concentrations of Imidacloprid than populations at low predatory pressure. Since predation risk and pesticides can be considered 'similarly-acting' stressors in an ecological sense, studying both types of stress within the same mechanistic framework can be of great value providing compatible data for modelling and allowing improved interpretation of ecological effects of relevant stressors. Esta tese é dedicada ao meu pai porque são dele os valores de humildade e integridade que vou aprendendo a ter como meus, e aos meus filhos, Diogo e Júlia, que todos os dias me relembram que é preciso continuar.