Food level and sex shape predator-induced physiological stress: immune defence and antioxidant defence.

Despite the potential impact on prey fitness and predator-prey interactions, most studies of predation risk ignore physiological responses and their dependence upon food level and sex. Therefore, we reared male and female larvae of the damselfly Lestes viridis under predator stress (dragonfly larvae) at high and low food levels, and subsequently scored for important variables of insect immune defence (i.e. phenoloxidase) and antioxidant defence [i.e. superoxide dismutase, and catalase (CAT)]. Under predation risk, larvae did not decrease growth rate or immune defence, and only slightly reduced food intake in the high food treatment, probably because of time stress, i.e. little time available to complete the larval development. However, larvae facing predator stress did show an upregulation of antioxidant enzymes. This upregulation was dependent upon food level for CAT and both food level and sex for SOD, consistent with energetic constraints and sex differences in the link between longevity and adult fitness. Our results illustrate that predator stress can influence life history, behavioural and physiological responses differentially and in a context-dependent way. This implies that non-consumptive physiological effects of predators on their prey show independent yet similar complexities in behavioural and life history response variables. In general, our results advocate that mechanistic studies on predator-prey interactions may benefit from including physiological variables.

Autotomy reduces immune function and antioxidant defence.

Costs of autotomy, an antipredator defence, are typically explained by impaired mobility; yet physiologically mediated costs may also play a role. Given the resemblance to wounding, a decreased immune function and an associated reduction in antioxidant defence is expected after autotomy. In line with this, after lamellae autotomy, larvae of the damselfly Lestes viridis showed lower levels of innate immunity (i.e. phenoloxidase, PO) and antioxidant defence (superoxide dismutase, SOD). Levels of catalase (CAT) remained, however, unaffected. In line with its cytotoxicity, PO covaried positively with CAT, yet negatively with SOD. We identified a novel cost of autotomy in terms of a reduced innate immunity, which may provide an alternative explanation for the often observed costs of autotomy and which may generate indirect interactions between predators and parasites.

Sublethal pesticide concentrations and predation jointly shape life history: behavioral and physiological mechanisms.

Despite their relevance for risk assessment, the interactive effects of pesticide and predation cues are poorly understood because the underlying behavioral and physiological mechanisms are largely unknown. To explore these mechanisms, we reared larvae of the damselfly Coenagrion puella at three different predation risk levels and a range of environmentally realistic concentrations of three pesticides used worldwide (atrazine, carbaryl, and endosulfan). We compared key development responses (growth rate, developmental time, and final size) against food ingestion, assimilation, and conversion efficiency, and acetylcholinesterase (AChE) activity. Predation risk impaired all endpoints, including AChE activity, while the effects of pesticide stress were smaller for atrazine and endosulfan and absent for carbaryl. The effects of both stressors and their interaction on life history were mostly indirect through resource acquisition and energy allocation. Compensatory physiological mechanisms to pesticide stress (atrazine and endosulfan) were present in larvae reared in the absence of predation stress but were offset under predation stress. As a result, smaller size (atrazine and endosulfan) and lower growth rate (endosulfan) from pesticide stress were only found in the highest predation risk treatment. Our results provide insight as to the conditions under which interactions between stressors are likely to occur: damselfly populations at high density and living in fish ponds will be more affected by pesticides than populations at low densities in fishless ponds. By identifying variables that may shape the interaction between predation stress and other stressors such as pesticides, our mechanistic approach may help to bridge the gap between laboratory and field studies.

Time constraints mediate predator-induced plasticity in immune function, condition, and life history.

The simultaneous presence of predators and a limited time for development imposes a conflict: accelerating growth under time constraints comes at the cost of higher predation risk mediated by increased foraging. The few studies that have addressed this tradeoff have dealt only with life history traits such as age and size at maturity. Physiological traits have largely been ignored in studies assessing the impact of environmental stressors, and it is largely unknown whether they respond independently of life history traits. Here, we studied the simultaneous effects of time constraints, i.e., as imposed by seasonality, and predation risk on immune defense, energy storage, and life history in lestid damselflies. As predicted by theory, larvae accelerated growth and development under time constraints while the opposite occurred under predation risk. The activity of phenoloxidase, an important component of insect immunity, and investment in fat storage were reduced both under time constraints and in the presence of predators. These reductions were smaller when time constraints and predation risk were combined. This indicates that predators can induce sublethal costs linked to both life history and physiology in their prey, and that time constraints can independently reduce the impact of predator-induced changes in life history and physiology.