Habitat isolation and the cues of three remote predators differentially modulate prey colonization dynamics in pond landscapes.

Recent evidence suggests predators may change colonization rates of prey in nearby predator-free patches as an example of context-dependent habitat selection. Such remote predator effects can be positive when colonizers are redirected to nearby patches (habitat compression), or negative when nearby patches are avoided (risk contagion). However, it is unknown to what extent such responses are predator- and prey-specific and change with increasing distance from predator patches. We evaluated how cues of fish, backswimmers and dragonfly larvae affect habitat selection in replicated pond landscapes with predator-free patches located at increasing distances from a predator patch. We found evidence for risk contagion and compression, but spatial colonization patterns were both predator- and prey-specific. The mosquito Culex pipiens and water beetle Hydraena testacea avoided patches next to patches with dragonfly larvae (i.e. risk contagion). Predator-free patches next to patches with backswimmers were avoided only by mosquitoes. Mosquitoes preferentially colonized patches at some distance from a fish or backswimmer patch (i.e. habitat compression). Colonization patterns of beetles also suggested habitat compression, although reward contagion could not be fully excluded as an alternative explanation. Water beetles preferred the most isolated patches regardless of whether predators were present in the landscape, showing that patch position in a landscape alone affects colonization. We conclude that habitat selection can be a complex product of patch isolation and the combined effects of different local and remote cues complicate current attempts to predict the distribution of mobile organisms in landscapes.

Prey colonization in freshwater landscapes can be stimulated or inhibited by the proximity of remote predators.

Recent findings suggest that the colonization of habitat patches may be affected by the quality of surrounding patches. For instance, patches that lack predators may be avoided when located near others with predators, a pattern known as risk contagion. Alternatively, predator avoidance might also redirect dispersal towards nearby predator-free patches resulting in so-called habitat compression. However, it is largely unknown how predators continue to influence these habitat selection behaviours at increasing distances from outside of their own habitat patch. In addition, current information is derived from artificial mesocosm experiments, while support from natural ecosystems is lacking. This study used bromeliad landscapes as a natural model system to study how oviposition habitat selection of Diptera responds to the cues of a distant predator, the carnivorous elephant mosquito larva. We established landscapes containing predator-free bromeliad habitat patches placed at increasing distances from a predator-containing patch, along with replicate control landscapes. These patches were then left to be colonized by ovipositing bromeliad insects. We found that distance to predators modulates habitat selection decisions. Moreover, different dipteran families had different responses suggesting different habitat selection strategies. In some families, predator-free patches at certain distances from the predator patch were avoided, confirming risk contagion. In other families, these patches received higher numbers of colonists providing evidence of predator-induced habitat compression. We confirm that effects of predators in a natural ecosystem can extend beyond the patch in which the predator is present and that the presence or absence of remote predator effects on habitat selection depends on the distance to predators. The notion that perceived habitat quality can depend on conditions in neighbouring patches forces habitat selection studies to adopt a landscape perspective and account for the effects of both present and remote predators when explaining community assembly in metacommunities.

Both local presence and regional distribution of predator cues modulate prey colonisation in pond landscapes.

Recent work on habitat selection has shown that the perceived quality of habitat patches may depend on the quality of adjacent patches. However, it is still unclear how local habitat selection cues can alter distribution patterns in metacommunities at a larger (regional) scale. We studied mosquito oviposition in pond landscapes that differed in the proportion of bad patches with fish predation risk. Our experiment provided conclusive evidence for two local and two regional types of habitat selection. Good patches near bad patches were avoided (local risk contagion) while more distant good patches experienced increased oviposition (regional compression). Oviposition in bad patches increased when located next to good patches (reward contagion) or when there were no good patches regionally present (regional compromise). This complex colonisation behaviour involving compromises at different spatial scales forces experimenters to reconsider the independence of spatial replicates and challenges available theories to predict species distribution patterns.

Species-specific responsiveness of four enzymes to endosulfan and predation risk questions their usefulness as general biomarkers.

General biochemical biomarkers are widely used in current ecotoxicology and may function as early warning signals. We have, however, poor knowledge on how ecologically similar species differ in their biomarker responsiveness and how predation risk may affect these biomarkers, potentially in an interactive way with pesticides. We evaluated this by exposing four corixid water bug species to combinations of endosulfan and predation risk and quantifying the activity of four general enzymatic biomarkers: acetylcholinesterase (AChE), phenoloxidase (PO), catalase (CAT) and superoxidedismutase (SOD). AChE activity was inhibited at an endosulfan concentration of 2 µg l(-1) and this did not differ significantly among species. Predation risk inhibited AChE activity with the same magnitude as endosulfan in one species, S. striata. Reduction in the investment of immune function following pesticide exposure, as measured by the activity of PO, was only observed in C. coleoptrata at 8 µg l(-1) while we observed an increase of PO levels in S. striata. Overall, PO was suppressed under predation risk at 8 µg l(-1) endosulfan. For SOD we observed a pesticide-induced increase across all species under predation risk, while for CAT the pesticide-induced increase was only present without predation risk. These results indicate that even within this group of ecologically similar and closely related species opposing biomarker responses may exist, as observed for PO. Effects of predation risk on all four enzymes, at a similar magnitude as the pesticide effects, further question their usefulness as general biomarkers.

Predator cues magnify effects of the pesticide endosulfan in water bugs in a multi-species test in outdoor containers.

Pesticides have become major stressors in many aquatic communities. Laboratory studies suggest their impact may be further magnified in the presence of cues from predators. Despite their importance for ecological risk assessment, synergisms between pesticides and predator cues have not been confirmed under semi-natural outdoor conditions. We evaluated how the presence of predator cues and the presence of a non-corixid community affect the pesticide sensitivity of five water bug (Corixidae) species in an outdoor, multi-species container experiment. The experiment employed a full factorial design with two pesticide treatments, two predator cue treatments and two (non-corixid) community treatments (absence versus presence of Cloeon dipterum mayfly larvae, Ischnura elegans damselfly larvae and Physa acuta snails). The pesticide treatment negatively affected survival in Cymatia coleoptrata, and to a lesser extent, Sigara lateralis, but not in the other three Corixidae species (Hesperocorixa linnaei, Sigara iactans and Sigara striata). The addition of pesticides did not significantly affect body mass in the latter four species, unless combined with predator cues. To our knowledge this is the first report of this synergism under semi-natural, outdoor conditions. Neither lethal nor sublethal pesticide effects in the Corixidae depended on the community context, yet the presence of the non-corixid community when combined with predator cues reduced survival and body mass. Our results suggest that the here documented synergism between pesticides and predator cues may occur in nature.

Species-specific patterns of swimming escape performance and cholinesterase activity in a guild of aquatic insects exposed to endosulfan.

Next to imposing direct lethal effects, pollutants may also indirectly impose mortality by making prey organisms more vulnerable to predation. We report that four water boatmen species differed strongly in direct endosulfan-imposed mortality, and only the species that suffered highest mortality, Sigara iactans, also showed a reduction in escape swimming speed. While head AChE activity was inhibited in all four species, body ChE was only inhibited in S. iactans where it covaried with escape swimming speed, indicating a mechanistic link between body ChE and swimming speed. Our study underscores the need for risk assessment to consider sublethal pollutant effects, which may considerably affect survival rates under natural conditions, also when testing concentrations of a pesticide that cause direct mortality. Such sublethal effects may generate discrepancies between laboratory and field studies and should be considered when designing safety factors for toxicants where the risk assessment is solely based on LC50 values.