To examine whether natural stressors like predation risk affect responses to anthropogenic contaminants, we exposed nauplii of the copepod Tigriopus brevicornis to chemical cues from fish (kairomones) and copper (Cu). We tested effects of these treatments, singly and combined, on copepod age and size at maturity, and development stage sensitivity, while controlling for effects of genetic heterogeneity (clutch identity). Predation risk, Cu and clutch identity interacted in their effect on development time. Predation risk alone had minor effects, but potentiated Cu toxicity in the combined treatment by doubling the delay in age at maturity, as compared to Cu exposure alone. This potentiating effect on developmental delay appeared already at the first copepodite stage. The specific strength of response varied among nauplii from different females' clutches. There were no differences in copepod size at maturity among treatments. We did, however, find an interaction between the effect of Cu and clutch identity on copepod growth. Our results demonstrate the importance of ecological interactions for potentiating the toxicity of environmental contaminants. We also demonstrate the need to consider genetic heterogeneity in ecotoxicology. Natural variation in stressor responses has implications for the interpretation of results from toxicological studies using single-clone or inbred culture populations.
Natural biotic and anthropogenic stressors can interact to alter contaminant toxicity. Energetic restrictions are potential mechanisms causing this pattern. To identify processes underlying observed effects of predation risk and copper (Cu) on delayed copepod age at maturity, we examined how these 2 stressors affect respiration rates. We tested 2 very different copepod species: the large, pelagic calanoid Calanus finmarchicus and the small, semibenthic harpacticoid Tigriopus brevicornis. Adult individuals were exposed for 12 h to the treatments: predation risk, Cu (23 µg L−1), combined predation risk and Cu (23 µg L−1), or control. Oxygen concentrations were monitored continuously. The 2 species differed in their responses. We found no clear effects of either stressor in C. finmarchicus. In T. brevicornis, predation risk increased respiration rates, whereas Cu alone had little impact. In contrast, combined exposure to predation risk and Cu interacted to reduce respiration rates to less than expected. We further observed an effect of sex because female‐biased T. brevicornis replicates were more sensitive to both predation risk (increased respiration rates) and Cu exposure (reduced respiration rates). The present study provides further evidence that predation risk can interact with copepod responses toward Cu exposure. Interactive effects of biotic stressors ought to be considered to improve future marine environmental monitoring. Environ Toxicol Chem 2020;39:1765–1773. © 2020 The Authors. Environmental Toxicology and Chemistry published by Wiley Periodicals LLC on behalf of SETAC.
Individual trait variation is essential for populations to cope with multiple stressors and continuously changing environments. The immense number of possible stressor combinations and the influence of phenotypic variation makes experimental testing for effects on organisms challenging. The acquisition of such data requires many replicates and is notoriously laborious. It is further complicated when responses occur over short time periods. To overcome such challenges, we developed an automated imaging platform to acquire temporally highly resolved individual data. We tested this platform by exposing copepods to a combination of a biotic stressor (predator cues) and a toxicant (copper) and measured the growth response of individual copepods. We tested the automatically acquired data against published manually acquired data with much lower temporal resolution. We find the same general potentiating effects of predator cues on the adverse effects of copper, and the influence of an individual’s clutch identity on its ability to resist stress, between the data obtained from low and high temporal resolution. However, when using the high temporal resolution, we also uncovered effects of clutch ID on the timing and duration of stage transitions, which highlights the importance of considering phenotypic variation in ecotoxicological testing. Phenotypic variation is usually not acknowledged in ecotoxicological testing. Our approach is scalable, affordable, and adjustable to accommodate both aquatic and terrestrial organisms, and a wide range of visually detectable endpoints. We discuss future extensions that would further widen its applicability.
In ecotoxicology and aquatic ecology, we often ignore responses of individuals and focus on average responses. However, both terrestrial and aquatic animals display consistent behavioral differences between individuals. The distribution of behavioral differences within a population contains vital information for predicting population responses to novel environmental challenges. Currently, individual data for behavioral and physiological traits of small marine invertebrates are few, partly because such variation is lost within published group means and assumed normality. We tested the combined effects of an inorganic contaminant (copper) and a biological stressor (i.e., chemical cues of a fish predator) on activity in a marine copepod. Although direct stress effects were weak, individuals behaved consistently differently, depending on the context. Individual differences in behavior were only expressed under the influence of kairomones, but not by copper exposure alone. This finding indicates that copepods express repeatable and context‐dependent behavior. We also demonstrate how large variations in behavioral data can hide consistent differences between individuals. Environ Toxicol Chem 2020;39:1017–1026. © 2020 The Authors. Environmental Toxicology and Chemistry published by Wiley Periodicals, Inc. on behalf of SETAC.
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