Drug-Induced Behavioral Changes: Using Laboratory Observations to Predict Field Observations

Jonatan Klaminder,Johan Fahlman,Jerker Fick,Gustav Hellström,Micael Jonsson,Tomas Brodin,Eva Bergman,Annelie Lagesson

doi:10.3389/fenvs.2016.00081

Jonatan Klaminder, Johan Fahlman + Show 6 more

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https://doi.org/10.3389/fenvs.2016.00081

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Abstract

Behavioral assays constitute important research tools when assessing how fish respond to environmental change. However, it is unclear how behavioral modifications recorded in laboratory assays are expressed in natural ecosystems, a limitation that makes it difficult to evaluate the predictive power of laboratory-based measurements. In this study, we hypothesized that exposure to a benzodiazepine (i.e., oxazepam) increases boldness and activity in laboratory assays as well as in field assays – that is, laboratory results can be used to predict field results. Moreover, we expected the modified behavior to affect other important ecological measures such as habitat selection and home range. To test our hypothesis, we exposed European perch (Perca fluviatilis) to oxazepam and measured subsequent changes in behavioral trials both in laboratory assays and in a lake ecosystem populated with a predatory fish species, pike (Esox lucius). In the lake, the positions of both perch and pike were tracked every three minutes for a month using acoustic telemetry. In the laboratory assay, the oxazepam-exposed perch were bolder and more active than the non-exposed perch. In the lake assay, the oxazepam-exposed perch were also more bold and active, had a larger home range, and used pelagic habitats more than the non-exposed perch. We conclude that ecotoxicological behavioral assays are useful for predicting the effects of exposure in natural systems. However, although individual responses to exposure were similar in both the laboratory and field trials, effects were more obvious in the field study, mainly due to reduced variability in the behavior measures from the lake. Hence, short-term behavioral assays may fail to detect all the effects expressed in natural environments. Nevertheless, our study clearly demonstrates that behavior modifications observed in laboratory settings can be used to predict how fish perform in aquatic ecosystems.

Highlights

Laboratory behavioral assays where behavioral traits are recognized as sensitive endpoints for assessing how fish respond to changes in water chemistry are becoming important tools in modern ecotoxicology (Jones and Reynolds, 1997; Scott and Sloman, 2004; Melvin and Wilson, 2013; Brodin et al, 2014)
As it has previously been shown that oxazepam increases boldness and activity in perch (Brodin et al, 2013, 2014; Klaminder et al, 2014), a directional hypothesis, and a one-tailed test (i.e., α = 0.1), justified the significance of the induced behavioral modifications
We show that the more active and exploratory behavior of fish exposed to oxazepam shown in laboratory experiments (Brodin et al, 2013; Klaminder et al, 2014) holds true in a natural lake ecosystem; our main hypothesis appears valid as behavioral traits, or even changes in trait expressions, in the wild can be predicted from laboratory assays

Summary

Introduction

Laboratory behavioral assays where behavioral traits are recognized as sensitive endpoints for assessing how fish respond to changes in water chemistry are becoming important tools in modern ecotoxicology (Jones and Reynolds, 1997; Scott and Sloman, 2004; Melvin and Wilson, 2013; Brodin et al, 2014). Recent studies have shown that ecologically important behavioral traits, such as activity. Largescale field studies that verify contamination-induced behavioral modifications are needed (Atchison et al, 1987). Behavioral traits observed in laboratory settings may be used to predict ecological and evolutionary consequences in natural settings (Réale et al, 2007), studies supporting this theory are largely based on short-term laboratory assays and field verifications are scarce (Conrad et al, 2011). Whole-lake experiments using fish of different origins (domestic and wild) have shown that active and bold fish (domestic) occupy more risky habitats and grow faster, these fish suffer from higher predation losses, findings that are in line with behavioral theory (Biro et al, 2004, 2006)

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