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

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 3 min 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 behavioral 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 behavioral modifications observed in laboratory settings can be used to predict how fish perform in aquatic ecosystems.

Direct and indirect effects of chemical contaminants on the behaviour, ecology and evolution of wildlife

“…Susceptibility differences between species are one of the key challenges in ecotoxicology. For example, studies have shown that small wild-caught prey fish are more sensitive to the anxiolytic effects of the pharmaceutical oxazepam than are larger predatory fish or laboratory-reared fish [5,80,81]. This could be due to species differences in the rate and extent of pharmaceuticals being taken up, metabolized and concentrated.…”

“…Research on chemical contaminants conventionally recorded a limited range of endpoints, most commonly by studying mortality following exposure in the laboratory and/ or by testing the impact of a single contaminant on a single species under standardized laboratory conditions ([4], but see [5]). These approaches are logistically tractable and repeatable but are criticized for their simplicity, particularly when such experiments neither take chemical nor biological complexity into account [6].…”

Urbanization, environment and pharmaceuticals: advancing comparative physiology, pharmacology and toxicology

“…Whether such behavioural observations in these common fish models translate to other less commonly studied fish species ( Saaristo et al , 2017 ; Martin et al , 2017 ) or wild fish responses to neuroactive and other therapeutics or stressors represent important research needs. For example, recent studies have extended laboratory studies with a benzodiazepine (Brodin et al , 2013) to use telemetry to observe fish behaviour in the field following pharmaceutical treatment ( Klaminder et al , 2016 ; Hellström et al , 2016a , b ). Behavioural studies with invertebrates and estuarine and marine species are much less common ( Fong and Ford, 2014 ; Pyle and Ford, 2016 ), yet human populations routinely reside on or immediately upstream from coastlines.…”

Environmentally relevant concentrations of the common anxiolytic pharmaceutical oxazepam do not have acute effect on spawning behavior in mature male Atlantic salmon (Salmo salar) parr

“…concentrations occurring in effluent waters entering natural systems) of one of the most commonly utilized benzodiazepines, oxazepam, have in laboratory assays been shown to affect several behavioral traits in fish, such as activity and risk taking (Brodin, Fick, Jonsson, & Klaminder, ; Klaminder, Jonsson, Fick, Sundelin, & Brodin, ). Further, effects of oxazepam on fish behavior have also been observed in natural lakes (Klaminder et al, ), raising concerns for environmental consequences.…”