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Fish on drugs: behaviour modifying contaminants in aquatic ecosystems
Umeå University, Faculty of Science and Technology, Department of Ecology and Environmental Sciences.
2018 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

Contamination of surface waters is a worldwide problem. One group of emerging contaminants that reach aquatic ecosystems via sewage treatment plant effluents and agricultural run-offs is pharmaceuticals. Impacts of pharmaceuticals on the behaviour of aquatic organisms can have important ecological and evolutionary consequences because behaviour is directly linked to fitness. The aim of my doctoral thesis was to increase our understanding of the fate and effects of behaviour modifying drugs in aquatic ecosystems.

While studying an aquatic ecosystem spiked with pharmaceuticals, I found that the benthic species at the bottom of the food chain were the main receivers (highest bioaccumulation factor; BAF) while fish at the top of the food web had the lowest uptake of the studied drugs. Interestingly, the BAF of the anxiolytic pharmaceutical oxazepam, increased in fish (perch; Perca fluviatilis) over the study period, suggesting that this drug can be transferred between trophic levels in food webs. To assess whether oxazepam could affect growth and survival in perch, I exposed perch populations to oxazepam for 2-months in a replicated pond experiment. In this study, I tested the hypothesis that oxazepam exposed perch would grow faster but also suffer from increased predation. Oxazepam has been shown previously to induce ‘anti-anxiety’ behaviours that improve foraging but may also make individuals more exposed to predators. In contrast, I found no statistically significant increase in growth and mortality in the exposed perch. However, the study revealed that the natural predator of perch (pike; Esox lucius) became less effective at catching prey when exposed to oxazepam. This exposure effect on predation efficiency likely contributed to the absence of predation effects in the exposed ponds. In two following laboratory studies I investigated effects of behaviour modifying drugs (oxazepam and a growth hormone, 17β-trenbolone) in combination with additional stressors (temperature and predator cues). Drug and temperature interactions were found for 17β-trenbolone, where water temperature interacted with treatment to induce changes in predator escape behaviour, boldness, and exploration in mosquitofish (Gambusia holbrooki). However, in the other study, we found that oxazepam, temperature, and predator cue all affected perch ‘anti-anxiety’ behaviours, but independently.

I conclude that pharmaceuticals can alter ecologically important behaviours in fish, and that at least some, can accumulate in aquatic food webs. It seems that in situ effects of behaviour modifying drugs in aquatic ecosystems depend on both species-specific responses and abiotic interactions. As such, it is far from straightforward to predict net ecosystem effects based on experiments conducted using single species and static conditions. Future studies should assess the effects of pharmaceuticals in aquatic ecosystems under more complex conditions for us to gain a better understanding of what consequences behaviour modifying drugs have in the environment.

Place, publisher, year, edition, pages
Umeå: Umeå universitet , 2018. , p. 33
Keywords [en]
Aquatic ecosystems, Behavioural effects, Ecotoxicology, Endocrine disruptors, Pharmaceuticals, Interaction effects
National Category
Environmental Sciences
Research subject
Ecotoxicology
Identifiers
URN: urn:nbn:se:umu:diva-151138ISBN: 978-91-7601-912-2 (print)OAI: oai:DiVA.org:umu-151138DiVA, id: diva2:1242471
Public defence
2018-09-21, Lilla Hörsalen, KB.E3.01, KBC-huset, Umeå, 12:00 (English)
Opponent
Supervisors
Available from: 2018-08-31 Created: 2018-08-28 Last updated: 2018-08-30Bibliographically approved
List of papers
1. Bioaccumulation of five pharmaceuticals at multiple trophic levels in an aquatic food web: Insights from a field experiment
Open this publication in new window or tab >>Bioaccumulation of five pharmaceuticals at multiple trophic levels in an aquatic food web: Insights from a field experiment
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2016 (English)In: Science of the Total Environment, ISSN 0048-9697, E-ISSN 1879-1026, Vol. 568, p. 208-215Article in journal (Refereed) Published
Abstract [en]

Pharmaceuticals derived from manufacturing and human consumption contaminate surface waters worldwide. To what extent such pharmaceutical contamination accumulates and disperses over time in different compartments of aquatic food webs is not well known. In this study we assess to what extent five pharmaceuticals (diphenhydramine, oxazepam, trimethoprim, diclofenac, and hydroxyzine) are taken up by fish (European perch) and four aquatic invertebrate taxa (damselfly larvae, mayfly larvae, waterlouse, and ramshorn snail), by tracing their bioconcentrations over several months in a semi-natural large-scale (pond) system. The results suggest both significant differences among drugs in their capacity to bioaccumulate and differences among species in uptake. While no support for in situ uptake of diclofenac and trimethoprim was found, oxazepam, diphenhydramine, and hydroxyzine were detected in all analyzed species. Here, the highest bioaccumulation factor (tissue:water ratio) was found for hydroxyzine. In the food web, the highest concentrations were found in the benthic species ramshorn snail and waterlouse, indicating that bottom-living organism at lower trophic positions are the prime receivers of the pharmaceuticals. In general, concentrations in the biota decreased over time in response to decreasing water concentrations. However, two interesting exceptions to this trend were noted. First, mayfly larvae (primarily grazers) showed peak concentrations (a fourfold increase) of oxazepam, diphenhydramine, and hydroxyzine about 30 days after initial addition of pharmaceuticals. Second, perch (top-predator) showed an increase in concentrations of oxazepam throughout the study period. Our results show that drugs can remain bioavailable for aquatic organism for long time periods (weeks to months) and even re-enter the food web at a later time. As such, for an understanding of accumulation and dispersion of pharmaceuticals in aquatic food webs, detailed ecological knowledge is required.

Keywords
Diclofenac, Hydroxyzine, Oxazepam, Risk assessment, Trophic transfer
National Category
Environmental Sciences
Identifiers
urn:nbn:se:umu:diva-125965 (URN)10.1016/j.scitotenv.2016.05.206 (DOI)000382258300024 ()27295593 (PubMedID)2-s2.0-84973358615 (Scopus ID)
Available from: 2016-10-17 Created: 2016-09-23 Last updated: 2018-08-28Bibliographically approved
2. No evidence of increased growth or mortality in fish exposed to oxazepam in semi-natural ecosystems
Open this publication in new window or tab >>No evidence of increased growth or mortality in fish exposed to oxazepam in semi-natural ecosystems
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2018 (English)In: Science of the Total Environment, ISSN 0048-9697, E-ISSN 1879-1026, Vol. 615, p. 608-614Article in journal (Refereed) Published
Abstract [en]

An increasing number of short-term laboratory studies on fish reports behavioral effects from exposure to aquatic contaminants or raised carbon dioxide levels affecting the GABAAreceptor. However, how such GABAergic behavioral modifications (GBMs) impact populations in more complex natural systems is not known. In this study, we induced GBMs in European perch (Perca fluviatilis) via exposure to a GABA agonist (oxazepam) and followed the effects on growth and survival over one summer (70 days) in replicated pond ecosystems. We hypothesized that anticipated GBMs, expressed as anti-anxiety like behaviors (higher activity and boldness levels), that increase feeding rates in laboratory assays, would; i) increase growth and ii) increase mortality from predation. To test our hypotheses, 480 PIT tagged perch of known individual weights, and 12 predators (northern pike, Esox lucius) were evenly distributed in 12 ponds; six control (no oxazepam) and six spiked (15.5 ± 4 μg l− 1 oxazepam [mean ± 1 S.E.]) ponds. Contrary to our hypotheses, even though perch grew on average 16% more when exposed to oxazepam, we found no significant difference between exposed and control fish in growth (exposed: 3.9 ± 1.2 g, control: 2.9 ± 1 g [mean ± 1 S.E.], respectively) or mortality (exposed: 26.5 ± 1.8 individuals pond− 1, control: 24.5 ± 2.6 individuals pond− 1, respectively). In addition, we show that reduced prey capture efficiency in exposed pike may explain the lack of significant differences in predation. Hence, our results suggest that GBMs, which in laboratory studies impact fish behavior, and subsequently also feeding rates, do not seem to generate strong effects on growth and predation-risk in more complex and resource limited natural environments.

Place, publisher, year, edition, pages
Elsevier, 2018
Keywords
GABA(A), Behavioral modifications, Ecological effects, Perca fluviatilis, Esox lucius
National Category
Environmental Sciences
Identifiers
urn:nbn:se:umu:diva-142442 (URN)10.1016/j.scitotenv.2017.09.070 (DOI)000414922600066 ()28988097 (PubMedID)
Available from: 2017-12-05 Created: 2017-12-05 Last updated: 2018-08-28Bibliographically approved
3. Behavioural effects of temperature, predation-risk and anxiolytic exposure on the European perch (Perca fluviatilis)
Open this publication in new window or tab >>Behavioural effects of temperature, predation-risk and anxiolytic exposure on the European perch (Perca fluviatilis)
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2018 (English)Manuscript (preprint) (Other academic)
Abstract [en]

With the ability to resist biodegradation and exert therapeutic effects at low concentrations, emerging contaminants have become environmental stressors for wildlife. One such contaminant is the anxiolytic oxazepam, a psychoactive pharmaceutical which is frequently detected in surface waters globally. Despite the growing interest in understanding how wildlife responds to such contaminants, the synergistic fitness effects of pharmaceuticals and increased variability in temperature remain unclear. Here, by using a multi-stressor approach, we investigated the effects of 7-d oxazepam exposure (6.5 μg/L) on anxiety-related behaviours in juvenile European perch (Perca fluviatilis). The multi-stressor approach was achieved by exposing perch to oxazepam at either low (10°C) or high (18°C) temperature, with or without a predation cue, generating 8 treatments. Our exposures resulted in a successful uptake of the drug from the water, i.e. oxazepam was measured at muscle tissue concentrations around 50 ± 17 ng/g (mean ± SD). We found significant effects on boldness induced by the studied drug: 92.8% of the fish in the 'oxazepam and predation and high temperature' treatment entered the white background (representing a novel area where exposure to presumed risks are higher) within the first 5 min, compared to 79.3% of the 'control and predation and high temperature' fish. We also found a significant effect on temperature on the total time freezing (i.e. staying motionless). Specifically, fish in the low temperature treatments (oxazepam, predation and control) froze for longer than fish in the high temperatures, respectively. Our study is the first to show altered anxiety-related behaviours in a native juvenile fish resulting from oxazepam, predation and high temperature. As adaptation to a range of biotic and abiotic pressures is essential to living organisms, our study highlights the need to focus on multiple stressors to improve understanding of how organisms not only survive, but adapt to human-induced environmental change.

Keywords
Behavioural ecotoxicology, Benzodiazepines, Freshwater fish, Multiple stressors, Scototaxis
National Category
Environmental Sciences
Research subject
Ecotoxicology
Identifiers
urn:nbn:se:umu:diva-151126 (URN)
Available from: 2018-08-28 Created: 2018-08-28 Last updated: 2018-08-28
4. Fish on steroids: Temperature dependent effects of 17β-trenbolone on anti-predator, risk-taking and exploratory behaviours
Open this publication in new window or tab >>Fish on steroids: Temperature dependent effects of 17β-trenbolone on anti-predator, risk-taking and exploratory behaviours
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2018 (English)In: Article in journal (Other academic) Submitted
Abstract [en]

Hormonal growth promoters (HGPs), widely used in beef cattle production globally, make their way into the environment as agricultural effluent—with potential impacts on aquatic ecosystems. One HPG of particular concern is 17β-trenbolone, which is persistent in freshwater habitats and can affect the development, morphology and reproductive behaviors of aquatic organisms. Despite this, few studies have investigated impacts of 17β-trenbolone on non-reproductive behaviors linked to growth and survival, like boldness and predator avoidance. None consider the interaction between 17β-trenbolone and other environmental stressors, such as temperature, although environmental challenges confronting animals in the wild seldom, if ever, occur in isolation. Accordingly, this study aimed to test the interactive effects of trenbolone and temperature on organismal behavior. To do this, eastern mosquitofish (Gambusia holbrooki) were subjected to an environmentally-relevant concentration of 17β-trenbolone (≤ 5.1 ± 0.5 ng/L) or freshwater (i.e. control) for 21 days under one of two temperatures (20 and 30°C), after which the predator escape, boldness and exploration behavior of fish were tested. Predator escape behavior was assayed by subjecting fish to a simulated predator strike, while boldness and exploration were assessed in a separate maze experiment. We found that trenbolone exposure increased boldness behavior. Interestingly, some behavioural effects of trenbolone depended on temperature, sex, or both. Specifically, significant effects of trenbolone on male predator escape behavior were only noted at 30°C, with males becoming less reactive to the simulated threat. Further, in the maze experiment, trenbolone-exposed fish had a higher activity and explored the maze faster than control fish, but only at 20°C. We conclude that field detected concentrations of 17β-trenbolone can impact ecologically important behaviors of fish, and such effects can be temperature dependent. Such findings underscore the importance of considering the potentially interactive effects of other environmental stressors when investigating behavioural effects of environmental contaminants.

Keywords
Anti-predator behavior, Behavioural ecotoxicology, Endocrine disrupting chemicals, Synthetic androgenic anabolic steroid, Temperature
National Category
Environmental Sciences
Research subject
Ecotoxicology
Identifiers
urn:nbn:se:umu:diva-151136 (URN)
Available from: 2018-08-28 Created: 2018-08-28 Last updated: 2018-08-28

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Lagesson, Annelie

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