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Bioaccumulation of five pharmaceuticals at multiple trophic levels in an aquatic food web: Insights from a field experiment
Umeå University, Faculty of Science and Technology, Department of Ecology and Environmental Sciences.
Umeå University, Faculty of Science and Technology, Department of Ecology and Environmental Sciences.
Umeå University, Faculty of Science and Technology, Department of Ecology and Environmental Sciences.
Umeå University, Faculty of Science and Technology, Department of Chemistry.ORCID iD: 0000-0002-3949-7371
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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.

Place, publisher, year, edition, pages
Elsevier, 2016. Vol. 568, p. 208-215
Keywords [en]
Diclofenac, Hydroxyzine, Oxazepam, Risk assessment, Trophic transfer
National Category
Environmental Sciences
Identifiers
URN: urn:nbn:se:umu:diva-125965DOI: 10.1016/j.scitotenv.2016.05.206ISI: 000382258300024PubMedID: 27295593Scopus ID: 2-s2.0-84973358615OAI: oai:DiVA.org:umu-125965DiVA, id: diva2:1037670
Available from: 2016-10-17 Created: 2016-09-23 Last updated: 2024-07-23Bibliographically approved
In thesis
1. Fish on drugs: behaviour modifying contaminants in aquatic ecosystems
Open this publication in new window or tab >>Fish on drugs: behaviour modifying contaminants in aquatic ecosystems
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
Aquatic ecosystems, Behavioural effects, Ecotoxicology, Endocrine disruptors, Pharmaceuticals, Interaction effects
National Category
Environmental Sciences
Research subject
Ecotoxicology
Identifiers
urn:nbn:se:umu:diva-151138 (URN)978-91-7601-912-2 (ISBN)
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
2. The fate and effect of pharmaceuticals in boreal surface waters
Open this publication in new window or tab >>The fate and effect of pharmaceuticals in boreal surface waters
2020 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

Traces of pharmaceuticals are often found in streams, rivers, and lakes as the result of effluent water discharge. This dissertation aims to create a better understanding of the fate of drugs in aquatic ecosystems and how oxazepam, an anxiolytic pharmaceutical commonly detected in surface waters, affects the behavior of perch (Perca fluviatilis). To address these issues, I used a series of large-scale field experiments to evaluate predictions made in controlled laboratory experiments. My dissertation shows that small-scale incubations commonly used to assess the persistence of pharmaceuticals (trimethoprim, diclofenac, hydroxyzine, diphenhydramine and oxazepam) in aquatic environments effectively predicts the fate of dissolved drugs in freshwater during the first week of contamination. However, these experiments and the conceptual models failed to predict that pharmaceuticals can remain dissolved in freshwater for months. In addition, the results suggest that the drugs remain bioactive for months and that the uptake of different drugs varied widely between trophic levels. For example, benthic species generally had a higher affinity to accumulate the studied drugs than species in higher trophic levels; however, the anxiolytic drug oxazepam was found in perch. To test the effect of oxazepam on perch behavior, I used acoustic telemetry to track the perch in situ (i.e., in the ponds). The in situ behavior of perch correlated with laboratory behavior when findings from several trials were merged into multidimensional behavioral profiles of the studied individuals, although oxazepam did not conclusively affect perch behavior in line with earlier theories, when though concentrations were much higher than concentrations measured in any contaminated environments. I conclude that simplified laboratory experiments have some predictive power regarding the fate and effects of pharmaceuticals in complex natural ecosystems, but laboratory environments may underestimate persistence of drugs in aquatic ecosystems and fail to detect important social drivers of animal behavior in natural settings.

Place, publisher, year, edition, pages
Umeå: Umeå Universitet, 2020. p. 29
Keywords
Aquatic ecosystems, behavioural effects, ecotoxicology, acoustic telemetry, field verification, social network
National Category
Environmental Sciences
Research subject
Ecotoxicology; environmental science
Identifiers
urn:nbn:se:umu:diva-174090 (URN)978-91-7855-319-8 (ISBN)978-91-7855-318-1 (ISBN)
Public defence
2020-09-11, Triple Helix, Umeå, 10:00 (English)
Opponent
Supervisors
Funder
Knut and Alice Wallenberg Foundation
Available from: 2020-08-21 Created: 2020-08-17 Last updated: 2020-10-20Bibliographically approved

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Lagesson, AnnelieFahlman, JohanBrodin, TomasFick, JerkerJonsson, MicaelByström, PärKlaminder, Jonatan

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