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Lagesson, Annelie
Publications (9 of 9) Show all publications
Saaristo, M., Lagesson, A., Bertram, M. G., Fick, J., Klaminder, J., Johnstone, C. P., . . . Brodin, T. (2019). Behavioural effects of psychoactive pharmaceutical exposure on European perch (Perca fluviatilis) in a multi-stressor environment. Science of the Total Environment, 655, 1311-1320
Open this publication in new window or tab >>Behavioural effects of psychoactive pharmaceutical exposure on European perch (Perca fluviatilis) in a multi-stressor environment
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2019 (English)In: Science of the Total Environment, ISSN 0048-9697, E-ISSN 1879-1026, Vol. 655, p. 1311-1320Article in journal (Refereed) Published
Abstract [en]

With the ability to resist biodegradation and exert therapeutic effects at low concentrations, pharmaceutical contaminants have become environmental stressors for wildlife. One such contaminant is the anxiolytic oxazepam, a psychoactive pharmaceutical that is frequently detected in surface waters globally. Despite growing interest in understanding how wildlife respond to anxiolytics, synergistic effects of pharmaceuticals and other abiotic (e.g. temperature) and biotic (e.g. predation risk) stressors remain unclear. Here, using a multi-stressor approach, we investigated effects of 7-day 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 two temperatures (10 °C and 18 °C), and at two predation risk regimes—generated using chemical cues from the northern pike (Esox lucius). Our exposures resulted in a successful uptake of the drug from the water, i.e., oxazepam was measured in perch muscle tissue at 50 ± 17 ng/g (mean ± SD). We found significant oxazepam-induced effects on boldness, with 76.7% of the treated fish entering the white background (i.e. ‘exposed’ area where exposure to presumed risks are higher) within the first 5 min, compared to 66.6% of the control fish. We also found a significant effect of temperature on total time spent freezing (i.e. staying motionless). Specifically, fish in the low temperature treatments (oxazepam, predation) froze for longer than fish in high temperatures. Our multi-stressor study is the first to uncover how anxiety-related behaviours in wild juvenile fish are altered by changes in water temperature and perceived predation risk. Importantly, our findings highlight the need to focus on multiple stressors to improve understanding of how organisms not only survive, but adapt to, human-induced environmental change.

Place, publisher, year, edition, pages
Elsevier, 2019
Keywords
Anti-predator behaviour, Behavioural ecotoxicology, Oxazepam, Pharmaceuticals, Temperature effect
National Category
Environmental Sciences
Identifiers
urn:nbn:se:umu:diva-155752 (URN)10.1016/j.scitotenv.2018.11.228 (DOI)000455034600127 ()30577123 (PubMedID)
Funder
Swedish Research Council Formas, 2013-4431
Available from: 2019-01-28 Created: 2019-01-28 Last updated: 2020-02-03Bibliographically approved
Lagesson, A., Saaristo, M., Brodin, T., Fick, J., Klaminder, J., Martin, J. M. & Wong, B. B. (2019). Fish on steroids: Temperature-dependent effects of 17 beta-trenbolone on predator escape, boldness, and exploratory behaviors. Environmental Pollution, 245, 243-252
Open this publication in new window or tab >>Fish on steroids: Temperature-dependent effects of 17 beta-trenbolone on predator escape, boldness, and exploratory behaviors
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2019 (English)In: Environmental Pollution, ISSN 0269-7491, E-ISSN 1873-6424, Vol. 245, p. 243-252Article in journal (Refereed) Published
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 MPG of particular concern is 17 beta-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 17 beta-trenbolone on non-reproductive behaviors linked to growth and survival, like boldness and predator avoidance. None consider the interaction between 17 beta-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 (Gambusio holbrooki) were subjected to an environmentally-relevant concentration of 17 beta-trenbolone (average measured concentration 3.0 +/- 0.2 ng/L) or freshwater (i.e. control) for 21 days under one of two temperatures (20 and 30 degrees 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 behavioral effects of trenbolone depended on temperature, sex, or both. Specifically, significant effects of trenbolone on male predator escape behavior were only noted at 30 degrees C, with males becoming less reactive to the simulated threat. Further, in the maze experiment, trenbolone-exposed fish explored the maze faster than control fish, but only at 20 degrees C. We conclude that field detected concentrations of 17 beta-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 behavioral effects of environmental contaminants.

Place, publisher, year, edition, pages
Elsevier, 2019
Keywords
Anti-predator behavior, Behavioral ecoroxicology, Endocrine disrupting chemicals, Synthetic androgenic anabolic steroid, Temperature
National Category
Environmental Sciences Ecology
Identifiers
urn:nbn:se:umu:diva-162768 (URN)10.1016/j.envpol.2018.10.116 (DOI)000457511900026 ()30423539 (PubMedID)
Available from: 2019-09-05 Created: 2019-09-05 Last updated: 2019-09-05Bibliographically approved
Saaristo, M., Lagesson, A., Bertram, M. G., Fick, J., Klaminder, J., Johnstone, C. P., . . . Brodin, T. (2018). 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: 2020-02-03
Lagesson, A. (2018). Fish on drugs: behaviour modifying contaminants in aquatic ecosystems. (Doctoral dissertation). Umeå: Umeå universitet
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
Lagesson, A., Saaristo, M., Brodin, T., Fick, J., Martin, J. M., Klaminder, J. & Wong, B. B. .. (2018). 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
Lagesson, A., Brodin, T., Fahlman, J., Fick, J., Jonsson, M., Persson, J., . . . Klaminder, J. (2018). No evidence of increased growth or mortality in fish exposed to oxazepam in semi-natural ecosystems. Science of the Total Environment, 615, 608-614
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
Brodin, T., Nordling, J., Lagesson, A., Klaminder, J., Hellström, G., Christensen, B. & Fick, J. (2017). Environmental relevant levels of a benzodiazepine (oxazepam) alters important behavioral traits in a common planktivorous fish, (Rutilus rutilus). Journal of Toxicology and Environmental Health, 80(16–18), 963-970
Open this publication in new window or tab >>Environmental relevant levels of a benzodiazepine (oxazepam) alters important behavioral traits in a common planktivorous fish, (Rutilus rutilus)
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2017 (English)In: Journal of Toxicology and Environmental Health, ISSN 1528-7394, E-ISSN 1087-2620, Vol. 80, no 16–18, p. 963-970Article in journal (Refereed) Published
Abstract [en]

Environmental pollution by pharmaceuticals is increasingly recognized as a major threat to aquatic ecosystems worldwide. A complex mix of pharmaceuticals enters waterways via treated wastewater effluent and many remain biochemically active after the drugs reach aquatic systems. However, to date little is known regarding the ecological effects that might arise following pharmaceutical contamination of aquatic environments. One group of particular concern is behaviorally modifying pharmaceuticals as seemingly minor changes in behavior may initiate marked ecological consequences. The aim of this study was to examine the influence of a benzodiazepine anxiolytic drug (oxazepam) on key behavioral traits in wild roach (Rutilus rutilus) at concentrations similar to those encountered in effluent surface waters. Roach exposed to water with high concentrations of oxazepam (280 mu g/L) exhibited increased boldness, while roach at low treatment (0.84 mu g/L) became bolder and more active compared to control fish. Our results reinforce the notion that anxiolytic drugs may be affecting fish behavior in natural systems, emphasizing the need for further research on ecological impacts of pharmaceuticals in aquatic systems and development of new tools to incorporate ecologically relevant behavioral endpoints into ecotoxicological risk assessment.

Place, publisher, year, edition, pages
TAYLOR & FRANCIS INC, 2017
National Category
Environmental Sciences
Identifiers
urn:nbn:se:umu:diva-143173 (URN)10.1080/15287394.2017.1352214 (DOI)000416346600014 ()28829722 (PubMedID)
Available from: 2017-12-19 Created: 2017-12-19 Last updated: 2018-06-09Bibliographically approved
Lagesson, A., Fahlman, J., Brodin, T., Fick, J., Jonsson, M., Byström, P. & Klaminder, J. (2016). Bioaccumulation of five pharmaceuticals at multiple trophic levels in an aquatic food web: Insights from a field experiment. Science of the Total Environment, 568, 208-215
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
Klaminder, J., Hellström, G., Fahlman, J., Jonsson, M., Fick, J., Lagesson, A., . . . Brodin, T. (2016). Drug-Induced Behavioral Changes: Using Laboratory Observations to Predict Field Observations. Frontiers in Environmental Science, 4, Article ID 81.
Open this publication in new window or tab >>Drug-Induced Behavioral Changes: Using Laboratory Observations to Predict Field Observations
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2016 (English)In: Frontiers in Environmental Science, E-ISSN 2296-665X, Vol. 4, article id 81Article in journal (Refereed) Published
Abstract [en]

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. 

Keywords
anxiety, field manipulation, behavior, GABAergic, landscape of fear
National Category
Other Biological Topics Ecology
Identifiers
urn:nbn:se:umu:diva-142369 (URN)10.3389/fenvs.2016.00081 (DOI)
Available from: 2017-11-28 Created: 2017-11-28 Last updated: 2018-10-17Bibliographically approved
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