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  • 1.
    Höglund, Erik
    et al.
    Norsk Inst Vannforskning, Niva, Gaustadalleen 21, NO-0349 Oslo, Norway;Univ Agder, Ctr Coastal Res, Kristiansand, Norway.
    Moltesen, Maria
    Danish Tech Univ, Inst Aquat Resources, Sect Aquaculture, POB 101, DK-9850 Hirtshals, Denmark;Univ Copenhagen, Dept Biol, Sect Ecol & Evolut, Univ Pk 15,Bldg 3,4th Floor, DK-2100 Copenhagen O, Denmark.
    Castanheira, Maria Filipa
    Univ Algarve, CCMAR, Fish Ethol & Welf Grp, Campus Gambelas, P-8005139 Faro, Portugal.
    Thörnqvist, Per-Ove
    Uppsala University, Disciplinary Domain of Medicine and Pharmacy, Faculty of Medicine, Department of Neuroscience, Winberg: Behavioral Neuroendocrinology.
    Silva, Patricia I. M.
    Danish Tech Univ, Inst Aquat Resources, Sect Aquaculture, POB 101, DK-9850 Hirtshals, Denmark;Univ Copenhagen, Dept Biol, Sect Ecol & Evolut, Univ Pk 15,Bldg 3,4th Floor, DK-2100 Copenhagen O, Denmark;Norwegian Univ Life Sci, Dept Anim & Aquacultural Sci, POB 5003, N-1432 As, Norway.
    Overli, Oyvind
    Norwegian Univ Life Sci, Dept Food Safety & Infect Biol, N-0454 Oslo, Norway.
    Martins, Catarina
    Univ Algarve, CCMAR, Fish Ethol & Welf Grp, Campus Gambelas, P-8005139 Faro, Portugal;Mowi, 4102 Sandviken,POB 5835, Bergen, Norway.
    Winberg, Svante
    Uppsala University, Disciplinary Domain of Medicine and Pharmacy, Faculty of Medicine, Department of Neuroscience, Winberg: Behavioral Neuroendocrinology.
    Contrasting neurochemical and behavioral profiles reflects stress coping styles but not stress responsiveness in farmed gilthead seabream (Sparus aurata)2020In: Physiology and Behavior, ISSN 0031-9384, E-ISSN 1873-507X, Vol. 214, article id 112759Article in journal (Refereed)
    Abstract [en]

    In fish, as well as in other vertebrates, contrasting suites of physiological and behavioral traits, or coping styles, are often shown in response to stressors. However, the magnitude of the response (i.e. stress responsiveness) has been suggested to be independent of stress coping style. One central neurotransmitter that has been associated with both stress responsiveness and differences in stress coping styles is serotonin (5-hydroxytryptamine, 5-HT). In this study, we investigated to what extent stress responsiveness reflects differences in stress coping, and the potential involvement of the 5-HT system in mediating such differences in farmed Gilthead seabream. Initially, fish were classified as proactive or reactive based on their behavioural response to net restraint. Following 1.5 months, fish classified as proactive still showed a higher number of escape attempts and spent longer time escaping than those classified as reactive. These differences were reflected in a generally higher brain stem 5-HT concentration and a lower telencephalic 5-HT activity, i.e. the ratio of 5-hydroxyindoleacetic acid (5-HIAA) to 5-HT, in proactive fish. Independent of stress coping styles, stress responsiveness was reflected in elevated 5-HIAA concentrations and 5-HIAA/5-HT ratios in telencephalon and brain stem together with increased plasma cortisol concentrations at 0.5 and 2 h following the last net restraint. The current results show that 5-HT signaling can reflect different behavioural output to a challenge which are independent of neuroendocrine responses to stress and lend support to the hypothesis that stress coping styles can be independent of stress responsiveness.

  • 2.
    Mustafa, Arshi
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology. Uppsala University, Disciplinary Domain of Medicine and Pharmacy, Faculty of Medicine, Department of Neuroscience, Winberg: Behavioral Neuroendocrinology.
    Roman, Erika
    Uppsala University, Disciplinary Domain of Medicine and Pharmacy, Faculty of Pharmacy, Department of Pharmaceutical Biosciences. Swedish Univ Agr Sci, Div Anat & Physiol, Dept Anat Physiol & Biochem, Uppsala, Sweden.
    Winberg, Svante
    Uppsala University, Disciplinary Domain of Medicine and Pharmacy, Faculty of Medicine, Department of Neuroscience, Winberg: Behavioral Neuroendocrinology.
    Boldness in Male and Female Zebrafish (Danio rerio) Is Dependent on Strain and Test2019In: Frontiers in Behavioral Neuroscience, ISSN 1662-5153, E-ISSN 1662-5153, Vol. 13, article id 248Article in journal (Refereed)
    Abstract [en]

    Differences in selection pressure in nature and labs have profound effects on zebrafish strains. The widely used AB strain of zebrafish has been domesticated over several decades. Recently, there has been an upsurge in the availability of genetically modified lines, e.g., the spiegeldanio (spd), which has a mutation in the fibroblast growth factor receptor 1a (fgfr1a) gene. This mutant strain (fgfr1a) has previously been reported to be bolder than fish of the Tubingen strain, from which it was generated. Our knowledge on behavioral differences between different zebrafish strains, relative to wild-caught zebrafish, is limited. In the present study we compare behaviors related to interpretation of boldness in male and female offspring (F1) of wild-caught fish, AB and fgfr1a(-/-) zebrafish. A second aim of the study was to compare the behavior of fish from these strains when tested in different behavioral assays, i.e., shelter seeking, novel tank diving and scototaxis tests. The results demonstrate that behavioral variation exists both within and between the strains, but interpretation of boldness reveals a complex pattern in which behavior differs between strains but is also related to sex and test. Therefore, a careful assessment of various strains of fish using both males and females is warranted in order to strengthen interpretation of results. This is especially important in studies where zebrafish are used as model organisms for human conditions as well as studies evaluating the effects of pharmacological or toxicological substances on behavior.

  • 3.
    Mustafa, Arshi
    et al.
    Uppsala University, Disciplinary Domain of Medicine and Pharmacy, Faculty of Medicine, Department of Neuroscience, Winberg: Behavioral Neuroendocrinology. Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology.
    Thörnqvist, Per-Ove
    Uppsala University, Disciplinary Domain of Medicine and Pharmacy, Faculty of Medicine, Department of Neuroscience, Winberg: Behavioral Neuroendocrinology.
    Roman, Erika
    Uppsala University, Disciplinary Domain of Medicine and Pharmacy, Faculty of Pharmacy, Department of Pharmaceutical Biosciences.
    Winberg, Svante
    Uppsala University, Disciplinary Domain of Medicine and Pharmacy, Faculty of Medicine, Department of Neuroscience, Winberg: Behavioral Neuroendocrinology.
    The aggressive spiegeldanio, carrying a mutation in the fgfr1a gene, has no advantage in dyadic fights with zebrafish of the AB strain2019In: Behavioural Brain Research, ISSN 0166-4328, E-ISSN 1872-7549, Vol. 370, article id 111942Article in journal (Refereed)
    Abstract [en]

    Zebrafish which carries a mutation in the fibroblast growth factor receptor 1A (fgfr1a), also known as spiegeldanio (spd), has previously been reported to be bolder and more aggressive than wildtype (AB) zebrafish. However, in previous studies aggression has been quantified in mirror tests. In dyadic fights the behavior of the combatants is modified by the behavior of their opponent, and fighting a mirror has been reported to have different effects on brain gene expression and brain monoaminergic systems. In the present study aggression was quantified in fgfr1a mutants and AB zebrafish using a mirror test after which the fish were allowed to interact in pairs, either consisting of two fgfr1a mutants or one AB and one fgfr1a mutant fish. Following dyadic interaction aggressive behavior was again quantified in individual fish in a second mirror test after which the fish were sacrificed and brain tissue analyzed for monoamines and monoamine metabolites. The results confirm that fgfr1a mutants are more aggressive than AB zebrafish in mirror tests. However, fgfr1a mutant fish did not have any advantage in fights for social dominance, and agonistic behavior of fgfr1a mutants did not differ from that of AB fish during dyadic interactions. Moreover, as the AB fish, fgfr1a mutant fish losing dyadic interactions showed a typical loser effect and social subordination resulted in an activation of the brain serotonergic system in fgfr1a mutants as well as in AB fish. Overall the effects of dyadic interaction were similar in fgfr1a mutant fish and zebrafish of the AB strain.

  • 4.
    Paula, Jose Ricardo
    et al.
    Univ Lisbon, MARE Marine & Environm Sci Ctr, Lab Maritimo da Guia, Fac Ciencias, Av Nossa Senhora do Cabo 939, P-2750374 Cascais, Portugal.
    Repolho, Tiago
    Univ Lisbon, MARE Marine & Environm Sci Ctr, Lab Maritimo da Guia, Fac Ciencias, Av Nossa Senhora do Cabo 939, P-2750374 Cascais, Portugal.
    Pegado, Maria Rita
    Univ Lisbon, MARE Marine & Environm Sci Ctr, Lab Maritimo da Guia, Fac Ciencias, Av Nossa Senhora do Cabo 939, P-2750374 Cascais, Portugal.
    Thörnqvist, Per-Ove
    Uppsala University, Disciplinary Domain of Medicine and Pharmacy, Faculty of Medicine, Department of Neuroscience, Winberg: Behavioral Neuroendocrinology.
    Bispo, Regina
    Univ Nova Lisboa, Dept Matemat, Ctr Matemat & Aplicacoes, Fac Ciencias & Tecnol, Campus Caparica, P-2829516 Caparica, Portugal.
    Winberg, Svante
    Univ Lisbon, MARE Marine & Environm Sci Ctr, Lab Maritimo da Guia, Fac Ciencias, Av Nossa Senhora do Cabo 939, P-2750374 Cascais, Portugal.
    Munday, Philip L.
    James Cook Univ, ARC Ctr Excellence Coral Reef Studies, Townsville, Qld 4811, Australia.
    Rosa, Rui
    Univ Lisbon, MARE Marine & Environm Sci Ctr, Lab Maritimo da Guia, Fac Ciencias, Av Nossa Senhora do Cabo 939, P-2750374 Cascais, Portugal.
    Neurobiological and behavioural responses of cleaning mutualisms to ocean warming and acidification2019In: Scientific Reports, ISSN 2045-2322, E-ISSN 2045-2322, Vol. 9, article id 12728Article in journal (Refereed)
    Abstract [en]

    Cleaning interactions are textbook examples of mutualisms. On coral reefs, most fishes engage in cooperative interactions with cleaners fishes, where they benefit from ectoparasite reduction and ultimately stress relief. Furthermore, such interactions elicit beneficial effects on clients' ecophysiology. However, the potential effects of future ocean warming (OW) and acidification (OA) on these charismatic associations are unknown. Here we show that a 45-day acclimation period to OW (+3 degrees C) and OA (980 mu atm pCO(2)) decreased interactions between cleaner wrasses (Labroides dimidiatus) and clients (Naso elegans). Cleaners also invested more in the interactions by providing tactile stimulation under OA. Although this form of investment is typically used by cleaners to prolong interactions and reconcile after cheating, interaction time and client jolt rate (a correlate of dishonesty) were not affected by any stressor. In both partners, the dopaminergic (in all brain regions) and serotoninergic (forebrain) systems were significantly altered by these stressors. On the other hand, in cleaners, the interaction with warming ameliorated dopaminergic and serotonergic responses to OA. Dopamine and serotonin correlated positively with motivation to interact and cleaners interaction investment (tactile stimulation). We advocate that such neurobiological changes associated with cleaning behaviour may affect the maintenance of community structures on coral reefs.

  • 5.
    Ullah, Imdad
    et al.
    Uppsala University, Disciplinary Domain of Medicine and Pharmacy, Faculty of Medicine, Department of Neuroscience. Abbottabad Univ Sci & Technol, Dept Zool, Havelian, Abbottabad, Pakistan.
    Zuberi, Amina
    Quaid I Azam Univ, Dept Anim Sci, Fac Biol Sci, Islamabad, Pakistan.
    Rehman, Humaira
    Quaid I Azam Univ, Dept Anim Sci, Fac Biol Sci, Islamabad, Pakistan.
    Ali, Zulfiqar
    Quaid I Azam Univ, Dept Stat, Islamabad, Pakistan.
    Thörnqvist, Per-Ove
    Uppsala University, Disciplinary Domain of Medicine and Pharmacy, Faculty of Medicine, Department of Neuroscience, Winberg: Behavioral Neuroendocrinology.
    Winberg, Svante
    Uppsala University, Disciplinary Domain of Medicine and Pharmacy, Faculty of Medicine, Department of Neuroscience, Winberg: Behavioral Neuroendocrinology.
    Effects of early rearing enrichments on modulation of brain monoamines and hypothalamic-pituitary-interrenal axis (HPI axis) of fish mahseer (Tor putitora)2020In: Fish Physiology & Biochemistry, ISSN 0920-1742, E-ISSN 1573-5168, Vol. 46, no 1, p. 75-88Article in journal (Refereed)
    Abstract [en]

    Enriching rearing environment is the strategy suggested for improving the post release survivorship of captive-reared animals. Here, an attempt has been made to evaluate the impact of early rearing enrichment on the hypothalamic-pituitary-interrenal axis (HPI axis), blood glucose, and brain dopaminergic and serotonergic systems of Tor putitora. Fifteen-day-old hatchlings of T. putitora were reared up to advanced fry stage in barren, semi-natural, and physically enriched environments and compared them with regard to pre-stress and post-stress levels of whole-body cortisol, blood glucose, brain serotonergic activity (5HIAA/5HT ratio), dopaminergic activity (DOPAC/DA and HVA/DA ratios) and norepinephrine (NE) levels. Significantly low basal whole-body cortisol, glucose and brain NE levels were observed in a physically enriched group of fish as compared to the other two groups. However, after acute stress, all rearing groups showed elevated levels of cortisol, blood glucose, brain 5HIAA/5HT, DOPAC/DA and HVA/DA ratios and NE levels but the magnitude of response was different among different rearing groups. The barren reared group showed a higher magnitude of response as compared to semi-natural and physically enriched groups. Similarly, the recovery rate of whole-body cortisol, blood glucose, and whole-brain monoamines were long-lasting in barren-reared mahseer. We illustrate that increased structural complexity (physical enrichment) during the early rearing significantly modulates various physiological and stress-coping mechanisms of mahseer.

  • 6.
    Vossen, Laura E.
    Uppsala University, Disciplinary Domain of Medicine and Pharmacy, Faculty of Medicine, Department of Neuroscience, Winberg: Behavioral Neuroendocrinology.
    Effect of elevated pCO2 and environmental oxazepam on the behavior and physiology of teleost fish2019Doctoral thesis, comprehensive summary (Other academic)
    Abstract [en]

    This doctoral thesis investigated the effect of two aquatic pollutants on the behavior and physiology of teleost fish: i) elevated concentrations of carbon dioxide (CO2) in the context of ocean acidification and ii) low concentrations of the anxiolytic pharmaceutical oxazepam in the context of pharmaceutical pollution.

    Anthropogenic emissions of CO2 are lowering the pH of the oceans. Studies on coral reef fish exposed to CO2 concentrations projected for the year 2100 (~1000 μatm) reported alarming behavioral effects, of which attraction to predator odor was the most surprising. To explain this behavioral reversal, it was hypothesized that ion-regulatory adjustments to compensate for the decrease in blood pH would result in altered transmembrane gradients of chloride ions, rendering the major inhibitory neurotransmitter in the brain, γ-aminobutyric acid (GABA), excitatory. We investigated whether zebrafish (Danio rerio), an often used model species, showed similar behavioral disruptions in elevated CO2. Zebrafish behavior was however largely unaffected by an approximately month long exposure to ~1600 μatm CO2. We continued by investigating the reproductive, anxiety-related behavior and aggression in another model species, the three-spined stickleback (Gasterosteus aculeatus). However, also stickleback behavior and responses to social subordination were not affected by CO2, in contrast to earlier findings. We concluded that CO2 had no major effect on the behavior of zebrafish and three-spined stickleback.

    In the second part of this thesis, I investigated behavioral effects of oxazepam, an anxiolytic pharmaceutical (benzodiazepine) acting on the GABA system. Studies on perch (Perca fluviatilis) have shown that exposure to dilute concentrations of oxazepam (1.8 μg L-1), close to those found outside the municipal sewage treatment plant in Uppsala (0.58 μg L-1), can increase activity, decrease sociality and increase feeding rates. I show that similar oxazepam concentrations can also affect zebrafish. Moreover, I show that females are more sensitive to oxazepam showing reduced anti-predator responses at 0.57 μg L-1 while in males this effect was observed first at 60 μg L-1. Furthermore, and in contrast to wild-caught zebrafish, laboratory zebrafish did not show any effect of the oxazepam exposure. This finding has implications for the use of laboratory zebrafish in ecotoxicological and pharmacological studies, as results might not translate to wild fish. Finally, I show that zebrafish can develop tolerance to the anxiolytic effects of oxazepam during chronic (28 days) exposure. This is an important discovery that could mitigate the effects of this form of pharmaceutical pollution on wild fish.

    List of papers
    1. Zebrafish (Danio rerio) behaviour is largely unaffected by elevated pCO2
    Open this publication in new window or tab >>Zebrafish (Danio rerio) behaviour is largely unaffected by elevated pCO2
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    2016 (English)In: Conservation Physiology, E-ISSN 2051-1434, Vol. 4, no 1, article id cow065Article in journal (Refereed) Published
    Abstract [en]

    Ocean acidification, the decrease in ocean pH caused by anthropogenic emission of carbon dioxide, can cause behavioural disturbances in marine teleost species. We investigated whether AB-strain zebrafish (Danio rerio) show similar behavioural disturbances in the presence of elevated CO2, because this model species could open up a toolbox to investigate the physiological and neurological mechanisms of CO2 exposure. We found no effect of elevated CO2 (~1600 μatm) on the behaviour of zebrafish in the open field test, indicating that zebrafish are largely insensitive to this elevated CO2 level. In the detour test of lateralization, however, zebrafish exposed to elevated CO2 swam more often to the right, whereas individuals exposed to control CO2 (~400 μatm) had no preference for left or right. This may indicate that some behaviours of some freshwater fishes can be altered by elevated CO2 levels. Given that elevated CO2 levels often occur in recirculating aquaculture and aquarium systems, we recommend that dissolved CO2 levels are measured and, if necessary, the aquarium water should be aerated, in order to exclude CO2 level as a confounding factor in experiments.

    Keywords
    Behavioural lateralization, detour, gabazine, ocean acidification, open field, zebrafish
    National Category
    Climate Research Behavioral Sciences Biology
    Identifiers
    urn:nbn:se:uu:diva-319061 (URN)10.1093/conphys/cow065 (DOI)000490955500030 ()28066551 (PubMedID)
    Funder
    Swedish Research Council, VR 621-2012-4679Swedish Research Council Formas, 2009-596
    Available from: 2017-03-31 Created: 2017-03-31 Last updated: 2020-01-08Bibliographically approved
    2. No effect of elevated carbon dioxide on reproductive behaviors in the three-spined stickleback
    Open this publication in new window or tab >>No effect of elevated carbon dioxide on reproductive behaviors in the three-spined stickleback
    2017 (English)In: Behavioral Ecology, ISSN 1045-2249, E-ISSN 1465-7279, Vol. 28, no 6, p. 1482-1491Article in journal (Refereed) Published
    Abstract [en]

    Ocean acidification, the reduction in ocean pH resulting from anthropogenic emissions of carbon dioxide (CO2), has been predicted to alter the behavior of fishes. During experimental exposure to CO2 concentrations projected for the year 2100 (~1000 μatm), fish have been reported to display disturbances in activity, learning, behavioral lateralization, and even attraction to predator cues. Reproductive behaviors have received far less attention, despite an intensive research effort on ocean acidification and its ecological importance. Here, we investigate whether elevated levels of CO2 affect reproduction in breeding pairs of the three-spined stickleback, Gasterosteus aculeatus, a model species in behavioral, evolutionary ecology, and environmental toxicology. We found that males under both present day levels (400 μatm) and future levels (1000 μatm) of CO2 developed normal sexual ornaments, pursued normal nest building activi-ties, exhibited similar levels of courtship behaviors and displacement fanning, and had the same mating probability. Moreover, fanning behavior during the paternal care period followed what is expected for the species for males from both treatments, and there was no effect of treatment on the numbers of offspring produced. This study is the first to investigate the effect of elevated CO2 on the com-plete breeding cycle in detail, studying an array of highly fitness-relevant traits. Our study showing surprising resilience of fish repro-duction is an important contribution in order to realistically predict the impacts of future ocean acidification.

    Place, publisher, year, edition, pages
    Oxford University Press, 2017
    National Category
    Behavioral Sciences Biology
    Identifiers
    urn:nbn:se:uu:diva-331063 (URN)10.1093/beheco/arx112 (DOI)000415675000010 ()
    Funder
    Swedish Research Council Formas, 2013–947Swedish Research Council Formas, 2009–596Swedish Research Council, 621-2012-4679The Royal Swedish Academy of Sciences, (FOA14SLC027The Royal Swedish Academy of Sciences, FOA14SLC016
    Available from: 2017-10-10 Created: 2017-10-10 Last updated: 2019-10-28Bibliographically approved
    3. No evidence that exposure to elevated pCO2 affects behaviour or monoamine neurotransmitters of three-spined stickleback
    Open this publication in new window or tab >>No evidence that exposure to elevated pCO2 affects behaviour or monoamine neurotransmitters of three-spined stickleback
    Show others...
    (English)Manuscript (preprint) (Other academic)
    National Category
    Behavioral Sciences Biology
    Identifiers
    urn:nbn:se:uu:diva-395988 (URN)
    Available from: 2019-10-28 Created: 2019-10-28 Last updated: 2019-10-28
    4. Low concentrations of the benzodiazepine drug oxazepam induce anxiolytic effects in wild-caught but not in laboratory zebrafish
    Open this publication in new window or tab >>Low concentrations of the benzodiazepine drug oxazepam induce anxiolytic effects in wild-caught but not in laboratory zebrafish
    Show others...
    2020 (English)In: Science of the Total Environment, ISSN 0048-9697, E-ISSN 1879-1026, Vol. 703, article id 134701Article in journal (Refereed) Published
    Abstract [en]

    Pollution by psychoactive pharmaceuticals has been found to disrupt anti-predator behaviors of wild fish. The challenge is now to identify which of the many psychoactive drugs pose the greatest threat. One strategy is to screen for behavioral effects of selected pharmaceuticals using a single, widely available fish species such as zebrafish. Here, we show that although such high-throughput behavioral screening might facilitate comparisons between pharmaceuticals, the choice of strain is essential. While wild-caught zebrafish exposed to concentrations of the anxiolytic drug oxazepam as low as 0.57 μg L−1 showed a reduction in the response to conspecific alarm pheromone, laboratory strain AB did not respond to the alarm cue, and consequently, the anxiolytic effect of oxazepam could not be measured. Adaptation to the laboratory environment may have rendered laboratory strains unfit for use in some ecotoxicological and pharmacological studies, since the results might not translate to wild fish populations.

    Place, publisher, year, edition, pages
    Elsevier, 2020
    National Category
    Behavioral Sciences Biology
    Identifiers
    urn:nbn:se:uu:diva-395990 (URN)10.1016/j.scitotenv.2019.134701 (DOI)000505924300102 ()31734507 (PubMedID)
    Funder
    Swedish Research Council, 2012-04679Swedish Research Council, 2017-03779The Kempe FoundationsThe Research Council of Norway, 62942Swedish Research Council Formas, 2013-4431
    Available from: 2019-10-28 Created: 2019-10-28 Last updated: 2020-02-20Bibliographically approved
    5. Chronic exposure to oxazepam pollution produces tolerance to anxiolytic effects in zebrafish (Danio rerio)
    Open this publication in new window or tab >>Chronic exposure to oxazepam pollution produces tolerance to anxiolytic effects in zebrafish (Danio rerio)
    Show others...
    2020 (English)In: Environmental Science and Technology, ISSN 0013-936X, E-ISSN 1520-5851, Vol. 54, no 3, p. 1760-1769Article in journal (Refereed) Published
    Abstract [en]

    Environmental concentrations of the anxiolytic drug oxazepam have been found to disrupt antipredator behaviors of wild fish. Most experiments exposed fish for a week, while evidence from mammals suggests that chronic exposure to therapeutic concentrations of benzodiazepines (such as oxazepam) results in the development of tolerance to the anxiolytic effects. If tolerance can also develop in response to the low concentrations found in the aquatic environment, it could mitigate the negative effects of oxazepam pollution. In the current study, we exposed wild-caught zebrafish to oxazepam (similar to 7 mu g L-1) for 7 or 28 days and evaluated behavioral and physiological parameters at both time points. Females showed reduced diving responses to conspecific alarm pheromone after 7 days, but not after 28 days, indicating that they had developed tolerance to the anxiolytic effects of the drug. Zebrafish males were not affected by this oxazepam concentration, in line with earlier results. Serotonin turnover (ratio 5-HIAA/5-HT) was reduced in exposed females and males after 28 days, indicating that brain neurochemistry had not normalized. Post-confinement cortisol concentrations and gene expression of corticotropin-releasing hormone (CRH) were not affected by oxazepam. We did not find evidence that chronically exposed fish had altered relative expression of GABA A receptor subunits, suggesting that some other still unknown mechanism caused the developed tolerance.

    National Category
    Behavioral Sciences Biology
    Identifiers
    urn:nbn:se:uu:diva-395991 (URN)10.1021/acs.est.9b06052 (DOI)000511508500049 ()31934760 (PubMedID)
    Funder
    Swedish Research Council, 2012-04679Swedish Research Council, 2017-03779The Kempe Foundations, 62942The Research Council of NorwaySwedish Research Council Formas, 2013-4431
    Available from: 2019-10-28 Created: 2019-10-28 Last updated: 2020-03-23Bibliographically approved
  • 7.
    Vossen, Laura E.
    et al.
    Uppsala University, Disciplinary Domain of Medicine and Pharmacy, Faculty of Medicine, Department of Neuroscience, Winberg: Behavioral Neuroendocrinology.
    Cerveny, Daniel
    Swedish University of Agricultural Sciences, Department of Wildlife, Fish and Environmental Studies, Umeå, Sweden; Umeå University, Department of Chemistry, Umeå, Sweden; University of South Bohemia in Ceske Budejovice, Faculty of Fisheries and Protection of Waters, South Bohemian Research Center of Aquaculture and Biodiversity of Hydrocenoses, Zátiší 728/II, 389 25 Vodňany, Czech Republic.
    Sen Sarma, Oly
    Uppsala University, Disciplinary Domain of Medicine and Pharmacy, Faculty of Medicine, Department of Neuroscience, Winberg: Behavioral Neuroendocrinology.
    Thörnqvist, Per-Ove
    Uppsala University, Disciplinary Domain of Medicine and Pharmacy, Faculty of Medicine, Department of Neuroscience, Winberg: Behavioral Neuroendocrinology.
    Jutfelt, Fredrik
    Norwegian University of Science and Technology, Department of Biology, Trondheim, Norway.
    Fick, Jerker
    University of South Bohemia in Ceske Budejovice, Faculty of Fisheries and Protection of Waters, South Bohemian Research Center of Aquaculture and Biodiversity of Hydrocenoses, Zátiší 728/II, 389 25 Vodňany, Czech Republic.
    Brodin, Tomas
    Swedish University of Agricultural Sciences, Department of Wildlife, Fish and Environmental Studies, Umeå, Sweden.
    Winberg, Svante
    Uppsala University, Disciplinary Domain of Medicine and Pharmacy, Faculty of Medicine, Department of Neuroscience, Winberg: Behavioral Neuroendocrinology.
    Low concentrations of the benzodiazepine drug oxazepam induce anxiolytic effects in wild-caught but not in laboratory zebrafish2020In: Science of the Total Environment, ISSN 0048-9697, E-ISSN 1879-1026, Vol. 703, article id 134701Article in journal (Refereed)
    Abstract [en]

    Pollution by psychoactive pharmaceuticals has been found to disrupt anti-predator behaviors of wild fish. The challenge is now to identify which of the many psychoactive drugs pose the greatest threat. One strategy is to screen for behavioral effects of selected pharmaceuticals using a single, widely available fish species such as zebrafish. Here, we show that although such high-throughput behavioral screening might facilitate comparisons between pharmaceuticals, the choice of strain is essential. While wild-caught zebrafish exposed to concentrations of the anxiolytic drug oxazepam as low as 0.57 μg L−1 showed a reduction in the response to conspecific alarm pheromone, laboratory strain AB did not respond to the alarm cue, and consequently, the anxiolytic effect of oxazepam could not be measured. Adaptation to the laboratory environment may have rendered laboratory strains unfit for use in some ecotoxicological and pharmacological studies, since the results might not translate to wild fish populations.

    The full text will be freely available from 2021-11-02 14:36
  • 8.
    Vossen, Laura E.
    et al.
    Uppsala University, Disciplinary Domain of Medicine and Pharmacy, Faculty of Medicine, Department of Neuroscience, Winberg: Behavioral Neuroendocrinology.
    Cerveny, Daniel
    Österkrans, Marcus
    Uppsala University, Disciplinary Domain of Medicine and Pharmacy, Faculty of Medicine, Department of Neuroscience.
    Thörnqvist, Per-Ove
    Uppsala University, Disciplinary Domain of Medicine and Pharmacy, Faculty of Medicine, Department of Neuroscience, Winberg: Behavioral Neuroendocrinology.
    Jutfelt, Fredrik
    Fick, Jerker
    Brodin, Tomas
    Winberg, Svante
    Uppsala University, Disciplinary Domain of Medicine and Pharmacy, Faculty of Medicine, Department of Neuroscience, Winberg: Behavioral Neuroendocrinology.
    Chronic exposure to oxazepam pollution produces tolerance to anxiolytic effects in zebrafish (Danio rerio)2020In: Environmental Science and Technology, ISSN 0013-936X, E-ISSN 1520-5851, Vol. 54, no 3, p. 1760-1769Article in journal (Refereed)
    Abstract [en]

    Environmental concentrations of the anxiolytic drug oxazepam have been found to disrupt antipredator behaviors of wild fish. Most experiments exposed fish for a week, while evidence from mammals suggests that chronic exposure to therapeutic concentrations of benzodiazepines (such as oxazepam) results in the development of tolerance to the anxiolytic effects. If tolerance can also develop in response to the low concentrations found in the aquatic environment, it could mitigate the negative effects of oxazepam pollution. In the current study, we exposed wild-caught zebrafish to oxazepam (similar to 7 mu g L-1) for 7 or 28 days and evaluated behavioral and physiological parameters at both time points. Females showed reduced diving responses to conspecific alarm pheromone after 7 days, but not after 28 days, indicating that they had developed tolerance to the anxiolytic effects of the drug. Zebrafish males were not affected by this oxazepam concentration, in line with earlier results. Serotonin turnover (ratio 5-HIAA/5-HT) was reduced in exposed females and males after 28 days, indicating that brain neurochemistry had not normalized. Post-confinement cortisol concentrations and gene expression of corticotropin-releasing hormone (CRH) were not affected by oxazepam. We did not find evidence that chronically exposed fish had altered relative expression of GABA A receptor subunits, suggesting that some other still unknown mechanism caused the developed tolerance.

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