Pharmaceutical pollution poses an increasing threat to global wildlife populations. Psychoactive pharmaceutical pollutants (e.g. antidepressants, anxiolytics) are a distinctive concern owing to their ability to act on neural pathways that mediate fitness-related behavioural traits. However, despite increasing research efforts, very little is known about how these drugs might influence the behaviour and survival of species in the wild. Here, we capitalize on the development of novel slow-release pharmaceutical implants and acoustic telemetry tracking tools to reveal that exposure to environmentally relevant concentrations of the benzodiazepine pollutant temazepam alters movement dynamics and decreases the migration success of brown trout (Salmo trutta) smolts in a natural lake system. This effect was potentially owing to temazepam-exposed fish suffering increased predation compared with unexposed conspecifics, particularly at the river-lake confluence. These findings underscore the ability of pharmaceutical pollution to alter key fitness-related behavioural traits under natural conditions, with likely negative impacts on the health and persistence of wildlife populations.

Australian Rivers Institute Griffith University Nathan Queensland 4111 Australia

Department of Wildlife Fish and Environmental Studies Swedish University of Agricultural Sciences Umeå 907 36 Sweden

Department of Zoology Stockholm University Stockholm 114 18 Sweden

Institute of Zoology Zoological Society of London London NW1 4RY UK

School of Biological Sciences Monash University Clayton Victoria 3800 Australia

University of South Bohemia in Ceske Budejovice Faculty of Fisheries and Protection of Waters South Bohemian Research Center of Aquaculture and Biodiversity of Hydrocenoses Zatisi 728 2 Vodnany Czech Republic

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Sigmund G, et al. . 2023. Addressing chemical pollution in biodiversity research. Glob. Chang. Biol. 29, 3240–3255. (10.1111/gcb.16689) PubMed DOI

Sylvester F, et al. . 2023. Better integration of chemical pollution research will further our understanding of biodiversity loss. Nat. Ecol. Evol. 7, 1552–1555. (10.1038/s41559-023-02117-6) PubMed DOI

Boxall ABA. 2018. Pharmaceuticals in the environment and human health. In Health care and environmental contamination (eds Boxall ABA, Kookana RS), pp. 123–136. Amsterdam, The Netherlands: Elsevier. (10.1016/B978-0-444-63857-1.00007-3) DOI

Wilkinson JL, et al. . 2022. Pharmaceutical pollution of the world’s rivers. Proc. Natl Acad. Sci. USA 119, e2113947119. (10.1073/pnas.2113947119) PubMed DOI PMC

Graumnitz S, Jungmann D. 2021. Final report: The database pharmaceuticals in the environment. Update for the period 2017–2020. (ed. Hein A), German Environment Agency (Umwelt bundesamt).

Saaristo M, et al. . 2018. Direct and indirect effects of chemical contaminants on the behaviour, ecology and evolution of wildlife. Proc. R. Soc. B 285, 20181297. (10.1098/rspb.2018.1297) PubMed DOI PMC

The IQVIA Institute . 2021. The global use of medicines 2022: outlook to 2026. See https://www.iqvia.com/insights/the-iqvia-institute/reports-and-publications/reports/the-global-use-of-medicines-2022.

Aulsebrook LC, et al. . 2020. Reproduction in a polluted world: implications for wildlife. Reproduction 160, R13–R23. (10.1530/REP-20-0154) PubMed DOI

Arnold KE, Brown AR, Ankley GT, Sumpter JP. 2014. Medicating the environment: assessing risks of pharmaceuticals to wildlife and ecosystems. Philos. Trans. R. Soc. Lond., B, Biol. Sci. 369, 20130569. (10.1098/rstb.2013.0569) PubMed DOI PMC

Oaks JL, et al. . 2004. Diclofenac residues as the cause of vulture population decline in Pakistan. Nature 427, 630–633. (10.1038/nature02317) PubMed DOI

Bertram MG, et al. . 2022. Frontiers in quantifying wildlife behavioural responses to chemical pollution. Biol. Rev. Camb. Philos. Soc. 97, 1346–1364. (10.1111/brv.12844) PubMed DOI PMC

Brodin T, Fick J, Jonsson M, Klaminder J. 2013. Dilute concentrations of a psychiatric drug alter behavior of fish from natural populations. Science 339, 814–815. (10.1126/science.1226850) PubMed DOI

Świacka K, Maculewicz J, Kowalska D, Caban M, Smolarz K, Świeżak J. 2022. Presence of pharmaceuticals and their metabolites in wild-living aquatic organisms – current state of knowledge. J. Hazard. Mater. 424, 127350. (10.1016/j.jhazmat.2021.127350) PubMed DOI

Grabicová K, Grabic R, Fedorova G, Kolářová J, Turek J, Brooks BW, Randák T. 2020. Psychoactive pharmaceuticals in aquatic systems: a comparative assessment of environmental monitoring approaches for water and fish. Environ. Pollut. 261, 114150. (10.1016/j.envpol.2020.114150) PubMed DOI

Cerveny D, Brodin T, Cisar P, McCallum ES, Fick J. 2020. Bioconcentration and behavioral effects of four benzodiazepines and their environmentally relevant mixture in wild fish. Sci. Total Environ. 702, 134780. (10.1016/j.scitotenv.2019.134780) PubMed DOI

McCallum ES, Sundelin A, Fick J, Alanärä A, Klaminder J, Hellström G, Brodin T. 2019. Investigating tissue bioconcentration and the behavioural effects of two pharmaceutical pollutants on sea trout (Salmo trutta) in the laboratory and field. Aquat. Toxicol. 207, 170–178. (10.1016/j.aquatox.2018.11.028) PubMed DOI

McCallum ES, Krutzelmann E, Brodin T, Fick J, Sundelin A, Balshine S. 2017. Exposure to wastewater effluent affects fish behaviour and tissue-specific uptake of pharmaceuticals. Sci. Total Environ. 605–606, 578–588. (10.1016/j.scitotenv.2017.06.073) PubMed DOI

Michelangeli M, Martin JM, Pinter-Wollman N, Ioannou CC, McCallum ES, Bertram MG, Brodin T. 2022. Predicting the impacts of chemical pollutants on animal groups. Trends Ecol. Evol. 37, 789–802. (10.1016/j.tree.2022.05.009) PubMed DOI

Niemelä PT, Dingemanse NJ. 2014. Artificial environments and the study of ‘adaptive’ personalities. Trends Ecol. Evol. 29, 245–247. (10.1016/j.tree.2014.02.007) PubMed DOI

Fisher DN, James A, Rodríguez-Muñoz R, Tregenza T. 2015. Behaviour in captivity predicts some aspects of natural behaviour, but not others, in a wild cricket population. Proc. R. Soc. B 282, 20150708. (10.1098/rspb.2015.0708) PubMed DOI PMC

Osborn A, Briffa M. 2017. Does repeatable behaviour in the laboratory represent behaviour under natural conditions? A formal comparison in sea anemones. Anim. Behav. 123, 197–206. (10.1016/j.anbehav.2016.10.036) DOI

Ferguson A, Reed TE, Cross TF, McGinnity P, Prodöhl PA. 2019. Anadromy, potamodromy and residency in brown trout Salmo trutta: the role of genes and the environment. J. Fish Biol. 95, 692–718. (10.1111/jfb.14005) PubMed DOI PMC

McIntosh A, McHugh P, Budy P. 2012. Salmo trutta l. (brown trout). In A handbook of global freshwater invasive species (ed. Francis RA), pp. 285–299. London, UK: Taylor & Francis Group.

Freyhof J. 2011. Salmo trutta. The IUCN red list of threatened species. See https://www.iucnredlist.org/resources/freyhof2011.

Smialek N, Pander J, Geist J. 2021. Environmental threats and conservation implications for Atlantic salmon and brown trout during their critical freshwater phases of spawning, egg development and juvenile emergence. Fish. Manag. Eco. 28, 437–467. (10.1111/fme.12507) DOI

Cloos JM, Ferreira V. 2009. Current use of benzodiazepines in anxiety disorders. Curr. Opin. Psychiatry 22, 90–95. (10.1097/YCO.0b013e32831a473d) PubMed DOI

McCallum ES, Dey CJ, Cerveny D, Bose APH, Brodin T. 2021. Social status modulates the behavioral and physiological consequences of a chemical pollutant in animal groups. Ecol. Appl. 31, e02454. (10.1002/eap.2454) PubMed DOI

Hellström G, Klaminder J, Finn F, Persson L, Alanärä A, Jonsson M, Fick J, Brodin T. 2016. GABAergic anxiolytic drug in water increases migration behaviour in salmon. Nat. Commun. 7, 13460. (10.1038/ncomms13460) PubMed DOI PMC

Klaminder J, Jonsson M, Leander J, Fahlman J, Brodin T, Fick J, Hellström G. 2019. Less anxious salmon smolt become easy prey during downstream migration. Sci. Total Environ. 687, 488–493. (10.1016/j.scitotenv.2019.05.488) PubMed DOI

McCallum ES, Cerveny D, Fick J, Brodin T. 2019. Slow-release implants for manipulating contaminant exposures in aquatic wildlife: a new tool for field ecotoxicology. Environ. Sci. Technol. 53, 8282–8290. (10.1021/acs.est.9b01975) PubMed DOI

McCallum ES, Cerveny D, Bose APH, Fick J, Brodin T. 2023. Cost-effective pharmaceutical implants in fish: validating the performance of slow-release implants for the antidepressant fluoxetine. Environ. Toxicol. Chem. 42, 1326–1336. (10.1002/etc.5613) PubMed DOI

Fick J, et al. . 2017. Screening of benzodiazepines in thirty European rivers. Chemosphere 176, 324–332. (10.1016/j.chemosphere.2017.02.126) PubMed DOI

Cerveny D, Fick J, Klaminder J, Bertram MG, Brodin T. 2021. Exposure via biotransformation: oxazepam reaches predicted pharmacological effect levels in European perch after exposure to temazepam. Ecotoxicol. Environ. Saf. 217, 112246. (10.1016/j.ecoenv.2021.112246) PubMed DOI

Vossen LE, Červený D, Sen Sarma O, Thörnqvist PO, Jutfelt F, Fick J, Brodin T, Winberg S. 2020. Low concentrations of the benzodiazepine drug oxazepam induce anxiolytic effects in wild-caught but not in laboratory zebrafish. Sci. Total Environ. 703, 134701. (10.1016/j.scitotenv.2019.134701) PubMed DOI

Palm D, Lundberg P, Persson L, Losee J, Brodin T, Hellström G. 2024. Lake survival of hatchery‐reared adfluvial brown trout—a case study in a large natural lake in Sweden. River Res. Appl. 40, 1432–1436. (10.1002/rra.4280) DOI

Jepsen N, Koed A, Thorstad EB, Baras E. 2002. Surgical implantation of telemetry transmitters in fish: how much have we learned? In Aquatic telemetry (eds Thorstad EB, Fleming IA, Næsje TF), pp. 239–248. Dordrecht, The Netherlands: Springer Netherlands. (10.1007/978-94-017-0771-8_28) DOI

Kiessling A, Johansson D, Zahl IH, Samuelsen OB. 2009. Pharmacokinetics, plasma cortisol and effectiveness of benzocaine, MS-222 and isoeugenol measured in individual dorsal aorta-cannulated Atlantic salmon (Salmo salar) following bath administration. Aquaculture 286, 301–308. (10.1016/j.aquaculture.2008.09.037) DOI

Prystay TS, Elvidge CK, Twardek WM, Logan JM, Reid CH, Clarke SH, Foster JG, Cooke ELL, Cooke SJ. 2017. Comparison of the behavioral consequences and recovery patterns of largemouth bass exposed to MS‐222 or electrosedation. Trans. Am. Fish. Soc. 146, 556–566. (10.1080/00028487.2017.1285354) DOI

Xue YJ, Chang CC, Lai JM, Wang JH. 2017. Determining the tranquilization dose and residue of tricaine methanesulfonate (MS-222) in sea bass Lates calcarifer tissue. Fish. Sci. 83, 625–633. (10.1007/s12562-017-1091-3) DOI

Rillig MC, Kim SW, Schäffer A, Sigmund G, Groh KJ, Wang Z. 2022. About 'controls' in pollution-ecology experiments in the Anthropocene. Environ. Sci. Technol. 56, 11928–11930. (10.1021/acs.est.2c05460) PubMed DOI

R Core Team . 2019. R: a language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing. See https://www.r-project.org.

Dhellemmes F, Aspillaga E, Monk CT. 2023. AfTiltR: a solution for managing and filtering detections from passive acoustic telemetry data. MethodsX 10, 102222. (10.1016/j.mex.2023.102222) PubMed DOI PMC

Wickham H, et al. . 2019. Welcome to the tidyverse. J. Open Source Softw. 4, 1686. (10.21105/joss.01686) DOI

Dhellemmes F, Aspillaga E, Rittweg T, Alós J, Möller P, Arlinghaus R. 2023. Body size scaling of space use in coastal pike (Esox lucius) in brackish lagoons of the southern Baltic sea. Fish. Res. 260, 106560. (10.1016/j.fishres.2022.106560) DOI

Tonkin Z, et al. . 2022. Movement behavior of a threatened native fish informs flow management in a modified floodplain river system. Ecosphere 13, e3916. (10.1002/ecs2.3916) DOI

Brand JA, Henry J, Melo GC, Wlodkowic D, Wong BBM, Martin JM. 2023. Sex differences in the predictability of risk-taking behavior. Behav. Ecol. 34, 108–116. (10.1093/beheco/arac105) PubMed DOI PMC

Bürkner PC. 2017. brms: an R package for Bayesian multilevel models using Stan. J. Stat. Softw. 80, 1–28. (10.18637/jss.v080.i01) DOI

Lenth RV, Buerkner P, Giné-Vázquez I, Herve M, Jung M, Love J, Miguez F, Riebl H, Singmann H. 2022. Emmeans: estimated marginal means, aka least-squares means. See https://rvlenth.github.io/emmeans/.

Lüdecke D, Ben-Shachar MS, Patil I, Wiernik BM, Bacher E, Thériault R, Makowski D. 2022. Easystats: an R framework for easy statistical modeling, visualization, and reporting. See https://easystats.github.io/easystats/.

Lemoine NP. 2019. Moving beyond noninformative priors: why and how to choose weakly informative priors in Bayesian analyses. Oikos 128, 912–928. (10.1111/oik.05985) DOI

McElreath R. 2020. Statistical rethinking: a Bayesian course with examples in R and Stan, 2nd edn. New York, NY: CRC Press.

Kruschke J. 2014. Doing Bayesian data analysis: a tutorial with R, JAGS, and Stan, 2nd edn. London, UK: Academic Press. (10.1016/B978-0-12-405888-0.00008-8) DOI

van Etten J. 2017. R package gdistance: distances and routes on geographical grids. J. Stat. Softw. 76, 1–21. (10.18637/jss.v076.i13) PubMed DOI

Bourgeois CE, O’Connell MF. 1988. Observations on the seaward migration of atlantic salmon (Salmo salar L.) smolts through a large lake as determined by radiotelemetry and Carlin tagging studies. Can. J. Zool. 66, 685–691. (10.1139/z88-101) DOI

Thorstad EB, Whoriskey F, Uglem I, Moore A, Rikardsen AH, Finstad B. 2012. A critical life stage of the Atlantic salmon Salmo salar: behaviour and survival during the smolt and initial post-smolt migration. J. Fish Biol. 81, 500–542. (10.1111/j.1095-8649.2012.03370.x) PubMed DOI

Kraft S, Gandra M, Lennox RJ, Mourier J, Winkler AC, Abecasis D. 2023. Residency and space use estimation methods based on passive acoustic telemetry data. Mov. Ecol. 11, 12. (10.1186/s40462-022-00364-z) PubMed DOI PMC

Cerveny D, Fick J, Klaminder J, McCallum ES, Bertram MG, Castillo NA, Brodin T. 2021. Water temperature affects the biotransformation and accumulation of a psychoactive pharmaceutical and its metabolite in aquatic organisms. Environ. Int. 155, 106705. (10.1016/j.envint.2021.106705) PubMed DOI

Cerveny D, et al. . 2021. Neuroactive drugs and other pharmaceuticals found in blood plasma of wild European fish. Environ. Int. 146, 106188. (10.1016/j.envint.2020.106188) PubMed DOI

Losee JP, Palm D, Claiborne A, Madel G, Persson L, Quinn TP, Brodin T, Hellström G. 2024. Anadromous trout from opposite sides of the globe: biology, ocean ecology, and management of anadromous brown and cutthroat trout. Rev. Fish Biol. Fish. 34, 461–490. (10.1007/s11160-023-09824-0) DOI

Hesthagen T, Sandlund OT, Finstad AG, Johnsen BO. 2015. The impact of introduced pike (Esox lucius L.) on allopatric brown trout (Salmo trutta L.) in a small stream. Hydrobiologia 744, 223–233. (10.1007/s10750-014-2078-z) DOI

Schwinn M, Baktoft H, Aarestrup K, Lucas MC, Koed A. 2018. Telemetry observations of predation and migration behaviour of brown trout (Salmo trutta) smolts negotiating an artificial lake. River Res. Apps. 34, 898–906. (10.1002/rra.3327) DOI

Hyvärinen P, Vehanen T. 2004. Effect of brown trout body size on post‐stocking survival and pike predation. Ecol. Freshw. Fish 13, 77–84. (10.1111/j.1600-0633.2004.00050.x) DOI

Kennedy RJ, Rosell R, Millane M, Doherty D, Allen M. 2018. Migration and survival of Atlantic salmon Salmo salar smolts in a large natural lake. J. Fish Biol. 93, 134–137. (10.1111/jfb.13676) PubMed DOI

Hanssen EM, Vollset KW, Salvanes AGV, Barlaup B, Whoriskey K, Isaksen TE, Normann ES, Hulbak M, Lennox RJ. 2022. Acoustic telemetry predation sensors reveal the tribulations of Atlantic salmon (Salmo salar) smolts migrating through lakes. Ecol. Freshw. Fish. 31, 424–437. (10.1111/eff.12641) DOI

Sundin J, Jutfelt F, Thorlacius M, Fick J, Brodin T. 2019. Behavioural alterations induced by the anxiolytic pollutant oxazepam are reversible after depuration in a freshwater fish. Sci. Total Environ. 665, 390–399. (10.1016/j.scitotenv.2019.02.049) PubMed DOI

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). J. Toxicol. Environ. Health Part A 80, 963–970. (10.1080/15287394.2017.1352214) PubMed DOI

Lennox RJ, et al. . 2023. Positioning aquatic animals with acoustic transmitters. Methods Ecol. Evol. 14, 2514–2530. (10.1111/2041-210X.14191) DOI

Lennox RJ, Dahlmo LS, Ford AT, Sortland LK, Vogel EF, Vollset KW. 2023. Predation research with electronic tagging. Wildlife Biol. 2023, e01045. (10.1002/wlb3.01045) DOI

Säterberg T, Jacobson P, Ovegård M, Rask J, Östergren J, Jepsen N, Florin A. 2023. Species‐ and origin‐specific susceptibility to bird predation among juvenile salmonids. Ecosphere 14, e4724. (10.1002/ecs2.4724) DOI

Kellner M, Porseryd T, Hallgren S, Porsch-Hällström I, Hansen SH, Olsén KH. 2016. Waterborne citalopram has anxiolytic effects and increases locomotor activity in the three-spine stickleback (Gasterosteus aculeatus). Aquat. Toxicol. 173, 19–28. (10.1016/j.aquatox.2015.12.026) PubMed DOI

Martin JM, Saaristo M, Bertram MG, Lewis PJ, Coggan TL, Clarke BO, Wong BBM. 2017. The psychoactive pollutant fluoxetine compromises antipredator behaviour in fish. Environ. Pollut. 222, 592–599. (10.1016/j.envpol.2016.10.010) PubMed DOI

Klaminder J, Hellström G, Fahlman J, Jonsson M, Fick J, Lagesson A, Bergman E, Brodin T. 2016. Drug-induced behavioral changes: using laboratory observations to predict field observations. Front. Environ. Sci. 4, 2016.00081. (10.3389/fenvs.2016.00081) DOI

Fahlman J, Hellström G, Jonsson M, Fick JB, Rosvall M, Klaminder J. 2021. Impacts of oxazepam on perch (Perca fluviatilis) behavior: fish familiarized to lake conditions do not show predicted anti-anxiety response. Environ. Sci. Technol. 55, 3624–3633. (10.1021/acs.est.0c05587) PubMed DOI PMC

Oziolor EM, Reid NM, Yair S, Lee KM, Guberman VerPloeg S, Bruns PC, Shaw JR, Whitehead A, Matson CW. 2019. Adaptive introgression enables evolutionary rescue from extreme environmental pollution. Science 364, 455–457. (10.1126/science.aav4155) PubMed DOI

Reid NM, et al. . 2016. The genomic landscape of rapid repeated evolutionary adaptation to toxic pollution in wild fish. Science 354, 1305–1308. (10.1126/science.aah4993) PubMed DOI PMC

Nathan R, et al. . 2022. Big-data approaches lead to an increased understanding of the ecology of animal movement. Science 375, eabg1780. (10.1126/science.abg1780) PubMed DOI

Jacoby DMP, Piper AT. 2023. What acoustic telemetry can and cannot tell us about fish biology. J. Fish Biol. 1–25. (10.1111/jfb.15588) PubMed DOI

OSFHome . 2024. Psychoactive pollutant alters movement dynamics of fish in a natural lake system. See https://osf.io/zsv68/. PubMed PMC

Brand JA, Bertram MG, Cerveny D, McCallum ES, Hellström G, Michelangeli M, Palm D, Brodin T. 2024. Supplementary material from: Psychoactive pollutant alters movement dynamics of fish in a natural lake system. Figshare. (10.6084/m9.figshare.c.7557353) PubMed DOI PMC

Psychoactive pollutant alters movement dynamics of fish in a natural lake system