Pharmaceutical pollution represents a rapidly growing threat to ecosystems worldwide. Drugs are now commonly detected in the tissues of wildlife and have the potential to alter the natural expression of behavior, though relatively little is known about how pharmaceuticals impact predator-prey interactions. We conducted parallel laboratory experiments using larval odonates (dragonfly and damselfly nymphs) to investigate the effects of exposure to two pharmaceuticals, cetirizine and citalopram, and their mixture on the outcomes of predator-prey interactions. We found that exposure to both compounds elevated dragonfly activity and impacted their predation success and efficiency in complex ways. While exposure to citalopram reduced predation efficiency, exposure to cetirizine showed varied effects, with predation success being enhanced in some contexts but impaired in others. Our findings underscore the importance of evaluating pharmaceutical effects under multiple contexts and indicate that these compounds can affect predator-prey outcomes at sublethal concentrations.

Department of Science and Environment Roskilde University Universitetsvej 1 4000 Roskilde Denmark

Department of Wildlife Fish and Environmental Studies Swedish University of Agricultural Sciences Skogsmarksgränd Umeå Västerbotten 907 36 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 Zatisi 728 2 Vodnany Czech Republic

Zobrazit více v PubMed

Escher B.I., Stapleton H.M., Schymanski E.L. Tracking complex mixtures of chemicals in our changing environment. Science. 2020;367:388–392. doi: 10.1126/science.aay6636. PubMed DOI PMC

EEA . European Environment Agency. Publications Office; LU: 2018. Chemicals for a Sustainable Future: Report of the EEA Scientific Committee Seminar: Copenhagen, 17 May 2017.

Bernhardt E.S., Rosi E.J., Gessner M.O. Synthetic chemicals as agents of global change. Front. Ecol. Environ. 2017;15:84–90. doi: 10.1002/fee.1450. DOI

Orive G., Lertxundi U., Brodin T., Manning P. Greening the pharmacy. Science. 2022;377:259–260. doi: 10.1126/science.abp9554. PubMed DOI

aus der Beek T., Weber F.A., Bergmann A., Hickmann S., Ebert I., Hein A., Küster A. Pharmaceuticals in the environment—global occurrences and perspectives. Environ. Toxicol. Chem. 2016;35:823–835. doi: 10.1002/etc.3339. PubMed DOI

Wilkinson J.L., Boxall A.B.A., Kolpin D.W., Leung K.M.Y., Lai R.W.S., Galbán-Malagón C., Adell A.D., Mondon J., Metian M., Marchant R.A., et al. Pharmaceutical pollution of the world’s rivers. Proc. Natl. Acad. Sci. USA. 2022;119 doi: 10.1073/pnas.2113947119. PubMed DOI PMC

Bertram M.G., Martin J.M., Wong B.B.M., Brodin T. Curr. Biol. 2022;32:R17–R19. doi: 10.1016/j.cub.2021.11.038. PubMed DOI

Duarte I.A., Fick J., Cabral H.N., Fonseca V.F. Bioconcentration of neuroactive pharmaceuticals in fish: relation to lipophilicity, experimental design and toxicity in the aquatic environment. Sci. Total Environ. 2022;812 doi: 10.1016/j.scitotenv.2021.152543. PubMed DOI

Miller T.H., Bury N.R., Owen S.F., MacRae J.I., Barron L.P. A review of the pharmaceutical exposome in aquatic fauna. Environ. Pollut. 2018;239:129–146. doi: 10.1016/j.envpol.2018.04.012. PubMed DOI PMC

Emnet P., Gaw S., Northcott G., Storey B., Graham L. Personal care products and steroid hormones in the Antarctic coastal environment associated with two Antarctic research stations, McMurdo Station and Scott Base. Environ. Res. 2015;136:331–342. doi: 10.1016/j.envres.2014.10.019. PubMed DOI

Arnnok P., Singh R.R., Burakham R., Pérez-Fuentetaja A., Aga D.S. Selective uptake and bioaccumulation of antidepressants in fish from effluent-impacted Niagara River. Environ. Sci. Technol. 2017;51:10652–10662. doi: 10.1021/acs.est.7b02912. PubMed DOI

Richmond E.K., Rosi E.J., Walters D.M., Fick J., Hamilton S.K., Brodin T., Sundelin A., Grace M.R. A diverse suite of pharmaceuticals contaminates stream and riparian food webs. Nat. Commun. 2018;9:4491–4499. doi: 10.1038/s41467-018-06822-w. PubMed DOI PMC

Oaks J.L., Gilbert M., Virani M.Z., Watson R.T., Meteyer C.U., Rideout B.A., Shivaprasad H.L., Ahmed S., Chaudhry M.J.I., Arshad M., et al. Diclofenac residues as the cause of vulture population decline in Pakistan. Nature. 2004;427:630–633. doi: 10.1038/nature02317. PubMed DOI

Kidd K.A., Blanchfield P.J., Mills K.H., Palace V.P., Evans R.E., Lazorchak J.M., Flick R.W. Collapse of a fish population after exposure to a synthetic estrogen. Proc. Natl. Acad. Sci. USA. 2007;104:8897–8901. doi: 10.1073/pnas.0609568104. PubMed DOI PMC

Adeel M., Song X., Wang Y., Francis D., Yang Y. Environmental impact of estrogens on human, animal and plant life: a critical review. Environ. Int. 2017;99:107–119. doi: 10.1016/j.envint.2016.12.010. PubMed DOI

Aulsebrook L.C., Bertram M.G., Martin J.M., Aulsebrook A.E., Brodin T., Evans J.P., Hall M.D., O’Bryan M.K., Pask A.J., Tyler C.R., Wong B.B.M. Reproduction in a polluted world: implications for wildlife. Reproduction. 2020;160:R13–R23. doi: 10.1530/REP-20-0154. PubMed DOI

Agathokleous E., Barceló D., Aschner M., Azevedo R.A., Bhattacharya P., Costantini D., Cutler G.C., De Marco A., Docea A.O., Dórea J.G., et al. Rethinking subthreshold effects in regulatory chemical risk assessments. Environ. Sci. Technol. 2022;56:11095–11099. doi: 10.1021/acs.est.2c02896. PubMed DOI

Bertram M.G., Gore A.C., Tyler C.R., Brodin T. Endocrine-disrupting chemicals. Curr. Biol. 2022;32:R727–R730. PubMed

Saaristo M., Brodin T., Balshine S., Bertram M.G., Brooks B.W., Ehlman S.M., McCallum E.S., Sih A., Sundin J., Wong B.B.M., Arnold K.E. Direct and indirect effects of chemical contaminants on the behaviour, ecology and evolution of wildlife. Proc. Biol. Sci. 2018;285 doi: 10.1098/rspb.2018.1297. PubMed DOI PMC

Michelangeli M., Martin J.M., Pinter-Wollman N., Ioannou C.C., McCallum E.S., Bertram M.G., Brodin T. Predicting the impacts of chemical pollutants on animal groups. Trends Ecol. Evol. 2022;37:789–802. doi: 10.1016/j.tree.2022.05.009. PubMed DOI

Wong B.B.M., Candolin U. Behavioral responses to changing environments. Behav. Ecol. 2015;26:665–673. doi: 10.1093/beheco/aru183. DOI

Brodin T., Fick J., Jonsson M., Klaminder J. Dilute concentrations of a psychiatric drug alter behavior of fish from natural populations. Science. 2013;339:814–815. PubMed

Markman S., Leitner S., Catchpole C., Barnsley S., Müller C.T., Pascoe D., Buchanan K.L. Pollutants increase song complexity and the volume of the brain area HVC in a songbird. PLoS One. 2008;3:e1674. doi: 10.1371/journal.pone.0001674. PubMed DOI PMC

Martin J.M., McCallum E.S. Incorporating animal social context in ecotoxicology: can a single individual tell the collective story? Environ. Sci. Technol. 2021;55:10908–10910. doi: 10.1021/acs.est.1c04528. PubMed DOI PMC

Schmitz O.J. Effects of predator hunting mode on grassland ecosystem function. Science. 2008;319:952–954. doi: 10.1126/science.1152355. PubMed DOI

Weis J.S., Smith G., Santiago-Bass C. Predator/prey interactions: a link between the individual level and both higher and lower level effects of toxicants in aquatic ecosystems. J. Aquat. Ecosys. Stress Recov. 2000;7:145–153. doi: 10.1023/A:1009923414208. DOI

McPeek M.A. Behavioral differences between Enallagma species (Odonata) influencing differential vulnerability to predators. Ecology. 1990;71:1714–1726. doi: 10.2307/1937580. DOI

Corbet P.S. Harley books; 1999. Dragonflies: Behaviour and Ecology of Odonata.

Stoks R. Effect of lamellae autotomy on survival and foraging success of the damselfly Lestes sponsa (Odonata: lestidae) Oecologia. 1998;117:443–448. doi: 10.1007/s004420050679. PubMed DOI

Bose A.P.H., Robinson B.W. Invertebrate predation predicts variation in an autotomy-related trait in larval damselfly. Evol. Ecol. 2013;27:27–38. doi: 10.1007/s10682-012-9581-3. DOI

Ferreras-Romero M., Márquez-Rodríguez J., Ruiz-García A. Implications of anthropogenic disturbance factors on the Odonata assemblage in a Mediterranean fluvial system. Int. J. Odonatol. 2009;12:413–428. doi: 10.1080/13887890.2009.9748354. DOI

Perron M.A.C., Pick F.R. Water quality effects on dragonfly and damselfly nymph communities: a comparison of urban and natural ponds. Environ. Pollut. 2020;263 doi: 10.1016/j.envpol.2020.114472. PubMed DOI

Kristofco L.A., Brooks B.W. Global scanning of antihistamines in the environment: analysis of occurrence and hazards in aquatic systems. Sci. Total Environ. 2017;592:477–487. doi: 10.1016/j.scitotenv.2017.03.120. PubMed DOI

Almeida Â., Calisto V., Esteves V.I., Schneider R.J., Soares A.M.V.M., Figueira E., Freitas R. Ecotoxicity of the antihistaminic drug cetirizine to Ruditapes philippinarum clams. Sci. Total Environ. 2017;601–602:793–801. doi: 10.1016/j.scitotenv.2017.05.149. PubMed DOI

Li M.H. Acute toxicity of 30 pharmaceutically active compounds to freshwater planarians. Toxicol. Environ. Chem. 2013;95:1157–1170. doi: 10.1080/02772248.2013.857671. DOI

Jonsson M., Fick J., Klaminder J., Brodin T. Antihistamines and aquatic insects: bioconcentration and impacts on behavior in damselfly larvae (Zygoptera) Sci. Total Environ. 2014;472:108–111. doi: 10.1016/j.scitotenv.2013.10.104. PubMed DOI

Jonsson M., Andersson M., Fick J., Brodin T., Klaminder J., Piovano S. High-speed imaging reveals how antihistamine exposure affects escape behaviours in aquatic insect prey. Sci. Total Environ. 2019;648:1257–1262. doi: 10.1016/j.scitotenv.2018.08.226. PubMed DOI

Tierney A.J. Feeding, hunger, satiety and serotonin in invertebrates. Proc. Biol. Sci. 2020;287 doi: 10.1098/rspb.2020.1386. PubMed DOI PMC

Perry C.J., Baciadonna L. Studying emotion in invertebrates: what has been done, what can be measured and what they can provide. J. Exp. Biol. 2017;220:3856–3868. doi: 10.1242/jeb.151308. PubMed DOI

Ravhe I.S., Krishnan A., Manoj N. Evolutionary history of histamine receptors: early vertebrate origin and expansion of the H3-H4 subtypes. Mol. Phylogenet. Evol. 2021;154 doi: 10.1016/j.ympev.2020.106989. PubMed DOI

Nässel D.R. Histamine in the brain of insects: a review. Microsc. Res. Tech. 1999;44:121–136. doi: 10.1002/(SICI)1097-0029(19990115/01)44:2/3<121::AID-JEMT6>3.0.CO;2. PubMed DOI

Brodin T., Johansson F. Conflicting selection pressures on the growth/predation-risk trade-off in a damselfly. Ecology. 2004;85:2927–2932. doi: 10.1890/03-3120. DOI

Stahl S.M. Mechanism of action of serotonin selective reuptake inhibitors: serotonin receptors and pathways mediate therapeutic effects and side effects. J. Affect. Disord. 1998;51:215–235. doi: 10.1016/S0165-0327(98)00221-3. PubMed DOI

Fong P.P., Hoy C.M. Antidepressants (venlafaxine and citalopram) cause foot detachment from the substrate in freshwater snails at environmentally relevant concentrations. Mar. Freshw. Behav. Physiol. 2012;45:145–153. doi: 10.1080/10236244.2012.690579. DOI

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

Kellner M., Porseryd T., Porsch-Hällström I., Hansen S.H., Olsén K.H. Environmentally relevant concentrations of citalopram partially inhibit feeding in the three-spine stickleback (Gasterosteus aculeatus) Aquat. Toxicol. 2015;158:165–170. doi: 10.1016/j.aquatox.2014.11.003. PubMed DOI

Ziegler M., Eckstein H., Köhler H.R., Tisler S., Zwiener C., Triebskorn R. Effects of the antidepressants citalopram and venlafaxine on the big ramshorn snail (Planorbarius corneus) Water. 2021;13:1722. doi: 10.3390/w13131722. DOI

Ziegler M., Knoll S., Köhler H.R., Tisler S., Huhn C., Zwiener C., Triebskorn R. Impact of the antidepressant citalopram on the behaviour of two different life stages of brown trout. PeerJ. 2020;8 doi: 10.7717/peerj.8765. PubMed DOI PMC

Minguez L., Farcy E., Ballandonne C., Lepailleur A., Serpentini A., Lebel J.M., Bureau R., Halm-Lemeille M.P. Acute toxicity of 8 antidepressants: what are their modes of action? Chemosphere. 2014;108:314–319. doi: 10.1016/j.chemosphere.2014.01.057. PubMed DOI

Bláha M., Grabicova K., Shaliutina O., Kubec J., Randák T., Zlabek V., Buřič M., Veselý L. Foraging behaviour of top predators mediated by pollution of psychoactive pharmaceuticals and effects on ecosystem stability. Sci. Total Environ. 2019;662:655–661. doi: 10.1016/j.scitotenv.2019.01.295. PubMed DOI

Hirvonen H., Ranta E. Prey to predator size ratio influences foraging efficiency of larval Aeshna juncea dragonflies. Oecologia. 1996;106:407–415. doi: 10.1007/BF00334569. PubMed DOI

Brauer R., Alfageh B., Blais J.E., Chan E.W., Chui C.S.L., Hayes J.F., Man K.K.C., Lau W.C.Y., Yan V.K.C., Beykloo M.Y., et al. Psychotropic medicine consumption in 65 countries and regions, 2008–19: a longitudinal study. Lancet Psychiatr. 2021;8:1071–1082. doi: 10.1016/S2215-0366(21)00292-3. PubMed DOI PMC

Cunha D.L., de Araujo F.G., Marques M. Psychoactive drugs: occurrence in aquatic environment, analytical methods, and ecotoxicity—a review. Environ. Sci. Pollut. Res. Int. 2017;24:24076–24091. doi: 10.1007/s11356-017-0170-4. PubMed DOI

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

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

Burnside C.A., Robinson J.V. The functional morphology of caudal lamellae in coenagrionid (Odonata: zygoptera) damselfly larvae. Zool. J. Linn. Soc. 1995;114:155–171. doi: 10.1111/j.1096-3642.1995.tb00117a.x. DOI

Brooks M., Kristensen K., Benthem K., Magnusson A., Berg C., Nielsen A., Skaug H., Mächler M., Bolker B. glmmTMB balances speed and flexibility among packages for zero-inflated generalized linear mixed modeling. R J. 2017;9:378–400. doi: 10.3929/ethz-b-000240890. DOI

Therneau T.M. 2022. Mixed Effects Cox Models [R Package Coxme.

Smithson M., Verkuilen J. A better lemon squeezer? Maximum-likelihood regression with beta-distributed dependent variables. Psychol. Methods. 2006;11:54–71. doi: 10.1037/1082-989X.11.1.54. PubMed DOI

R Core Team R: a Language and environment for statistical computing. 2021. www.R-project.org

Pharmaceutical Pollution Alters the Structure of Freshwater Communities and Hinders Their Recovery from a Fish Predator