Methamphetamine (METH), a central nervous system stimulant used as a recreational drug, is frequently found in surface waters at potentially harmful concentrations. To determine effects of long-term exposure to environmentally relevant levels on nontarget organisms, we analysed cardiac and locomotor responses of signal crayfish Pacifastacus leniusculus to acute stress during a 21-day exposure to METH at 1 μg L-1 followed by 14 days depuration. Heart rate and locomotion were recorded over a period of 30 min before and 30 min after exposure to haemolymph of an injured conspecific four times during METH exposure and four times during the depuration phase. Methamphetamine-exposed crayfish showed a weaker cardiac response to stress than was observed in controls during both exposure and depuration phases. Similarly, methamphetamine-exposed crayfish, during METH exposure, showed lower locomotor reaction poststressor application in contrast to controls. Results indicate biological alterations in crayfish exposed to METH at low concentration level, potentially resulting in a shift in interactions among organisms in natural environment.

Faculty of Fisheries and Protection of Waters South Bohemian Research Center of Aquaculture and Biodiversity of Hydrocenoses Zátiší 728 2 University of South Bohemia in České Budějovice 389 25 Vodňany Czech Republic

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Pal R., Megharaj M., Kirkbride K.P., Naidu R. Illicit drugs and the environment—A review. Sci. Total Environ. 2013;463:1079–1092. doi: 10.1016/j.scitotenv.2012.05.086. PubMed DOI

Nefau T., Karolak S., Castillo L., Boireau V., Levi Y. Corrigendum to “Presence of illicit drugs and metabolites in influents and effluents of 25 sewage water treatment plants and map of drug consumption in France” [Sci. Total Environ. 461–462 (2013) 712–722] Sci. Total Environ. 2014:1179–1181. doi: 10.1016/j.scitotenv.2013.12.001. PubMed DOI

United Nations Office on Drugs and Crime . World Drug Report 2019. United Nations Office on Drugs and Crime; Vienna, Austria: 2019. pp. 9–10. United Nations publication, Sales No. E.19.XI.8.

Bramness J.G., Reid M.J., Solvik K.F., Vindenes V. Recent trends in the availability and use of amphetamine and methamphetamine in Norway. Forensic Sci. Int. 2015;246:92–97. doi: 10.1016/j.forsciint.2014.11.010. PubMed DOI

European Monitoring Centre for Drugs and Drug Addiction . European Drug Report 2019: Trends and Developments. Publications Office of the European Union; Luxembourg: 2019. pp. 52–53.

Du P., Li K., Li J., Xu Z., Fu X., Yang J., Zhang H., Li X. Methamphetamine and ketamine use in major Chinese cities, a nationwide reconnaissance through sewage-based epidemiology. Water Res. 2015;84:76–84. doi: 10.1016/j.watres.2015.07.025. PubMed DOI

Boleda M.R., Galceran M.T., Ventura F. Monitoring of opiates, cannabinoids and their metabolites in wastewater, surface water and finished water in Catalonia, Spain. Water Res. 2009;43:1126–1136. doi: 10.1016/j.watres.2008.11.056. PubMed DOI

Boleda M.R., Huerta-Fontela M., Ventura F., Galceran M.T. Evaluation of the presence of drugs of abuse in tap waters. Chemosphere. 2011;84:1601–1607. doi: 10.1016/j.chemosphere.2011.05.033. PubMed DOI

Causanilles A., Ruepert C., Ibáñez M., Emke E., Hernández F., de Voogt P. Occurrence and fate of illicit drugs and pharmaceuticals in wastewater from two wastewater treatment plants in Costa Rica. Sci. Total Environ. 2017;599:98–107. doi: 10.1016/j.scitotenv.2017.04.202. PubMed DOI

González-Mariño I., Baz-Lomba J.A., Alygizakis N.A., Andrés-Costa M.J., Bade R., Barron L.P., Been F., Berset J.D., Bijlsma L., Bodík I. Spatio-temporal assessment of illicit drug use at large scale: Evidence from 7 years of international wastewater monitoring. Addiction. 2020;115:109–120. doi: 10.1111/add.14767. PubMed DOI PMC

Li K., Du P., Xu Z., Gao T., Li X. Occurrence of illicit drugs in surface waters in China. Environ. Pollut. 2016;213:395–402. doi: 10.1016/j.envpol.2016.02.036. PubMed DOI

Lopes A., Silva N., Bronze M., Ferreira J., Morais J. Analysis of cocaine and nicotine metabolites in wastewater by liquid chromatography–tandem mass spectrometry. Cross abuse index patterns on a major community. Sci. Total Environ. 2014;487:673–680. doi: 10.1016/j.scitotenv.2013.10.042. PubMed DOI

Mackuľak T., Bodík I., Hasan J., Grabic R., Golovko O., Vojs-Staňová A., Gál M., Naumowicz M., Tichý J., Brandeburová P. Dominant psychoactive drugs in the Central European region: A wastewater study. Forensic Sci. Int. 2016;267:42–51. doi: 10.1016/j.forsciint.2016.08.016. PubMed DOI

Mastroianni N., López-García E., Postigo C., Barceló D., de Alda M.L. Five-year monitoring of 19 illicit and legal substances of abuse at the inlet of a wastewater treatment plant in Barcelona (NE Spain) and estimation of drug consumption patterns and trends. Sci. Total Environ. 2017;609:916–926. doi: 10.1016/j.scitotenv.2017.07.126. PubMed DOI

Xu Z., Du P., Li K., Gao T., Wang Z., Fu X., Li X. Tracing methamphetamine and amphetamine sources in wastewater and receiving waters via concentration and enantiomeric profiling. Sci. Total Environ. 2017;601:159–166. doi: 10.1016/j.scitotenv.2017.05.045. PubMed DOI

Miller T.H., Ng K.T., Bury S.T., Bury S.E., Bury N.R., Barron L.P. Biomonitoring of pesticides, pharmaceuticals and illicit drugs in a freshwater invertebrate to estimate toxic or effect pressure. Environ. Int. 2019;129:595–606. doi: 10.1016/j.envint.2019.04.038. PubMed DOI PMC

Capaldo A., Gay F., Maddaloni M., Valiante S., De Falco M., Lenzi M., Laforgia V. Presence of cocaine in the tissues of the European eel, Anguilla anguilla, exposed to environmental cocaine concentrations. Water Air Soil Pollut. 2012;223:2137–2143. doi: 10.1007/s11270-011-1010-7. DOI

Binelli A., Marisa I., Fedorova M., Hoffmann R., Riva C. First evidence of protein profile alteration due to the main cocaine metabolite (benzoylecgonine) in a freshwater biological model. Aquat. Toxicol. 2013;140:268–278. doi: 10.1016/j.aquatox.2013.06.013. PubMed DOI

Binelli A., Pedriali A., Riva C., Parolini M. Illicit drugs as new environmental pollutants: Cyto-genotoxic effects of cocaine on the biological model Dreissena polymorpha. Chemosphere. 2012;86:906–911. doi: 10.1016/j.chemosphere.2011.10.056. PubMed DOI

Parolini M., Pedriali A., Riva C., Binelli A. Sub-lethal effects caused by the cocaine metabolite benzoylecgonine to the freshwater mussel Dreissena polymorpha. Sci. Total Environ. 2013;444:43–50. doi: 10.1016/j.scitotenv.2012.11.076. PubMed DOI

Sacavage S., Patel H., Zielinski M., Acker J., Phillips A.G., Raffa R.B., Rawls S.M. Withdrawal-like behavior in planarians is dependent on drug exposure duration. Neurosci. Lett. 2008;439:84–88. doi: 10.1016/j.neulet.2008.04.086. PubMed DOI

Kusayama T., Watanabe S. Reinforcing effects of methamphetamine in planarians. Neuroreport. 2000;11:2511–2513. doi: 10.1097/00001756-200008030-00033. PubMed DOI

Alcaro A., Panksepp J., Huber R. D-amphetamine stimulates unconditioned exploration/approach behaviors in crayfish: Towards a conserved evolutionary function of ancestral drug reward. Pharmacol. Biochem. Behav. 2011;99:75–80. doi: 10.1016/j.pbb.2011.04.004. PubMed DOI PMC

Imeh-Nathaniel A., Adedeji A., Huber R., Nathaniel T.I. The rewarding properties of methamphetamine in an invertebrate model of drug addiction. Physiol. Behav. 2016;153:40–46. doi: 10.1016/j.physbeh.2015.10.017. PubMed DOI

Nathaniel T.I., Huber R., Panksepp J. Repeated cocaine treatments induce distinct locomotor effects in crayfish. Brain Res. Bull. 2012;87:328–333. doi: 10.1016/j.brainresbull.2011.11.022. PubMed DOI

Shipley A.T., Imeh-Nathaniel A., Orfanakos V.B., Wormack L.N., Huber R., Nathaniel T.I. The Sensitivity of the crayfish reward system to mammalian drugs of abuse. Front. Physiol. 2017;8:1007. doi: 10.3389/fphys.2017.01007. PubMed DOI PMC

van Staaden M.J., Huber R. Crayfish learning: Addiction and the ganglionic brain. Perspect. Behav. Sci. 2018;41:417–429. doi: 10.1007/s40614-018-00181-z. PubMed DOI PMC

Liao P.-H., Hwang C.-C., Chen T.-H., Chen P.-J. Developmental exposures to waterborne abused drugs alter physiological function and larval locomotion in early life stages of medaka fish. Aquat. Toxicol. 2015;165:84–92. doi: 10.1016/j.aquatox.2015.05.010. PubMed DOI

Gay F., Maddaloni M., Valiante S., Laforgia V., Capaldo A. Endocrine disruption in the European eel, Anguilla anguilla, exposed to an environmental cocaine concentration. Water Air Soil Pollut. 2013;224:1579. doi: 10.1007/s11270-013-1579-0. DOI

Kaye S., McKetin R., Duflou J., Darke S. Methamphetamine and cardiovascular pathology: A review of the evidence. Addiction. 2007;102:1204–1211. doi: 10.1111/j.1360-0443.2007.01874.x. PubMed DOI

Völlm B.A., De Araujo I.E., Cowen P.J., Rolls E.T., Kringelbach M.L., Smith K.A., Jezzard P., Heal R.J., Matthews P.M. Methamphetamine activates reward circuitry in drug naive human subjects. Neuropsychopharmacology. 2004;29:1715–1722. doi: 10.1038/sj.npp.1300481. PubMed DOI

Hossain M.S., Kubec J., Grabicová K., Grabic R., Randák T., Guo W., Kouba A., Buřič M. Environmentally relevant concentrations of methamphetamine and sertraline modify the behavior and life history traits of an aquatic invertebrate. Aquat. Toxicol. 2019;213:105222. doi: 10.1016/j.aquatox.2019.105222. PubMed DOI

Guo W., Hossain M.S., Kubec J., Grabicová K., Randák T., Buřič M., Kouba A. Psychoactive compounds at environmental concentration alter burrowing behavior in the freshwater crayfish. Sci. Total Environ. 2019;711:135138. doi: 10.1016/j.scitotenv.2019.135138. PubMed DOI

Kubec J., Hossain M.S., Grabicová K., Randák T., Kouba A., Grabic R., Roje S., Buřič M. Oxazepam alters the behavior of crayfish at diluted concentrations, venlafaxine does not. Water. 2019;11:196. doi: 10.3390/w11020196. DOI

Kuklina I., Ložek F., Císař P., Kouba A., Kozák P. Crayfish can distinguish between natural and chemical stimuli as assessed by cardiac and locomotor reactions. Environ. Sci. Pollut. Res. 2018;25:8396–8403. doi: 10.1007/s11356-017-1183-8. PubMed DOI

Tierney A., Hanzlik K., Hathaway R., Powers C., Roy M. Effects of fluoxetine on growth and behavior in the crayfish Orconectes rusticus. Mar. Freshw. Behav. Physiol. 2016;49:133–145. doi: 10.1080/10236244.2015.1119974. DOI

Kuklina I., Ložek F., Císař P., Pautsina A., Buřič M., Kozák P. Continuous noninvasive measuring of crayfish cardiac and behavioral activities. JoVE (J. Vis. Exp.) 2019:e58555. doi: 10.3791/58555. PubMed DOI

Ložek F., Kuklina I., Grabicová K., Kubec J., Buřič M., Grabic R., Randák T., Císař P., Kozák P. Behaviour and cardiac response to stress in signal crayfish exposed to environmental concentrations of tramadol. Aquat. Toxicol. 2019;213:105217. doi: 10.1016/j.aquatox.2019.05.019. PubMed DOI

Hazlett B.A. Alarm responses in the crayfishOrconectes virilis andOrconectes propinquus. J. Chem. Ecol. 1994;20:1525–1535. doi: 10.1007/BF02059878. 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

Brodin T., Piovano S., Fick J., Klaminder J., Heynen M., Jonsson M. Ecological effects of pharmaceuticals in aquatic systems—Impacts through behavioural alterations. Philos. Trans. R. Soc. B Biol. Sci. 2014;369:20130580. doi: 10.1098/rstb.2013.0580. PubMed DOI PMC

Imeh-Nathaniel A., Rincon N., Orfanakos V.B., Brechtel L., Wormack L., Richardson E., Huber R., Nathaniel T.I. Effects of chronic cocaine, morphine and methamphetamine on the mobility, immobility and stereotyped behaviors in crayfish. Behav. Brain Res. 2017;332:120–125. doi: 10.1016/j.bbr.2017.05.069. PubMed DOI

Mark K.A., Soghomonian J.-J., Yamamoto B.K. High-dose methamphetamine acutely activates the striatonigral pathway to increase striatal glutamate and mediate long-term dopamine toxicity. J. Neurosci. 2004;24:11449–11456. doi: 10.1523/JNEUROSCI.3597-04.2004. PubMed DOI PMC

Won S., Hong R.A., Shohet R.V., Seto T.B., Parikh N.I. Methamphetamine-associated cardiomyopathy. Clin. Cardiol. 2013;36:737–742. doi: 10.1002/clc.22195. PubMed DOI PMC

Buřič M., Grabicová K., Kubec J., Kouba A., Kuklina I., Kozák P., Grabic R., Randák T. Environmentally relevant concentrations of tramadol and citalopram alter behaviour of an aquatic invertebrate. Aquat. Toxicol. 2018;200:226–232. doi: 10.1016/j.aquatox.2018.05.008. PubMed DOI