Response of Parasite Community Composition to Aquatic Pollution in Common Carp (Cyprinus carpio L.): A Semi-Experimental Study

. 2023 Apr 25 ; 13 (9) : . [epub] 20230425

Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid37174501

Grantová podpora
MUNI/A/1422/2022 Masaryk University
"CENAKVA" LM2018099 Ministry of Education, Youth and Sports of the Czech Republic
CZ.02.1.01/0.0/0.0/16_019/0000869 PROFISH Ministry of Education, Youth and Sports of the Czech Republic

The response of parasite communities to aquatic contamination has been shown to vary with both type of pollutant and parasite lifestyle. In this semi-experimental study, we examined uptake of pharmaceutical compounds in common carp (Cyprinus carpio L.) restocked from a control pond to a treatment pond fed with organic pollution from a sewage treatment plant and assessed changes in parasite community composition and fish biometric parameters. The parasite community of restocked fish changed over the six-month exposure period, and the composition of pharmaceutical compounds in the liver and brain was almost the same as that in fish living in the treatment pond their whole life. While fish size and weight were significantly higher in both treatment groups compared to the control, condition indices, including condition factor, hepatosomatic index, and splenosomatic index, were significantly higher in control fish. Parasite diversity and species richness decreased at the polluted site, alongside a significant increase in the abundance of a single parasite species, Gyrodactylus sprostonae. Oviparous monogeneans of the Dactylogyridae and Diplozoidae families and parasitic crustaceans responded to pollution with a significant decrease in abundance, the reduction in numbers most likely related to the sensitivity of their free-living stages to pollution.

Zobrazit více v PubMed

Carpenter S.R., Stanley E.H., Vander Zanden M.J. State of the World’s Freshwater Ecosystems: Physical, Chemical, and Biological Changes. Annu. Rev. Environ. Resour. 2011;36:75–99. doi: 10.1146/annurev-environ-021810-094524. DOI

Blettler M.C.M., Abrial E., Khan F.R., Sivri N., Espinola L.A. Freshwater plastic pollution: Recognising research biases and identifying knowledge gaps. Water Res. 2018;143:416–424. doi: 10.1016/j.watres.2018.06.015. PubMed DOI

Amoatey P., Baawain M.S. Effects of pollution on freshwater aquatic organisms. Water Environ. Res. 2019;91:1272–1287. doi: 10.1002/wer.1221. PubMed DOI

Ebele A.J., Abdallah M.A., Harrad S. Pharmaceuticals and personal care products (PPCPs) in the freshwater aquatic environment. Emerg. Contam. 2017;3:1–16. doi: 10.1016/j.emcon.2016.12.004. DOI

Fekadu S., Alemayehu E., Dewil R., Van der Bruggen B. Pharmaceuticals in freshwater aquatic environments: A comparison of the African and European challenge. Sci. Total Environ. 2019;654:324–337. doi: 10.1016/j.scitotenv.2018.11.072. PubMed DOI

Patel N., Khan M.Z.A., Shahane S., Rai D., Chauhan D., Kant C., Chaudhary V.K. Emerging Pollutants in Aquatic Environment: Source, Effect, and Challenges in Biomonitoring and Bioremediation—A Review. Pollution. 2020;6:99–113.

Fent K., Weston A.A., Caminada D. Ecotoxicology of human pharmaceuticals. Aquat. Toxicol. 2006;76:122–159. doi: 10.1016/j.aquatox.2005.09.009. PubMed DOI

Morley N.J. Environmental risk and toxicology of human and veterinary waste pharmaceutical exposure to wild aquatic host-parasite relationships. Environ. Toxicol. Pharmacol. 2009;27:161–175. doi: 10.1016/j.etap.2008.11.004. PubMed DOI

Hamilton W.L., Doyle C., Halliwell-Ewen M., Lambert G. Public health interventions to protect against falsified medicines: A systematic review of international, national and local policies. Health Policy Plan. 2016;31:1448–1466. doi: 10.1093/heapol/czw062. PubMed DOI

Nilsen E., Smalling K.L., Ahrens L., Gros M., Miglioranza K.S., Pico Y., Schoenfuss H.L. Critical review: Grand challenges in assessing the adverse effects of contaminants of emerging concern on aquatic food webs. Environ. Toxicol. Chem. 2019;38:46–60. doi: 10.1002/etc.4290. PubMed DOI

Marcogliese D.J., Pietrock M. Combined effects of parasites and contaminants on animal health: Parasites do matter. Trends Parasitol. 2011;27:123–130. doi: 10.1016/j.pt.2010.11.002. PubMed DOI

Sures B., Nachev M., Selbach C., Marcogliese D.J. Parasite responses to pollution: What we know and where we go in ‘Environmental Parasitology’. Parasit. Vectors. 2017;10:65. doi: 10.1186/s13071-017-2001-3. PubMed DOI PMC

Marcogliese D.J. Parasites of the superorganism: Are they indicators of ecosystem health? Int. J. Parasitol. 2005;35:705–716. doi: 10.1016/j.ijpara.2005.01.015. PubMed DOI

Blanar C.A., Marcogliese D.J., Couillard C.M. Natural and anthropogenic factors shape metazoan parasite community structure in mummichog (Fundulus heteroclitus) from two estuaries in New Brunswick, Canada. Folia Parasitol. 2011;58:240–248. doi: 10.14411/fp.2011.023. PubMed DOI

Pietrock M., Marcogliese D.J. Free-living endohelminth stages: At the mercy of environmental conditions. Trends Parasitol. 2003;19:293–299. doi: 10.1016/S1471-4922(03)00117-X. PubMed DOI

Hua J., Buss N., Kim J., Orlofske S.A., Hoverman J.T. Population-specific toxicity of six insecticides to the trematode Echinoparyphium sp. Parasitology. 2016;143:542–550. doi: 10.1017/S0031182015001894. PubMed DOI

Gilbert B.M., Avenant-Oldewage A. Effects of altered water quality and trace elements on the infection variables of Paradiplozoon ichthyoxanthon (Monogenea: Diplozoidae) from two sites in the Vaal River system, South Africa. Acta Parasitol. 2016;61:52–62. doi: 10.1515/ap-2016-0005. PubMed DOI

Möller H. Pollution and parasitism in the aquatic environment. Int. J. Parasitol. 1987;17:353–361. doi: 10.1016/0020-7519(87)90110-X. PubMed DOI

Gilbert B.M., Avenant-Oldewage A. Monogeneans as bioindicators: A meta-analysis of effect size of contaminant exposure toward Monogenea (Platyhelminthes) Ecol. Indic. 2021;130:108062. doi: 10.1016/j.ecolind.2021.108062. DOI

Marcogliese D.J. Parasites: Small players with crucial roles in the ecological theatre. EcoHealth. 2004;1:151–164. doi: 10.1007/s10393-004-0028-3. DOI

Blanar C.A., Munkittrick K.R., Houlahan J., MacLatchy D.L., Marcogliese D.J. Pollution and parasitism in aquatic animals: A meta-analysis of effect size. Aquat. Toxicol. 2009;93:18–28. doi: 10.1016/j.aquatox.2009.03.002. PubMed DOI

Koskivaara M., Valtonen E.T., Prost M. Seasonal occurrence of gyrodactylid monogeneans on the roach (Rutilus rutilus) and variations between four lakes of differing water quality in Finland. Aqua Fenn. 1991;21:47–55.

Brázová T., Torres J., Eira C., Hanzelová V., Miklisová D., Šalamún P. Perch and its parasites as heavy metal biomonitors in a freshwater environment: The Case Study of the Ružín Water Reservoir, Slovakia. Sensors. 2012;12:3068–3081. doi: 10.3390/s120303068. PubMed DOI PMC

Pravdova M., Kolarova J., Grabicova K., Mikl L., Blaha M., Randak T., Kvach Y., Jurajda P., Ondrackova M. Associations between pharmaceutical contaminants, parasite load and health status in brown trout exposed to sewage effluent in a small stream. Ecohydrol. Hydrobiol. 2021;21:233–243. doi: 10.1016/j.ecohyd.2020.09.001. DOI

Pravdova M., Kolarova J., Grabicova K., Randak T., Janac M., Kvach Y., Jurajda P., Ondrackova M. Pharmaceutical contamination and biotic factors affecting parasitism in common carp (Cyprinus carpio) Aquacult. Res. 2022;53:4116–4127. doi: 10.1111/are.15913. DOI

Giang P., Sakalli S., Fedorova G., Sarvenaz K.T., Bakal T., Najmanova L., Grabicova K., Kolarova J., Sampels S., Zamaratskaia G., et al. Biomarker response, health indicators, and intestinal microbiome composition in wild brown trout (Salmo trutta m. fario L.) exposed to a sewage treatment plant effluent-dominated stream. Sci. Total Environ. 2018;625:1494–1509. PubMed

Grabicova K., Grabic R., Fedorova G., Stanova A., Blaha M., Randak T., Brooks B., Zlabek V. Water reuse and aquaculture: Pharmaceutical bioaccumulation by fish during tertiary treatment in a wastewater stabilization pond. Environ. Pollut. 2020;267:115593. doi: 10.1016/j.envpol.2020.115593. PubMed DOI

Fedorova G., Grabic R., Grabicova K., Turek J., Van Nguyen T., Randak T., Brooks B.W., Zlabek V. Water reuse for aquaculture: Comparative removal efficacy and aquatic hazard reduction of pharmaceuticals by a pond treatment system during a one-year study. J. Hazard. Mater. 2022;421:126712. doi: 10.1016/j.jhazmat.2021.126712. PubMed DOI

Kares M. Bachelor’s Thesis. University of South Bohemia; Ceske Budejovice, Czech Republic: 2019. Do Fish Kept in a Biological Pond Supplied with Water from a WWTP Meet the Requirements for Hygienic Meat Quality?

Rohlenová K., Morand S., Hyršl P., Tolarová S., Flajšhans M., Šimková A. Are fish immune systems really affected by parasites? An immunoecological study of common carp (Cyprinus carpio) Parasites Vectors. 2011;4:120. doi: 10.1186/1756-3305-4-120. PubMed DOI PMC

Giang P.T., Burkina V., Sakalli S., Schmidt-Posthaus H., Rasmussen M.K., Randak T., Grabic R., Grabicova K., Fedorova G., Koba O., et al. Effects of multi-component mixtures from sewage treatment plant effluent on common carp (Cyprinus carpio) under fully realistic condition. Environ. Manage. 2019;63:466–484. doi: 10.1007/s00267-017-0964-7. PubMed DOI

Koubova A., Van Nguyen T., Grabicova K., Burkina V., Aydin F.G., Grabic R., Novakova P., Svecova H., Lepic P., Fedorova G., et al. Metabolome adaptation and oxidative stress response of common carp (Cyprinus carpio) to altered water pollution levels. Environ. Pollut. 2022;303:119117. doi: 10.1016/j.envpol.2022.119117. PubMed DOI

Ricker W.E. Bulletin of the Fisheries Research Board of Canada. Volume 191. Department of the Environment, Fisheries and Marine Service; Ottawa, ON, Canada: 1975. Computation and interpretation of biological statistics of fish populations; pp. 1–382.

Grabicova K., Vojs Stanova A., Koba Ucun O., Borik A., Randak T., Grabic R. Development of a robust extraction procedure for the HPLC-ESI-HRPS determination of multi-residual pharmaceuticals in biota samples. Anal. Chim. Acta. 2018;1022:53–60. doi: 10.1016/j.aca.2018.04.011. PubMed DOI

Georgiev B., Biserkov V., Genov T. In toto staining method for cestodes with iron acetocarmine. Helminthologia. 1986;23:279–281.

Georgieva S., Soldánová M., Pérez-del-Olmo A., Dangel D.R., Sitko J., Sures B., Kostadinova A. Molecular prospecting for European Diplostomum (Digenea: Diplostomidae) reveals cryptic diversity. Int. J. Parasitol. 2013;43:57–72. doi: 10.1016/j.ijpara.2012.10.019. PubMed DOI

Bauer O.N. Key to the Parasites of Freshwater Fishes of the USSR. Nauka; Leningrad, Russia: 1987. pp. 1–584. (In Russian)

Gusev A.V., Dubinina M.N., Raikova E.V., Khotenkovskiy I.A., Pugachev O.N., Ergens R. Metazoan parasites, Part Monogenea. In: Bauer O.N., editor. Key to the Parasites of Freshwater Fishes of the USSR. Nauka; Leningrad, Russia: 1985. pp. 1–425. (In Russian)

Moravec F. Parasitic Nematodes of Freshwater Fishes of Europe. 2nd ed. Academia Prague; Prague, Czech Republic: 2013. pp. 1–601.

Bush A.O., Lafferty K., Lotz M.J., Shostak A.W. Parasitology meets ecology on its own terms: Margolis et al. Revisited. J. Parasitol. 1997;83:575–583. doi: 10.2307/3284227. PubMed DOI

Magurran A.E. Measuring biological diversity. Cur. Biol. 2021;31:R1174–R1177. doi: 10.1016/j.cub.2021.07.049. PubMed DOI

Hammer R., Harper D.A.T., Ryan P.D. PAST: Paleontological statistics software package for education and data analysis. Palaeontol. Electron. 2001;4:9.

Hothorn T., Bretz F., Westfall P. Simultaneous inference in general parametric models. Biom. J. J. Math. Methods Biosci. 2008;50:346–363. doi: 10.1002/bimj.200810425. PubMed DOI

Doledec S., Chessel D. Co-inertia analysis: An alternative method for studying species-environment relationships. Freshwater Biol. 1994;31:277–294. doi: 10.1111/j.1365-2427.1994.tb01741.x. DOI

Dray S., Chessel D., Thioulouse J. Co-inertia analysis and the linking of ecological data tables. Ecology. 2003;84:3078–3089. doi: 10.1890/03-0178. DOI

R Core Team . R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing; Vienna, Austria: 2021. [(accessed on 22 September 2022)]. Available online: http://www.Rproject.org/

Chapman J.M., Marcogliese D.J., Suski C.D., Cooke S.J. Variation in parasite communities and health indices of juvenile Lepomis gibbosus across a gradient of watershed land-use and habitat quality. Ecol. Indic. 2015;57:564–572. doi: 10.1016/j.ecolind.2015.05.013. DOI

Marcogliese D.J., Gendron A.D., Plante C., Fournier M., Cyr D. Parasites of spottail shiners (Notropis hudsonius) in the St. Lawrence River: Effects of municipal effluents and habitat. Can. J. Zool. 2006;84:1461–1481. doi: 10.1139/z06-088. DOI

Nachev M., Sures B. The endohelminth fauna of barbel (Barbus barbus) correlates with water quality of the Danube River in Bulgaria. Parasitology. 2009;136:545–552. doi: 10.1017/S003118200900571X. PubMed DOI

Wenger M., Ondrackova M., Machala M., Neca J., Hyrsl P., Simkova A., Jurajda P., von der Ohe P., Segner H. Assessing relationships between chemical exposure, parasite infection, fish health, and fish ecological status: A case study using chub (Leuciscus cephalus) in the Bílina River, Czech Republic. Environ. Toxicol. Chem. 2010;29:453–466. doi: 10.1002/etc.57. PubMed DOI

Hanzelová V., Oros M., Scholz T. Pollution and diversity of fish parasites: Impact of pollution on the diversity of fish parasites in the Tisa River in Slovakia. In: Tepper G.H., editor. Species Diversity and Extinction. Nova Science Publishers, Inc.; Hauppauge, NY, USA: 2011. pp. 265–296.

Morley N.J., Lewis J.W., Hoole D. Pollutant-induced effects on immunological and physiological interactions in aquatic host-trematode systems: Implications for parasite transmission. J. Helminthol. 2006;80:137–149. doi: 10.1079/JOH2006345. PubMed DOI

Austin B. The effects of pollution on fish health. J. Appl. Microbiol. 1998;85((Suppl. 1)):234–242. doi: 10.1111/j.1365-2672.1998.tb05303.x. PubMed DOI

Dwivedi A., Seth P.C., Iqbal S.A. Trace metal concentration in ambient air at selected sites of Mandideep Township, in vicinity of Bhopal (India) Pollut. Res. 2001;20:125–128.

Evering T., Weiss L.M. The immunology of parasite infections in immunocompromised hosts. Parasite Immunol. 2006;28:549–565. doi: 10.1111/j.1365-3024.2006.00886.x. PubMed DOI PMC

Buchmann K., Bresciani J. Microenvironment of Gyrodactylus derjavini on rainbow trout Oncorhynchus mykiss: Association between mucous cell density in skin and site selection. Parasitol. Res. 1997;84:17–24. doi: 10.1007/s004360050350. PubMed DOI

Gheorgiu C., Marcogliese D.J., Scott M. Concentration-dependent effects of waterborne zinc on population dynamics of Gyrodactylus turnbulli (Monogenea) on isolated guppies (Poecilia reticulata) Parasitology. 2006;132:225–232. doi: 10.1017/S003118200500898X. PubMed DOI

Bakke T.A., Harris P.D., Jansen P.A. The susceptibility of Salvelinus fontinalis (Mitchill) to Gyrodactylus salaris Malmberg (Platyhelminthes; Monogenea) under experimental conditions. J. Fish Biol. 1992;41:499–507. doi: 10.1111/j.1095-8649.1992.tb02677.x. DOI

Marcogliese D.J., Nagler J.J., Cyr D.G. Effects of exposure to contaminated sediments on the parasite fauna of American plaice (Hippoglossoides platessoides) Bull. Environ. Contamin. Toxicol. 1998;61:88–95. doi: 10.1007/s001289900733. PubMed DOI

Madanire-Moyo G.N., Luus-Powell W.J., Olivier P.A. Diversity of metazoan parasites of the Mozambique tilapia, Oreochromis mossambicus (Peters, 1852), as indicators of pollution in the Limpopo and Olifants River systems. Onderstepoort J. Vet. Res. 2012;79:1–9. doi: 10.4102/ojvr.v79i1.362. PubMed DOI

Shah H.B., Yousuf A.R., Chishti M.Z., Ahmad F. Seasonal changes in infrapopulations of Diplozoon kashmirensis Kaw, 1950 (Monogenea: Diplozoidae) along a eutrophic gradient. Parasitol. Res. 2013;112:3347–3356. doi: 10.1007/s00436-013-3514-0. 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

Vasquez M.I., Lambrianides A., Schneider M., Kümmerer K., Fatta-Kassinos D. Environmental side effects of pharmaceutical cocktails: What we know and what we should know. J. Hazard. Mater. 2014;279:169–189. doi: 10.1016/j.jhazmat.2014.06.069. PubMed DOI

Sueiro M.C., Bagnato E., Palacios M.G. Parasite infection and immune and health-state in wild fish exposed to marine pollution. Mar. Pollut. Bull. 2017;119:320–324. doi: 10.1016/j.marpolbul.2017.04.011. PubMed DOI

Grabicova K., Lindberg R.H., Östman M., Grabic R., Randak T., Larsson D.J. Tissue-specific bioconcentration of antidepressants in fish exposed to effluent from a municipal sewage treatment plant. Sci. Total Environ. 2014;488:46–50. doi: 10.1016/j.scitotenv.2014.04.052. PubMed DOI

Dzieweczynski T.L., Hebert O.L. Fluoxetine alters behavioral consistency of aggression and courtship in male Siamese fighting fish, Betta splendens. Physiol. Behav. 2012;107:92–97. doi: 10.1016/j.physbeh.2012.06.007. PubMed DOI

Barry M.J. Effects of fluoxetine on the swimming and behavioural responses of the Arabian killifish. Ecotoxicology. 2013;22:425–432. doi: 10.1007/s10646-012-1036-7. PubMed DOI

Melvin S.D., Wilson S.P. The utility of behavioral studies for aquatic toxicology testing: A meta-analysis. Chemosphere. 2013;93:2217–2223. doi: 10.1016/j.chemosphere.2013.07.036. PubMed 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. doi: 10.1126/science.1226850. 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. Lond. B Biol. Sci. 2014;369:20130580. doi: 10.1098/rstb.2013.0580. PubMed DOI PMC

Bagge A.M., Valtonen E.T. Experimental study on the influence of paper and pulp mill effluent on the gill parasite communities of roach (Rutilus rutilus) Parasitology. 1996;112:499–508. doi: 10.1017/S0031182000076964. DOI

Najít záznam

Citační ukazatele

Nahrávání dat ...

    Možnosti archivace