{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,8,18]],"date-time":"2026-08-18T17:26:10Z","timestamp":1787073970997,"version":"build-2736575974"},"reference-count":41,"publisher":"Oxford University Press (OUP)","license":[{"start":{"date-parts":[[2026,7,21]],"date-time":"2026-07-21T00:00:00Z","timestamp":1784592000000},"content-version":"am","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by-nc\/4.0\/"}],"funder":[{"name":"Universidad Nacional Aut\u00f3noma de M\u00e9xico Postdoctoral"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"abstract":"<jats:title>Abstract<\/jats:title>\n                  <jats:p>Coastal water pollution is a global problem, especially in karstic areas, where pollutants from point and nonpoint sources reach coastal systems. The Chelem Lagoon in the Yucatan Peninsula exemplifies such environments, where the presence and effects of pollutants have been previously reported. This study presents and evaluates an integrated assessment framework to characterize pollution sources and ecotoxicological impacts in complex coastal systems. This approach combines nutrient concentrations, caffeine (as an urban wastewater tracer), carbon and nitrogen stable isotopes, and a suite of physiological and biochemical biomarkers in the resident fish Sphoeroides testudineus and provides a valuable basis for informing environmental management in karstic environments. The results showed that our integrated approach successfully defined a longitudinal pollution gradient and revealed a complex tissue-specific physiological response in S. testudineus. In the midlagoon (Chuburna area), the presence of caffeine indicated recent or ongoing wastewater inputs. The pollution gradient induced distinct stress profiles. The east (Progreso), characterized by high ammonium concentrations, showed biomarker responses consistent with localized physiological stress, including increased liver protein oxidation. Conversely, the west (accumulation zone), characterized by higher nitrate concentrations and \u03b415N in suspended and sedimentary particulate organic matter, exhibited different biomarker responses, including muscle acetylcholinesterase inhibition, catalase depletion, and higher liver lipid peroxidation. Overall, this integrated multibiomarker framework, using S. testudineus as a sentinel species, provides a useful basis for characterizing complex pollution patterns and assessing wastewater influence in coastal karstic lagoons. This framework is scalable and can support environmental monitoring and management in similar high-priority ecosystems.<\/jats:p>","DOI":"10.1093\/inteam\/vjag118","type":"journal-article","created":{"date-parts":[[2026,7,21]],"date-time":"2026-07-21T12:19:35Z","timestamp":1784636375000},"source":"Crossref","is-referenced-by-count":0,"title":["Integrated assessment of wastewater pollution in a karstic coastal lagoon: Linking nutrients, caffeine, stable isotopes, and fish physiological responses"],"prefix":"10.1093","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-7029-4564","authenticated-orcid":false,"given":"Xurxo","family":"Barral-Pintos","sequence":"first","affiliation":[{"name":"Escuela Nacional de Estudios Superiores Unidad M\u00e9rida, Universidad Nacional Aut\u00f3noma de M\u00e9xico , Uc\u00fa, M\u00e9xico"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-7742-0183","authenticated-orcid":false,"given":"Jorge","family":"Herrera-Silveira","sequence":"additional","affiliation":[{"name":"Unidad M\u00e9rida, Departamento de Recursos Marinos, Centro de Investigaciones y Estudios Avanzados del Instituto Polit\u00e9cnico Nacional , M\u00e9rida,","place":["M\u00e9xico"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-0800-1222","authenticated-orcid":false,"given":"Elsa","family":"Nore\u00f1a-Barroso","sequence":"additional","affiliation":[{"name":"Unidad de Qu\u00edmica Sisal, Facultad de Qu\u00edmica, Universidad Nacional Aut\u00f3noma de M\u00e9xico , Sisal,","place":["M\u00e9xico"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-6260-9653","authenticated-orcid":false,"given":"Gabriela","family":"Gaxiola","sequence":"additional","affiliation":[{"name":"Unidad Multidisciplinaria de Docencia e Investigaci\u00f3n, Facultad de Ciencias, Universidad Nacional Aut\u00f3noma de M\u00e9xico , Sisal,","place":["M\u00e9xico"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-6891-0148","authenticated-orcid":false,"given":"Vanesa","family":"Papiol","sequence":"additional","affiliation":[{"name":"Escuela Nacional de Estudios Superiores Unidad M\u00e9rida, Universidad Nacional Aut\u00f3noma de M\u00e9xico , Uc\u00fa, M\u00e9xico"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"286","published-online":{"date-parts":[[2026,7,21]]},"reference":[{"key":"2026081812345402900_vjag118-B1","first-page":"1","article-title":"Standard procedure for the determination of chlorophyll a by spectroscopic methods","volume":"30","author":"Aminot","year":"2000","journal-title":"ICES Techniques in Marine Environmental Sciences"},{"key":"2026081812345402900_vjag118-B2","volume-title":"PERMANOVA\u2009+\u2009for PRIMER: Guide to software and statistical methods","author":"Anderson","year":"2008"},{"key":"2026081812345402900_vjag118-B3","doi-asserted-by":"publisher","first-page":"58","DOI":"10.1007\/s00128-014-1416-1","article-title":"Impacts of geochemical and environmental factors on seasonal variation of heavy metals in a coastal lagoon Yucatan, Mexico","volume":"94","author":"Arcega-Cabrera","year":"2015","journal-title":"Bulletin of Environmental Contamination and Toxicology"},{"key":"2026081812345402900_vjag118-B4","doi-asserted-by":"publisher","first-page":"1","DOI":"10.31080\/ASNH.2020.04.0659","article-title":"Antioxidant enzymes and their role in preventing cell damage","volume":"4","author":"Bratovcic","year":"2020","journal-title":"Acta Scientific Nutritional Health"},{"key":"2026081812345402900_vjag118-B5","doi-asserted-by":"publisher","first-page":"15967","DOI":"10.1007\/s11356-019-04757-3","article-title":"Water quality in the eastern karst region of the Yucatan Peninsula: Nutrients and stable nitrogen isotopes in turtle grass, Thalassia testudinum","volume":"27","author":"Camacho-Cruz","year":"2020","journal-title":"Environmental Science and Pollution Research International"},{"key":"2026081812345402900_vjag118-B6","doi-asserted-by":"publisher","first-page":"849","DOI":"10.15517\/rbt.v61i2.11229","article-title":"H\u00e1bitos alimenticios de Sphoeroides testudineus (Perciformes: Tetraodontidae) en el sistema lagunar de R\u00eda Lagartos, Yucat\u00e1n, M\u00e9xico","volume":"61","author":"Chi-Esp\u00ednola","year":"2013","journal-title":"Revista de Biolog\u00eda Tropical"},{"key":"2026081812345402900_vjag118-B7","doi-asserted-by":"publisher","first-page":"152","DOI":"10.1016\/j.marpolbul.2013.03.021","article-title":"High congruence of isotope sewage signals in multiple marine taxa","volume":"71","author":"Connolly","year":"2013","journal-title":"Marine Pollution Bulletin"},{"key":"2026081812345402900_vjag118-B8","doi-asserted-by":"publisher","first-page":"939","DOI":"10.3390\/antiox14080939","article-title":"Oxidative stress and neurotoxicity biomarkers in fish toxicology","volume":"14","author":"Formicki","year":"2025","journal-title":"Antioxidants"},{"key":"2026081812345402900_vjag118-B9","doi-asserted-by":"crossref","DOI":"10.1007\/0-387-33745-8","volume-title":"Stable isotope ecology","author":"Fry","year":"2006"},{"key":"2026081812345402900_vjag118-B10","doi-asserted-by":"publisher","first-page":"1387","DOI":"10.1007\/s12237-019-00576-4","article-title":"Site fidelity and habitat use by young-of-the-year transient fishes in salt marsh intertidal creeks","volume":"42","author":"Garwood","year":"2019","journal-title":"Estuaries and Coasts"},{"key":"2026081812345402900_vjag118-B11","doi-asserted-by":"publisher","first-page":"2007","DOI":"10.1007\/s11356-012-0909-x","article-title":"Glutathione, glutathione S-transferase, and glutathione conjugates, complementary markers of oxidative stress in aquatic biota","volume":"19","author":"Hellou","year":"2012","journal-title":"Environmental Science and Pollution Research International"},{"key":"2026081812345402900_vjag118-B12","doi-asserted-by":"publisher","first-page":"11889","DOI":"10.3390\/app142411889","article-title":"Three-year follow-up assessment of anthropogenic contamination in the nichupte lagoon","volume":"14","author":"Herrera-Silveira","year":"2024","journal-title":"Applied Sciences"},{"key":"2026081812345402900_vjag118-B13","doi-asserted-by":"publisher","first-page":"395","DOI":"10.1016\/j.watres.2011.11.003","article-title":"Caffeine as an indicator for the quantification of untreated wastewater in karst systems","volume":"46","author":"Hillebrand","year":"2012","journal-title":"Water Research"},{"key":"2026081812345402900_vjag118-B14","doi-asserted-by":"publisher","first-page":"759","DOI":"10.1016\/j.scitotenv.2018.09.076","article-title":"Significantly depleted 15N in suspended particulate organic matter indicating a strong influence of sewage loading in Daya Bay, China","volume":"650","author":"Ke","year":"2019","journal-title":"The Science of the Total Environment"},{"key":"2026081812345402900_vjag118-B15","doi-asserted-by":"crossref","first-page":"65","DOI":"10.1023\/A:1007481206399","article-title":"Implications of fish home range size and relocation for marine reserve function","volume":"55","author":"Kramer","year":"1999","journal-title":"Environmental Biology of Fishes"},{"key":"2026081812345402900_vjag118-B16","doi-asserted-by":"publisher","DOI":"10.1155\/2013\/321213","volume-title":"Acetylcholinesterase inhibition as a relevant biomarker in environmental biomonitoring: New insights and perspectives","author":"Lionetto","year":"2013"},{"key":"2026081812345402900_vjag118-B17","doi-asserted-by":"publisher","first-page":"711","DOI":"10.1007\/s10695-015-0171-5","article-title":"Contaminant-induced oxidative stress in fish: A mechanistic approach","volume":"42","author":"Lushchak","year":"2016","journal-title":"Fish Physiology and Biochemistry"},{"key":"2026081812345402900_vjag118-B18","doi-asserted-by":"publisher","first-page":"169742","DOI":"10.1016\/j.scitotenv.2023.169742","article-title":"Multiple biomarkers in pufferfish as a proxy of environmental health in Brazilian marine protected areas","volume":"914","author":"Marinsek","year":"2024","journal-title":"The Science of the Total Environment"},{"key":"2026081812345402900_vjag118-B19","doi-asserted-by":"publisher","first-page":"182","DOI":"10.1007\/s00128-021-03428-9","article-title":"Caffeine and paraxanthine as tracers of anthropogenic wastewater in coastal lagoons in Yucatan, Mexico","volume":"108","author":"Mart\u00ednez-Casales","year":"2022","journal-title":"Bulletin of Environmental Contamination and Toxicology"},{"key":"2026081812345402900_vjag118-B20","doi-asserted-by":"publisher","first-page":"1277","DOI":"10.1016\/B978-0-12-372522-6.00029-3","volume-title":"Nitrogen in the marine environment","author":"Montoya","year":"2008","edition":"2nd ed."},{"key":"2026081812345402900_vjag118-B21","doi-asserted-by":"publisher","first-page":"136","DOI":"10.1016\/j.rsma.2018.06.008","article-title":"Spatial heterogeneity and seasonal structure of physical factors and benthic species in a tropical coastal lagoon, Celestun, Yucatan Peninsula","volume":"22","author":"Morelos-Villegas","year":"2018","journal-title":"Regional Studies in Marine Science"},{"key":"2026081812345402900_vjag118-B22","doi-asserted-by":"publisher","first-page":"4109","DOI":"10.1038\/s41598-018-22463-x","article-title":"Habitat degradation alters trophic pathways but not food chain length on shallow Caribbean coral reefs","volume":"8","author":"Morillo-Velarde","year":"2018","journal-title":"Scientific Reports"},{"key":"2026081812345402900_vjag118-B23","doi-asserted-by":"publisher","first-page":"449","DOI":"10.1016\/j.ecss.2007.04.005","article-title":"Isotopic and elemental indicators of nutrient sources and status of coastal habitats in the Caribbean Sea, Yucatan Peninsula, Mexico","volume":"74","author":"Mutchler","year":"2007","journal-title":"Estuarine Coastal and Shelf Science"},{"key":"2026081812345402900_vjag118-B24","doi-asserted-by":"publisher","first-page":"107217","DOI":"10.1016\/j.ecolind.2020.107217","article-title":"Carboxylesterase activities as potential biomarkers of pollution in marine pelagic predators","volume":"122","author":"Nos","year":"2021","journal-title":"Ecological Indicators"},{"key":"2026081812345402900_vjag118-B25","doi-asserted-by":"publisher","first-page":"47","DOI":"10.2166\/wst.2023.182","article-title":"Perspectives and prospects of chelation extraction of heavy metals from wastewater: A review","volume":"88","author":"Nyamato","year":"2023","journal-title":"Water Science and Technology"},{"key":"2026081812345402900_vjag118-B26","doi-asserted-by":"publisher","first-page":"2315","DOI":"10.1016\/j.scitotenv.2008.11.05","article-title":"The checkered puffer (Sphoeroides testudineus) and its helminths as bioindicators of chemical pollution in Yucatan coastal lagoons","volume":"407","author":"Pech","year":"2009","journal-title":"The Science of the Total Environment"},{"key":"2026081812345402900_vjag118-B27","doi-asserted-by":"publisher","first-page":"1160","DOI":"10.1016\/j.scitotenv.2018.04.188","article-title":"The effects of sewage treatment plant effluents on hepatic and intestinal biomarkers in common carp (Cyprinus carpio)","volume":"635","author":"Sakalli","year":"2018","journal-title":"The Science of the Total Environment"},{"key":"2026081812345402900_vjag118-B28","doi-asserted-by":"publisher","first-page":"115091","DOI":"10.1016\/j.marpolbul.2023.115091","article-title":"Influence of pelagic sargassum influxes on the \u03b415N in Thalassia testudinum of the Mexican Caribbean coastal ecosystem","volume":"192","author":"S\u00e1nchez","year":"2023","journal-title":"Marine Pollution Bulletin"},{"key":"2026081812345402900_vjag118-B29","doi-asserted-by":"publisher","first-page":"86","DOI":"10.1016\/j.ecss.2013.01.021","article-title":"Stable nitrogen isotopes in the turtle grass Thalassia testudinum from the Mexican Caribbean: Implications of anthropogenic development","volume":"135","author":"S\u00e1nchez","year":"2013","journal-title":"Estuarine, Coastal and Shelf Science"},{"key":"2026081812345402900_vjag118-B30","doi-asserted-by":"publisher","first-page":"1708","DOI":"10.1016\/j.marpolbul.2006.07.015","article-title":"Esterase activities and lipid peroxidation levels in offshore commercial species of the NW Mediterranean Sea","volume":"52","author":"Sol\u00e9","year":"2006","journal-title":"Marine Pollution Bulletin"},{"key":"2026081812345402900_vjag118-B31","volume-title":"A practical handbook of seawater analysis","author":"Strickland","year":"1972","edition":"2nd"},{"key":"2026081812345402900_vjag118-B32","doi-asserted-by":"publisher","first-page":"666","DOI":"10.1111\/eth.13403","article-title":"No evidence that the widespread environmental contaminant caffeine alters energy balance or stress responses in fish","volume":"129","author":"Tan","year":"2023","journal-title":"Ethology"},{"key":"2026081812345402900_vjag118-B33","doi-asserted-by":"publisher","first-page":"418","DOI":"10.1016\/j.ecss.2007.07.025","article-title":"Water quality variability and eutrophic trends in karstic tropical coastal lagoons of the Yucat\u00e1n Peninsula","volume":"76","author":"Tapia-Gonz\u00e1lez","year":"2008","journal-title":"Estuarine, Coastal and Shelf Science"},{"key":"2026081812345402900_vjag118-B34","author":"Tzeek-Tuz","year":"2013"},{"key":"2026081812345402900_vjag118-B35","doi-asserted-by":"publisher","first-page":"2061","DOI":"10.4319\/lo.2001.46.8.2061","article-title":"Variation in \u03b415N and \u03b413C trophic fractionation: Implications for aquatic food web studies","volume":"46","author":"Vander Zanden","year":"2001","journal-title":"Limnology and Oceanography"},{"key":"2026081812345402900_vjag118-B36","doi-asserted-by":"publisher","first-page":"81","DOI":"10.1016\/j.jembe.2012.07.024","article-title":"The relative importance of mangroves and seagrass beds as feeding areas for resident and transient fishes among different mangrove habitats in Florida and Belize: Evidence from dietary and stable-isotope analyses","volume":"434-435","author":"Vaslet","year":"2012","journal-title":"Journal of Experimental Marine Biology and Ecology"},{"key":"2026081812345402900_vjag118-B37","first-page":"348","volume-title":"Pollution and fish health in tropical ecosystems","author":"Venancio","year":"2014"},{"key":"2026081812345402900_vjag118-B38","doi-asserted-by":"publisher","first-page":"131675","DOI":"10.1016\/j.chemosphere.2021.131675","article-title":"Caffeine as a contaminant of concern: A review on concentrations and impacts in marine coastal systems","volume":"286","author":"Vieira","year":"2022","journal-title":"Chemosphere"},{"key":"2026081812345402900_vjag118-B39","doi-asserted-by":"crossref","first-page":"329","DOI":"10.1002\/(SICI)1099-095X(199805\/06)9:3<329::AID-ENV308>3.0.CO;2-9","article-title":"Characterization of the trophic conditions of marine coastal waters with special reference to the NW Adriatic Sea: Proposal for a trophic scale, turbidity and generalized water quality index","volume":"9","author":"Vollenweider","year":"1998","journal-title":"Environmetrics"},{"key":"2026081812345402900_vjag118-B40","doi-asserted-by":"publisher","first-page":"111","DOI":"10.1006\/ecss.2000.0731","article-title":"The impact of sewage discharge in a marine embayment: A stable isotope reconnaissance","volume":"52","author":"Waldron","year":"2001","journal-title":"Estuarine, Coastal and Shelf Science"},{"key":"2026081812345402900_vjag118-B41","doi-asserted-by":"publisher","first-page":"463","DOI":"10.1017\/S0266467411000277","article-title":"Food-web structure of coastal streams in Costa Rica revealed by dietary and stable isotope analyses","volume":"27","author":"Winemiller","year":"2011","journal-title":"Journal of Tropical Ecology"}],"container-title":["Integrated Environmental Assessment and Management"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/academic.oup.com\/ieam\/advance-article-pdf\/doi\/10.1093\/inteam\/vjag118\/69682886\/vjag118.pdf","content-type":"application\/pdf","content-version":"am","intended-application":"syndication"},{"URL":"https:\/\/academic.oup.com\/ieam\/advance-article-pdf\/doi\/10.1093\/inteam\/vjag118\/69682886\/vjag118.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,8,18]],"date-time":"2026-08-18T16:35:00Z","timestamp":1787070900000},"score":1,"resource":{"primary":{"URL":"https:\/\/academic.oup.com\/ieam\/advance-article\/doi\/10.1093\/inteam\/vjag118\/8739095"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2026,7,21]]},"references-count":41,"URL":"https:\/\/doi.org\/10.1093\/inteam\/vjag118","relation":{},"ISSN":["1551-3777","1551-3793"],"issn-type":[{"value":"1551-3777","type":"print"},{"value":"1551-3793","type":"electronic"}],"subject":[],"published":{"date-parts":[[2026,7,21]]},"article-number":"vjag118"}}