Wastewater effluent affects behaviour and metabolomic endpoints in damselfly larvae
Ternes, T. A. Occurrence of drugs in German sewage treatment plants and rivers. Water Res. 32, 3245–3260 (1998).CAS
Article
Google Scholar
Heberer, T. Occurrence, fate, and removal of pharmaceutical residues in the aquatic environment: A review of recent research data. Toxicol. Lett. 131, 5–17 (2002).CAS
PubMed
Article
Google Scholar
Luo, Y. et al. A review on the occurrence of micropollutants in the aquatic environment and their fate and removal during wastewater treatment. Sci. Total Environ. 473–474, 619–641 (2014).ADS
PubMed
Article
CAS
Google Scholar
Ternes, T., Joss, A. & Oehlmann, J. Occurrence, fate, removal and assessment of emerging contaminants in water in the water cycle (from wastewater to drinking water). Water Res. 72, 1–2 (2015).CAS
PubMed
Article
Google Scholar
Zorita, S., Mårtensson, L. & Mathiasson, L. Occurrence and removal of pharmaceuticals in a municipal sewage treatment system in the south of Sweden. Sci. Total Environ. 407, 2760–2770 (2009).ADS
CAS
PubMed
Article
Google Scholar
Yang, Y., Ok, Y. S., Kim, K.-H., Kwon, E. E. & Tsang, Y. F. Occurrences and removal of pharmaceuticals and personal care products (PPCPs) in drinking water and water/sewage treatment plants: A review. Sci. Total Environ. 596–597, 303–320 (2017).ADS
PubMed
Article
CAS
Google Scholar
Eggen, R. I. L., Hollender, J., Joss, A., Schärer, M. & Stamm, C. Reducing the discharge of micropollutants in the aquatic environment: The benefits of upgrading wastewater treatment plants. Environ. Sci. Technol. 48, 7683–7689 (2014).ADS
CAS
PubMed
Article
Google Scholar
Kümmerer, K., Dionysiou, D. D., Olsson, O. & Fatta-Kassinos, D. Reducing aquatic micropollutants: Increasing the focus on input prevention and integrated emission management. Sci. Total Environ. 652, 836–850 (2019).ADS
PubMed
Article
CAS
Google Scholar
Love, A. C., Crooks, N. & Ford, A. T. The effects of wastewater effluent on multiple behaviours in the amphipod. Gammarus pulex. Environ. Pollut. 267, 115386 (2020).CAS
PubMed
Article
Google Scholar
Rodrigues, C., Guimarães, L. & Vieira, N. Combining biomarker and community approaches using benthic macroinvertebrates can improve the assessment of the ecological status of rivers. Hydrobiolgia 839, 1–24 (2019).CAS
Article
Google Scholar
Previšić, A. et al. Aquatic macroinvertebrates under stress: Bioaccumulation of emerging contaminants and metabolomics implications. Sci. Total Environ. 704, 135333 (2020).ADS
PubMed
Article
CAS
Google Scholar
De Castro-Català, N., Muñoz, I., Riera, J. L. & Ford, A. T. Evidence of low dose effects of the antidepressant fluoxetine and the fungicide prochloraz on the behavior of the keystone freshwater invertebrate Gammarus pulex. Environ. Pollut. 231, 406–414 (2017).PubMed
Article
CAS
Google Scholar
Pisa, L. W. et al. Effects of neonicotinoids and fipronil on non-target invertebrates. Environ. Sci. Pollut. Res. 22, 68–102 (2015).CAS
Article
Google Scholar
Jonsson, M., Fick, J., Klaminder, J. & Brodin, T. Antihistamines and aquatic insects: Bioconcentration and impacts on behavior in damselfly larvae (Zygoptera). Sci. Total Environ. 472, 108–111 (2014).ADS
CAS
PubMed
Article
Google Scholar
Stoks, R. & Córdoba-Aguilar, A. Evolutionary ecology of odonata: A complex life cycle perspective. Annu. Rev. Entomol. 57, 249–265 (2012).CAS
PubMed
Article
Google Scholar
Janssens, L. & Stoks, R. Stronger effects of Roundup than its active ingredient glyphosate in damselfly larvae. Aquat. Toxicol. 193, 210–216 (2017).CAS
PubMed
Article
Google Scholar
Brodin, T. & Johansson, F. Conflicting selection pressures on the growth/predation-risk trade-off in a damselfly. Ecology 85, 2927–2932 (2004).Article
Google Scholar
Smith, B. R. & Blumstein, D. T. Fitness consequences of personality: A meta-analysis. Behav. Ecol. 19, 448–455 (2008).Article
Google Scholar
Monserrat, J. M. et al. Pollution biomarkers in estuarine animals: Critical review and new perspectives. Comp. Biochem. Physiol. Part C 146, 221–234 (2007).
Google Scholar
Ågerstrand, M. et al. Emerging investigator series: Use of behavioural endpoints in the regulation of chemicals. Environ. Sci. Process. Impacts 22, 49–65 (2020).PubMed
Article
Google Scholar
Sardo, A. M. & Soares, A. M. V. M. Assessment of the effects of the pesticide imidacloprid on the behaviour of the aquatic oligochaete Lumbriculus variegatus. Arch. Environ. Contam. Toxicol. 58, 648–656 (2010).CAS
PubMed
Article
Google Scholar
Bossus, M. C., Guler, Y. Z., Short, S. J., Morrison, E. R. & Ford, A. T. Behavioural and transcriptional changes in the amphipod Echinogammarus marinus exposed to two antidepressants, fluoxetine and sertraline. Aquat. Toxicol. 151, 46–56 (2014).CAS
PubMed
Article
Google Scholar
Rodrigues, A. C. M. et al. Behavioural responses of freshwater planarians after short-term exposure to the insecticide chlorantraniliprole. Aquat. Toxicol. 170, 371–376 (2016).CAS
PubMed
Article
Google Scholar
Nielsen, M. E. & Roslev, P. Behavioral responses and starvation survival of Daphnia magna exposed to fluoxetine and propranolol. Chemosphere 211, 978–985 (2018).ADS
CAS
PubMed
Article
Google Scholar
Al-Badran, A. A., Fujiwara, M. & Mora, M. A. Effects of insecticides, fipronil and imidacloprid, on the growth, survival, and behavior of brown shrimp Farfantepenaeus aztecus. PLoS ONE 14, e0223641 (2019).CAS
PubMed
PubMed Central
Article
Google Scholar
Leonard, J. A., Cope, W. G., Barnhart, M. C. & Bringolf, R. B. Metabolomic, behavioral, and reproductive effects of the synthetic estrogen 17 α-ethinylestradiol on the unionid mussel Lampsilis fasciola. Aquat. Toxicol. 150, 103–116 (2014).CAS
PubMed
Article
Google Scholar
Robert Michaud, M. et al. Metabolomics reveals unique and shared metabolic changes in response to heat shock, freezing and desiccation in the Antarctic midge, Belgica antarctica. J. Insect Physiol. 54, 645–655 (2008).CAS
PubMed
Article
Google Scholar
Chou, H., Pathmasiri, W., Deese-Spruill, J., Sumner, S. & Buchwalter, D. B. Metabolomics reveal physiological changes in mayfly larvae (Neocloeon triangulifer) at ecological upper thermal limits. J. Insect Physiol. 101, 107–112 (2017).CAS
PubMed
PubMed Central
Article
Google Scholar
Hidalgo, K., Beaugeard, E., Renault, D., Dedeine, F. & Lécureuil, C. Physiological and biochemical responses to thermal stress vary among genotypes in the parasitic wasp Nasonia vitripennis. J. Insect Physiol. 117, 103909 (2019).PubMed
Article
CAS
Google Scholar
Hines, A., Oladiran, G. S., Bignell, J. P., Stentiford, G. D. & Viant, M. R. Direct sampling of organisms from the field and knowledge of their phenotype: Key recommendations for environmental metabolomics. Environ. Sci. Technol. 41, 3375–3381 (2007).ADS
CAS
PubMed
Article
Google Scholar
Agbo, S. O. et al. Changes in Lumbriculus variegatus metabolites under hypoxic exposure to benzo(a)pyrene, chlorpyrifos and pentachlorophenol: Consequences on biotransformation. Chemosphere 93, 302–310 (2013).ADS
CAS
PubMed
Article
Google Scholar
Venter, L. et al. Uncovering the metabolic response of abalone (Haliotis midae) to environmental hypoxia through metabolomics. Metabolomics 14, 49 (2018).PubMed
Article
CAS
Google Scholar
Melvin, S. D. Short-term exposure to municipal wastewater influences energy, growth, and swimming performance in juvenile Empire Gudgeons (Hypseleotris compressa). Aquat. Toxicol. Amst. Neth. 170, 271–278 (2016).CAS
Article
Google Scholar
Du, S. N. N. et al. Metabolic costs of exposure to wastewater effluent lead to compensatory adjustments in respiratory physiology in bluegill sunfish. Environ. Sci. Technol. 52, 801–811 (2018).ADS
CAS
PubMed
Article
Google Scholar
Mehdi, H., Dickson, F. H., Bragg, L. M., Servos, M. R. & Craig, P. M. Impacts of wastewater treatment plant effluent on energetics and stress response of rainbow darter (Etheostoma caeruleum) in the Grand River watershed. Comp. Biochem. Physiol. B 224, 270–279 (2018).CAS
PubMed
Article
Google Scholar
Simmons, D. B. D. et al. Altered expression of metabolites and proteins in wild and caged fish exposed to wastewater effluents in situ. Sci. Rep. 7, 17000 (2017).ADS
CAS
PubMed
PubMed Central
Article
Google Scholar
McCallum, E. S. et al. Exposure to wastewater effluent affects fish behaviour and tissue-specific uptake of pharmaceuticals. Sci. Total Environ. 605–606, 578–588 (2017).ADS
PubMed
Article
CAS
Google Scholar
Simmons, D. B. D. et al. Reduced anxiety is associated with the accumulation of six serotonin reuptake inhibitors in wastewater treatment effluent exposed goldfish Carassius auratus. Sci. Rep. 7, 17001 (2017).ADS
CAS
PubMed
PubMed Central
Article
Google Scholar
Gauthier, P. T. & Vijayan, M. M. Municipal wastewater effluent exposure disrupts early development, larval behavior, and stress response in zebrafish. Environ. Pollut. 259, 113757 (2020).CAS
PubMed
Article
Google Scholar
Finotello, S., Feckler, A., Bundschuh, M. & Johansson, F. Repeated pulse exposures to lambda-cyhalothrin affect the behavior, physiology, and survival of the damselfly larvae Ischnura graellsii (Insecta; Odonata). Ecotoxicol. Environ. Saf. 144, 107–114 (2017).CAS
PubMed
Article
Google Scholar
Späth, J. et al. Novel metabolomic method to assess the effect-based removal efficiency of advanced wastewater treatment techniques. Environ. Chem. https://doi.org/10.1071/EN19270 (2020).Article
PubMed
PubMed Central
Google Scholar
Späth, J. et al. Oxylipins at intermediate larval stages of damselfly Coenagrion hastulatum as biochemical biomarkers for anthropogenic pollution. Environ. Sci. Pollut. Res. https://doi.org/10.1007/s11356-021-12503-x (2021).Article
Google Scholar
Späth, J. et al. Metabolomics reveals changes in metabolite profiles due to growth and metamorphosis during the on. J. Insect Physiol. 136, 104341 (2022).PubMed
Article
CAS
Google Scholar
Rodriguez, A. et al. ToxTrac: A fast and robust software for tracking organisms. Methods Ecol. Evol. 9, 460–464 (2018).Article
Google Scholar
Treit, D. & Fundytus, M. Thigmotaxis as a test for anxiolytic activity in rats. Pharmacol. Biochem. Behav. 31, 959–962 (1988).CAS
PubMed
Article
Google Scholar
Brodin, T. Behavioral syndrome over the boundaries of life—carryovers from larvae to adult damselfly. Behav. Ecol. 20, 30–37 (2009).Article
Google Scholar
Jonsson, M. et al. High-speed imaging reveals how antihistamine exposure affects escape behaviours in aquatic insect prey. Sci. Total Environ. 648, 1257–1262 (2019).ADS
CAS
PubMed
Article
Google Scholar
Gullberg, J., Jonsson, P., Nordström, A., Sjöström, M. & Moritz, T. Design of experiments: An efficient strategy to identify factors influencing extraction and derivatization of Arabidopsis thaliana samples in metabolomic studies with gas chromatography/mass spectrometry. Anal. Biochem. 331, 283–295 (2004).CAS
PubMed
Article
Google Scholar
Teixeira, P. F. et al. A multi-step peptidolytic cascade for amino acid recovery in chloroplasts. Nat. Chem. Biol. 13, 15–17 (2017).CAS
PubMed
Article
Google Scholar
Rohart, F., Gautier, B., Singh, A. & Cao, K.-A.L. mixOmics: An R package for ‘omics feature selection and multiple data integration. PLOS Comput. Biol. 13, e1005752 (2017).PubMed
PubMed Central
Article
CAS
Google Scholar
Gorrochategui, E., Jaumot, J., Lacorte, S. & Tauler, R. Data analysis strategies for targeted and untargeted LC-MS metabolomic studies: Overview and workflow. TrAC Trends Anal. Chem. 82, 425–442 (2016).CAS
Article
Google Scholar
Chong, J., Wishart, D. S. & Xia, J. Using MetaboAnalyst 40 for comprehensive and integrative metabolomics data analysis. Curr. Protoc. Bioinform. 68, e86 (2019).Article
Google Scholar
Van Gossum, H. et al. Behaviour of damselfly larvae (Enallagma cyathigerum) (Insecta, Odonata) after long-term exposure to PFOS. Environ. Pollut. 157, 1332–1336 (2009).PubMed
Article
CAS
Google Scholar
Bownik, A., Ślaska, B., Bochra, J., Gumieniak, K. & Gałek, K. Procaine penicillin alters swimming behaviour and physiological parameters of Daphnia magna. Environ. Sci. Pollut. Res. 26, 18662–18673 (2019).CAS
Article
Google Scholar
Di Cicco, M. et al. Effects of diclofenac on the swimming behavior and antioxidant enzyme activities of the freshwater interstitial crustacean Bryocamptus pygmaeus (Crustacea, Harpacticoida). Sci. Total Environ. 799, 149461 (2021).ADS
PubMed
Article
CAS
Google Scholar
Di Nica, V., González, A. B. M., Lencioni, V. & Villa, S. Behavioural and biochemical alterations by chlorpyrifos in aquatic insects: An emerging environmental concern for pristine Alpine habitats. Environ. Sci. Pollut. Res. 27, 30918–30926 (2020).Article
CAS
Google Scholar
Cappello, T. et al. Sex steroids and metabolic responses in mussels Mytilus galloprovincialis exposed to drospirenone. Ecotoxicol. Environ. Saf. 143, 166–172 (2017).CAS
PubMed
Article
Google Scholar
Rodrigues, A. C. M. et al. Energetic costs and biochemical biomarkers associated with esfenvalerate exposure in Sericostoma vittatum. Chemosphere 189, 445–453 (2017).ADS
CAS
PubMed
Article
Google Scholar
Ji, C. et al. Proteomic and metabolomic analysis of earthworm Eisenia fetida exposed to different concentrations of 2,2′,4,4′-tetrabromodiphenyl ether. J. Proteom. 91, 405–416 (2013).CAS
Article
Google Scholar
Felten, V. et al. Physiological and behavioural responses of Gammarus pulex (Crustacea: Amphipoda) exposed to cadmium. Aquat. Toxicol. 86, 413–425 (2008).CAS
PubMed
Article
Google Scholar
De Lange, H. J., Peeters, E. T. H. M. & Lürling, M. Changes in ventilation and locomotion of Gammarus pulex (Crustacea, Amphipoda) in response to low concentrations of pharmaceuticals. Hum. Ecol. Risk Assess. Int. J. 15, 111–120 (2009).Article
CAS
Google Scholar
Ashauer, R., Caravatti, I., Hintermeister, A. & Escher, B. I. Bioaccumulation kinetics of organic xenobiotic pollutants in the freshwater invertebrate Gammarus pulex modeled with prediction intervals. Environ. Toxicol. Chem. 29, 1625–1636 (2010).CAS
PubMed
Article
Google Scholar
Schroeder-Spain, K., Fisher, L. L. & Smee, D. L. Uncoordinated: Effects of sublethal malathion and carbaryl exposures on juvenile and adult blue crabs (Callinectes sapidus). J. Exp. Mar. Biol. Ecol. 504, 1–9 (2018).CAS
Article
Google Scholar
Janssens, L. & Stoks, R. Synergistic effects between pesticide stress and predator cues: Conflicting results from life history and physiology in the damselfly Enallagma cyathigerum. Aquat. Toxicol. 132–133, 92–99 (2013).PubMed
Article
CAS
Google Scholar
Ernest, S. K. M. Homeostasis. In Encyclopedia of Ecology (eds Jørgensen, S. E. & Fath, B. D.) 1879–1884 (Academic Press, 2008).Chapter
Google Scholar
Karanova, M. V. & Andreev, A. A. Free amino acids and reducing sugars in the freshwater shrimp Gammarus lacustris (Crustacea, Amphipoda) at the initial stage of preparation to winter season. J. Evol. Biochem. Physiol. 46, 335–340 (2010).CAS
Article
Google Scholar
Maity, S. et al. Starvation causes disturbance in amino acid and fatty acid metabolism in Diporeia. Comp. Biochem. Physiol. B 161, 348–355 (2012).CAS
PubMed
Article
Google Scholar
Cappello, T. et al. Impact of environmental pollution on caged mussels Mytilus galloprovincialis using NMR-based metabolomics. Mar. Pollut. Bull. 77, 132–139 (2013).CAS
PubMed
Article
Google Scholar
Jiang, Y., Jiao, H., Sun, P., Yin, F. & Tang, B. Metabolic response of Scapharca subcrenata to heat stress using GC/MS-based metabolomics. PeerJ 8, e8445 (2020).PubMed
PubMed Central
Article
CAS
Google Scholar
Roznere, I., Watters, G. T., Wolfe, B. A. & Daly, M. Effects of relocation on metabolic profiles of freshwater mussels: Metabolomics as a tool for improving conservation techniques. Aquat. Conserv. Mar. Freshw. Ecosyst. 27, 919–926 (2017).Article
Google Scholar
Cappello, T., Maisano, M., Mauceri, A. & Fasulo, S. 1H NMR-based metabolomics investigation on the effects of petrochemical contamination in posterior adductor muscles of caged mussel Mytilus galloprovincialis. Ecotoxicol. Environ. Saf. 142, 417–422 (2017).CAS
PubMed
Article
Google Scholar
Cao, C. & Wang, W.-X. Chronic effects of copper in oysters Crassostrea hongkongensis under different exposure regimes as shown by NMR-based metabolomics. Environ. Toxicol. Chem. 36, 2428–2435 (2017).CAS
PubMed
Article
Google Scholar
Aru, V., Sarais, G., Savorani, F., Engelsen, S. B. & Cesare Marincola, F. Metabolic responses of clams, Ruditapes decussatus and Ruditapes philippinarum, to short-term exposure to lead and zinc. Mar. Pollut. Bull. 107, 292–299 (2016).CAS
PubMed
Article
Google Scholar
Tufi, S., Stel, J. M., de Boer, J., Lamoree, M. H. & Leonards, P. E. G. Metabolomics to explore imidacloprid-induced toxicity in the central nervous system of the freshwater snail Lymnaea stagnalis. Environ. Sci. Technol. 49, 14529–14536 (2015).ADS
CAS
PubMed
Article
Google Scholar
Tanguy, A., Boutet, I. & Moraga, D. Molecular characterization of the glutamine synthetase gene in the Pacific oyster Crassostrea gigas: Expression study in response to xenobiotic exposure and developmental stage. Biochim. Biophys. Acta BBA 1681, 116–125 (2005).CAS
PubMed
Article
Google Scholar
Chen, X., Shi, X., Gan, F., Huang, D. & Huang, K. Glutamine starvation enhances PCV2 replication via the phosphorylation of p38 MAPK, as promoted by reducing glutathione levels. Vet. Res. 46, 32 (2015).PubMed
PubMed Central
Article
CAS
Google Scholar
Leroy, D., Haubruge, E., De Pauw, E., Thomé, J. P. & Francis, F. Development of ecotoxicoproteomics on the freshwater amphipod Gammarus pulex: Identification of PCB biomarkers in glycolysis and glutamate pathways. Ecotoxicol. Environ. Saf. 73, 343–352 (2010).CAS
PubMed
Article
Google Scholar
Ch, R., Singh, A. K., Pandey, P., Saxena, P. N. & Mudiam, M. K. R. Identifying the metabolic perturbations in earthworm induced by cypermethrin using gas chromatography-mass spectrometry based metabolomics. Sci. Rep. 5, 15674 (2015).ADS
CAS
PubMed
PubMed Central
Article
Google Scholar
Simpson, J. W., Allen, K. & Awapara, J. Free amino acids in some aquatic invertebrates. Biol. Bull. 117, 371–381 (1959).CAS
Article
Google Scholar
Fu, Q., Scheidegger, A., Laczko, E. & Hollender, J. Metabolomic profiling and toxicokinetics modeling to assess the effects of the pharmaceutical diclofenac in the aquatic invertebrate Hyalella azteca. Environ. Sci. Technol. 55, 7920–7929 (2021).ADS
CAS
PubMed
Article
Google Scholar
Tikunov, A. P., Johnson, C. B., Lee, H., Stoskopf, M. K. & Macdonald, J. M. Metabolomic investigations of american oysters using 1H-NMR spectroscopy. Mar. Drugs 8, 2578–2596 (2010).CAS
PubMed
PubMed Central
Article
Google Scholar
Gülçin, İ. Antioxidant and antiradical activities of l-carnitine. Life Sci. 78, 803–811 (2006).PubMed
Article
CAS
Google Scholar
Yuan, D. et al. Ancestral genetic complexity of arachidonic acid metabolism in Metazoa. Biochim. Biophys. Acta 1841, 1272–1284 (2014).CAS
PubMed
Article
Google Scholar
Garreta-Lara, E. et al. Effect of psychiatric drugs on Daphnia magna oxylipin profiles. Sci. Total Environ. 644, 1101–1109 (2018).ADS
CAS
PubMed
Article
Google Scholar
Dwyer, G. K., Stoffels, R. J., Rees, G. N., Shackleton, M. E. & Silvester, E. A predicted change in the amino acid landscapes available to freshwater carnivores. Freshw. Sci. 37, 108–120 (2017).Article
Google Scholar More