Behavioral and biochemical effects of the antifouler and antidandruff zinc pyrithione on the freshwater fish Gambusia holbrooki

  • Bruno Falcão
  • Márcia Marques
  • Bruno NunesEmail author


The presence of pharmaceutical residues in the aquatic environment is receiving great attention since the levels of these substances have significantly increased in this compartment, potentially leading to adverse ecological effects. Zinc pyrithione (ZnPt) is a widely used organometallic biocide, which is incorporated into antifouling formulas, such as paints, to prevent the establishment of biofilms on surfaces exposed to the aquatic environment. It is also used in cosmetics, such as antidandruff shampoos and soaps. Considering this wide use, and the absence of a significant amount of data on the toxicity of ZnPt especially towards non-target organisms, the objective of this study was to characterize the toxicity of ZnPt, on several ecological relevant endpoints assessed in the fish Gambusia holbrooki. For this purpose, we measured traits related to feeding and aggressive behavior, as well as indicators of oxidative stress (CAT and GSTs), neurotoxicity (AChE), and anaerobic metabolism (LDH), after acute and chronic exposures to ZnPt. In terms of behavioral features, the feeding test showed the occurrence of significant differences between the control animals and those exposed to a concentration of ZnPt of 45 μg/L. In addition, ZnPt caused changes in terms of oxidative stress biomarkers (CAT and GSTs), for both exposure periods. ZnPt was also capable of causing changes in the cholinergic neurotransmission functioning and anaerobic metabolism, but only following the chronic exposure.


Acute and chronic toxicity Biocides Biomarkers Mosquitofish Personal care products 


Funding information

Bruno Nunes was hired through the Investigator FCT program (IF/01744/2013). Thanks are due, for the financial support to CESAM (UID/AMB/50017), to FCT/MEC through national funds, and the co-funding by the FEDER, within the PT2020 Partnership Agreement and Compete 2020.


  1. Abdel-moneim, A., Moreira-Santos, M., & Ribeiro, R. (2015). A short-term sublethal toxicity assay with zebra fish based on preying rate and its integration with mortality.
  2. Aebi H (1984) Oxygen radicals in biological systems. Methods Enzymol 105(1947):121–126. Google Scholar
  3. Ahmad I, Pacheco M, Santos MA (2006) Anguilla anguilla L. oxidative stress biomarkers: an in situ study of freshwater wetland ecosystem (Pateira de Fermentelos, Portugal). Chemosphere 65(6):952–962. Google Scholar
  4. Amara I, Miled W, Slama RB, Ladhari N (2018) Antifouling processes and toxicity effects of antifouling paints on marine environment. A review. Environ Toxicol Pharmacol 57(2017):115–130. Google Scholar
  5. Armstrong RN (1997) Structure, catalytic mechanism, and evolution of the glutathione transferases. Chem Res Toxicol 10(1):2–18Google Scholar
  6. Balzarini V, Taborsky M, Wanner S, Koch F, Frommen JG (2014) Mirror, mirror on the wall: the predictive value of mirror tests for measuring aggression in fish. Behav Ecol Sociobiol 68(5):871–878. Google Scholar
  7. Birben E, Sahiner UM, Sackesen C, Erzurum S, Kalayci O (2012) Oxidative stress and antioxidant defense. World Allergy Organ J 5(1):9–19. Google Scholar
  8. Borg DA, Trombetta LD (2010) Toxicity and bioaccumulation of the booster biocide copper pyrithione, copper 2-pyridinethiol-1-oxide, in gill tissues of Salvelinus fontinalis (brook trout). Toxicol Ind Health 26(3):139–150. Google Scholar
  9. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72(1–2):248–254. Google Scholar
  10. Brandão FP, Rodrigues S, Castro BB, Gonçalves F, Antunes SC, Nunes B (2013) Short-term effects of neuroactive pharmaceutical drugs on a fish species: biochemical and behavioural effects. Aquat Toxicol 144–145:218–229. Google Scholar
  11. Cabral JA, Marques JC (1999) Life history, population dynamics and production of eastern mosquitofish, Gambusia holbrooki (Pisces, Poeciliidae), in rice fields of the lower Mondego River Valley, Western Portugal. Acta Oecol 20(6):607–620. Google Scholar
  12. Cattelan S, Lucon-Xiccato T, Pilastro A, Griggio M (2017) Is the mirror test a valid measure of fish sociability? Anim Behav 127:109–116. Google Scholar
  13. Cleuvers M (2003) Aquatic ecotoxicity of pharmaceuticals including the assessment of combination effects. Toxicol Lett 142(3):185–194. Google Scholar
  14. Colovic MB, Krstic DZ, Lazarevic-Pasti TD, Bondzic AM, Vasic VM (2013) Acetylcholinesterase inhibitors: pharmacology and toxicology. Curr Neuropharmacol 11(3):315–335Google Scholar
  15. Dahm KC d S, Rückert C, Tonial EM, Bonan CD (2006) In vitro exposure of heavy metals on nucleotidase and cholinesterase activities from the digestive gland of Helix aspersa. Comp Biochem Physiol C Toxicol Pharmacol 143(3):316–320. Google Scholar
  16. Dang HM, Inagaki Y, Yamauchi Y, Kurihara T, Vo CH, Sakakibara Y (2017) Acute exposure to 17Α-ethinylestradiol alters aggressive behavior of mosquitofish (Gambusia affinis) toward Japanese medaka (Oryzias latipes). Bull Environ Contam Toxicol 98(5):643–648. Google Scholar
  17. Das UN (2007) Acetylcholinesterase and butyrylcholinesterase as possible markers of low grade systemic inflammation. Med Sci Monit 13:214–221Google Scholar
  18. Daughton CG, Ternes TA (1999) Pharmaceuticals and personal care products in the environment: agents of subtle change? Environ Health Perspect 107(SUPPL. 6):907–938. Google Scholar
  19. Desjardins JK, Fernald RD (2010) What do fish make of mirror images? Biol Lett 6(6):744–747. Google Scholar
  20. Diamantino TC, Almeida E, Soares A, Guilhermino L (2001) Lactate dehydrogenase activity as an effect criterion in toxicity tests with Daphnia magna straus. Chemosphere 45(4–5):553–560. Google Scholar
  21. Ellman GL, Courtney KD, Andres V Jr, Featherstone RM (1961) A new and rapid colorimetric determination of acetylcholinesterase activity. Biochem Pharmacol 7(2):88–95Google Scholar
  22. Elumalai M, Antunes C, Guilhermino L (2007) Enzymatic biomarkers in the crab Carcinus maenas from the Minho River estuary (NW Portugal) exposed to zinc and mercury. Chemosphere 66(7):1249–1255. Google Scholar
  23. Elwood RW, Stoilova V, McDonnell A, Earley RL, Arnott G (2014) Do mirrors reflect reality in agonistic encounters? A test of mutual cooperation in displays. Anim Behav 97:63–67. Google Scholar
  24. Escobar JA, Rubio MA, Lissi EA (1996) SOD and catalase inactivation by singlet oxygen and peroxyl radicals. Free Radic Biol Med 20(3):285–290. Google Scholar
  25. Ferreira G, Simas T, Nobre A, Silva C, Shiffereggen K, Lencart-Silva J (2003) Identification of sensitive areas and vulnerable zones in transitional and coastal Portuguese systems: application of the United States National Estuarine Eutrophication Assessment to the Minho, Lima, Douro, Ria de Aveiro, Mondego, Tagus, Sado, Mira, Ria Formosa and Guadiana systems. INAG/IMARGoogle Scholar
  26. Finkel T, Holbrook NJ (2000) Oxidants, oxidative stress and the biology of ageing. Nature 408(6809):239–247. Google Scholar
  27. Fitridge I, Dempster T, Guenther J, de Nys R (2012) The impact and control of biofouling in marine aquaculture: a review. Biofouling 28(7):649–669. Google Scholar
  28. Fontana BD, Meinerz DL, Rosa LVC, Mezzomo NJ, Silveira A, Giuliani GS, Quadros VA, Filho GLB, Blaser RB, Rosemberg DB (2016) Modulatory action of taurine on ethanol-induced aggressive behavior in zebrafish. Pharmacol Biochem Behav 141:18–27. Google Scholar
  29. Frasco MF, Guilhermino L (2002) Effects of dimethoate and beta-naphthoflavone on selected biomarkers of Poecilia reticulata. Fish Physiol Biochem 26(2):149–156. Google Scholar
  30. Garcia LM, Castro B, Ribeiro R, Guilhermino L (2000) Characterization of cholinesterase from guppy (Poecilia reticulata) muscle and its in vitro inhibition by environmental contaminants. Biomarkers 5(4):274–284. Google Scholar
  31. Gebauer DL, Pagnussat N, Piato ÂL, Schaefer IC, Bonan CD, Lara DR (2011) Effects of anxiolytics in zebrafish: similarities and differences between benzodiazepines, buspirone and ethanol. Pharmacol Biochem Behav 99(3):480–486. Google Scholar
  32. Guilhermino L, Lopes MC, Donato AM, Silveira L, Carvalho AP, Soares AM (1994) Comparative study between the toxicity of 3, 4-dichloroaniline and sodium bromide with 21-days chronic test and using lactate dehydrogenase activity of Daphnia magna Straus. Chemosphere 28(11):2021–2027Google Scholar
  33. Gule NP, Begum NM, Klumperman B (2016) Advances in biofouling mitigation: a review. Crit Rev Environ Sci Technol 46(6):535–555. Google Scholar
  34. Gulick A, Fahl W (1995) Forced evolution of glutathione S-transferase to create a more efficient drug detoxication enzyme. Proc Natl Acad Sci 92:8140–8144. Google Scholar
  35. Gumm JM, Snekser JL, Itzkowitz M (2008) Conservation and conflict between endangered desert fishes. Biol Lett 4(6):655–658. Google Scholar
  36. Gumm JM, Snekser JL, Leese JM, Little KP, Leiser JK, Imhoff VE, Westrick B, Itzkowitz M (2011) Management of interactions between endangered species using habitat restoration. Biol Conserv 144(9):2171–2176. Google Scholar
  37. Habig WH, Pabst MJ, Jakoby WB (1974) Glutathione S-transferases the first enzymatic step in mercapturic acid formation. J Biol Chem 249(22):7130–7139Google Scholar
  38. Hodgson E (ed) (2004) A textbook of modern toxicology. John Wiley & SonsGoogle Scholar
  39. Jurado A, Vàzquez-Suñé E, Carrera J, López de Alda M, Pujades E, Barceló D (2012) Emerging organic contaminants in groundwater in Spain: a review of sources, recent occurrence and fate in a European context. Sci Total Environ 440:82–94. Google Scholar
  40. Kono Y, Fridovich I (1982) Superoxide radical inhibits catalase. J Biol Chem 257(10):5751–5754. Google Scholar
  41. Leticia A-G, Gerardo G-B (2008) Determination of esterase activity and characterization of cholinesterases in the reef fish Haemulon plumieri. Ecotoxicol Environ Saf 71(3):787–797. Google Scholar
  42. Luna-López A, González-Puertos VY, López-Diazguerrero NE, Königsberg M (2014) New considerations on hormetic response against oxidative stress. J Cell Commun Signal 8(4):323–331. Google Scholar
  43. Luo Y, Guo W, Ngo HH, Nghiem LD, Hai FI, Zhang J, Liang S, Wang XC (2014) 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. Google Scholar
  44. MacKie DS, Van Den Berg CMG, Readman JW (2004) Determination of pyrithione in natural waters by cathodic stripping voltammetry. Anal Chim Acta 511(1):47–53. Google Scholar
  45. Maraldo K, Dahllöf I (2004) Indirect estimation of degradation time for zinc pyrithione and copper pyrithione in seawater. Mar Pollut Bull 48(9–10):894–901. Google Scholar
  46. Massoulié J, Perrier N, Noureddine H, Liang D, Bon S (2008) Old and new questions about cholinesterases. Chem Biol Interact 175(1–3):30–44. Google Scholar
  47. Matus GN, Pereira BVR, Silva-Zacarin ECM, Costa MJ, Cordeiro Alves dos Santos A, Nunes B (2018) Behavior and histopathology as biomarkers for evaluation of the effects of paracetamol and propranolol in the neotropical fish species Phalloceros harpagos. Environ Sci Pollut Res 25(28):28601–28618. Google Scholar
  48. Maximino C, Marques De Brito T, De Mattos Dias CAG, Gouveia A, Morato S (2010) Scototaxis as anxiety-like behavior in fish. Nat Protoc 5(2):221–228. Google Scholar
  49. Mochida K, Ito K, Harino H, Tanaka H, Onduka T, Kakuno A, Fujii K (2009) Inhibition of acetylcholinesterase by metabolites of copper pyrithione (CuPT) and its possible involvement in vertebral deformity of a CuPT-exposed marine teleostean fish. Comp Biochem Physiol C Toxicol Pharmacol 149(4):624–630. Google Scholar
  50. Monteiro M, Quintaneiro C, Morgado F, Soares AMVM, Guilhermino F (2005) Characterization of the cholinesterases present in head tissues of the estuarine fish Pomatoschistus microps: application to biomonitoring. Ecotoxicol Environ Saf 62(3):341–347. Google Scholar
  51. Morgan LA, Buttemer WA (1996) Predation by the non-native fish Gambusia holbrooki on small Litoria aurea and L. dentata tadpoles. Aust Zool 30(2):143–149. Google Scholar
  52. Morgan MJ, Kiceniuk JW (1990) Effect of fenitrothion on the foraging behavior of juvenile Atlantic salmon. Environ Toxicol Chem 9(4):489–495. Google Scholar
  53. Morgan DL, Shines CJ, Jeter SP, Wilson RE, Elwell MP, Price HC, Moskowitz PD (1995) Acute pulmonary toxicity of copper gallium diselenide, copper indium diselenide, and cadmium telluride intratracheally instilled into rats. Environ Res 71:16–24. Google Scholar
  54. Naito Y, Masaichi CIL, Kato Y, Nagai R, Yonei Y (2010) Oxidative stress markers. Anti-Aging Med 7(5):36–44Google Scholar
  55. Nelson L, Cox M (2005) Lehninger: principles of biochemistry (4th edn) D. L. Nelson and M. C. Cox, W. H. Freeman & Co., New York, 1119 pp (plus 17 pp glossary), ISBN 0-7167-4339-6 (2004). Cell Biochem Funct 23(4):293–294.
  56. Nogueira AF, Pereira JL, Antunes SC, Gonçalves FJM, Nunes B (2018) Effects of zinc pyrithione on biochemical parameters of the freshwater Asian clam Corbicula fluminea. Aquat Toxicol 204:100–106. Google Scholar
  57. Nunes B (2011) The use of cholinesterases in ecotoxicology. Rev Environ Contam Toxicol 212:29–59. Google Scholar
  58. Nunes B, Carvalho F, Guilhermino L (2004) Acute and chronic effects of clofibrate and clofibric acid on the enzymes acetylcholinesterase, lactate dehydrogenase and catalase of the mosquitofish, Gambusia holbrooki. Chemosphere 57(11):1581–1589. Google Scholar
  59. Nunes B, Carvalho F, Guilhermino L (2005a) Acute toxicity of widely used pharmaceuticals in aquatic species: Gambusia holbrooki, Artemia parthenogenetica and Tetraselmis chuii. Ecotoxicol Environ Saf 61(3):413–419. Google Scholar
  60. Nunes B, Carvalho F, Guilhermino L (2005b) Characterization and use of the total head soluble cholinesterases from mosquitofish (Gambusia holbrooki) for screening of anticholinesterase activity. J Enzyme Inhib Med Chem 20(4):369–376. Google Scholar
  61. Nunes B, Carvalho F, Guilhermino L (2006) Effects of widely used pharmaceuticals and a detergent on oxidative stress biomarkers of the crustacean Artemia parthenogenetica. Chemosphere 62(4):581–594. Google Scholar
  62. Nunes B, Gaio AR, Carvalho F, Guilhermino L (2008) Behaviour and biomarkers of oxidative stress in Gambusia holbrooki after acute exposure to widely used pharmaceuticals and a detergent. Ecotoxicol Environ Saf 71(2):341–354. Google Scholar
  63. Nunes B, Antunes SC, Gomes R, Campos JC, Braga MR, Ramos AS, Correia AT (2015a) Acute effects of tetracycline exposure in the freshwater fish Gambusia holbrooki: antioxidant effects, neurotoxicity and histological alterations. Arch Environ Contam Toxicol 68(2):371–381. Google Scholar
  64. Nunes B, Braga MR, Campos JC, Gomes R, Ramos AS, Antunes SC, Correia AT (2015b) Ecotoxicological effect of zinc pyrithione in the freshwater fish Gambusia holbrooki. Ecotoxicology 24(9):1896–1905. Google Scholar
  65. Nunes B, Caldeira C, Pereira JL, Gonçalves F, Correia AT (2015c) Chronic effects of realistic concentrations of non-essential and essential metals (lead and zinc) on oxidative stress biomarkers of the mosquitofish, Gambusia holbrooki. Arch Environ Contam Toxicol 69(4):586–595. Google Scholar
  66. Nunes B, Caldeira C, Pereira JL, Gonçalves F, Correia AT (2015d) Perturbations in ROS-related processes of the fish Gambusia holbrooki after acute and chronic exposures to the metals copper and cadmium. Environ Sci Pollut Res 22(5):3756–3765. Google Scholar
  67. OECD (1984a) Test no. 203: fish, acute toxicity test. OECD Guidel Test Chem 1(2):1–9Google Scholar
  68. OECD (1984b) OECD guideline for testing of chemicals. Test 204: fish, prolonged toxicity test: 14 day studyGoogle Scholar
  69. Oggier D, Weisbrod C, Stoller A, Zenker A, Fent K (2010) Effects of diazepam on gene expression and link to physiological effects in different life stages in zebrafish Danio rerio. Environ Sci Technol 44(19):7685–7691. Google Scholar
  70. Onduka T, Mochida K, Harino H, Ito K, Kakuno A, Fujii K (2010) Toxicity of metal pyrithione photodegradation products to marine organisms with indirect evidence for their presence in seawater. Arch Environ Contam Toxicol 58(4):991–997. Google Scholar
  71. Oyama TM, Saito M, Yonezawa T, Okano Y, Oyama Y (2012) Nanomolar concentrations of zinc pyrithione increase cell susceptibility to oxidative stress induced by hydrogen peroxide in rat thymocytes. Chemosphere 87(11):1316–1322. Google Scholar
  72. Pandey S, Parvez S, Ansari RA, Ali M, Kaur M, Hayat F, Ahmad F, Raisuddin S (2008) Effects of exposure to multiple trace metals on biochemical, histological and ultrastructural features of gills of a freshwater fish, Channa punctata Bloch. Chem Biol Interact 174(3):183–192Google Scholar
  73. Pessoa PC, Luchmann KH, Ribeiro AB, Veras MM, Correa JRMB, Nogueira AJ, Bainy ACD, Carvalho PSM (2011) Cholinesterase inhibition and behavioral toxicity of carbofuran on Oreochromis niloticus early life stages. Aquat Toxicol 105(3–4):312–320Google Scholar
  74. Polverino G, Liao JC, Porfiri M (2013) Mosquitofish (Gambusia affinis) preference and behavioral response to animated images of conspecifics altered in their color, aspect ratio, and swimming depth. PLoS One 8(1):1–7. Google Scholar
  75. Pyke GH (2005) A review of the biology of Gambusia affinis and G. holbrooki. Rev Fish Biol Fish 15(4):339–365. Google Scholar
  76. Rendón-von Osten J, Ortiz-Arana A, Guilhermino L, Soares AMVM (2005) In vivo evaluation of three biomarkers in the mosquitofish (Gambusia yucatana) exposed to pesticides. Chemosphere 58(5):627–636Google Scholar
  77. Ribeiro S, Guilhermino L, Sousa JP, Soares AMVM (1999) Novel bioassay based on acetylcholinesterase and lactate dehydrogenase activities to evaluate the toxicity of chemicals to soil isopods. Ecotoxicol Environ Saf 44(3):287–293. Google Scholar
  78. Rodrigues S, Antunes SC, Brandão FP, Castro BB, Gonçalves F, Nunes B (2012) Effects of anticholinesterase drugs on biomarkers and behavior of pumpkinseed, Lepomis gibbosus (Linnaeus, 1758). J Environ Monit 14(6):1638–1644. Google Scholar
  79. Roex EWM, Keijzers R, Van Gestel CAM (2003) Acetylcholinesterase inhibition and increased food consumption rate in the zebrafish, Danio rerio, after chronic exposure to parathion. Aquat Toxicol 64(4):451–460. Google Scholar
  80. Rudolf E, Cervinka M (2011) Stress responses of human dermal fibroblasts exposed to zinc pyrithione. Toxicol Lett 204(2–3):164–173. Google Scholar
  81. Sakkas VA, Shibata K, Yamaguchi Y, Sugasawa S, Albanis T (2007) Aqueous phototransformation of zinc pyrithione: degradation kinetics and byproduct identification by liquid chromatography–atmospheric pressure chemical ionisation mass spectrometry. J Chromatogr A 1144(2):175–182Google Scholar
  82. Sandahl JF, Baldwin DH, Jenkins JJ, Scholz NL (2005) Comparative thresholds for acetylcholinesterase inhibition and behavioral impairment in coho salmon exposed to chlorpyrifos. Environ Toxicol Chem 24(1):136. Google Scholar
  83. Schmidt K, Steinberg CEW, Pflugmacher S, Staaks GBO (2004) Xenobiotic substances such as PCB mixtures (Aroclor 1254) and TBT can influence swimming behavior and biotransformation activity (GST) of carp (Cyprinus carpio). Environ Toxicol 19(5):460–470. Google Scholar
  84. Sherratt, P. J., & Hayes, J. D. (2002). Glutathione S-transferases. Enzyme systems that metabolise drugs and other xenobiotics, 319-352.Google Scholar
  85. Silva AS, Santurio JM, Roza LF, Bottari NB, Galli GM, Morsch VM, Schetinger MRC, Baldissera MD, Stefani LM, Radavelli WM, Tomasi T, Boiago MM (2017) Aflatoxins produced by Aspergillus parasiticus present in the diet of quails increase the activities of cholinesterase and adenosine deaminase. Microb Pathog 107:309–312. Google Scholar
  86. Sismeiro-Vivas J, Abrantes N, Pereira JL, Castro BB, Gonçalves F (2007) Short-term effects of Quirlan® (chlorfenvinphos) on the behavior and acetylcholinesterase activity of Gambusia holbrooki. Environ Toxicol Int J 22(2):194–202Google Scholar
  87. Strungaru SA, Robea MA, Plavan G, Todirascu-Ciornea E, Ciobica A, Nicoara M (2018) Acute exposure to methylmercury chloride induces fast changes in swimming performance, cognitive processes and oxidative stress of zebrafish (Danio rerio) as reference model for fish community. J Trace Elem Med Biol 47:115–123. Google Scholar
  88. Tierney KB (2011) Behavioural assessments of neurotoxic effects and neurodegeneration in zebrafish. Biochim Biophys Acta Mol basis Dis 1812(3):381–389. Google Scholar
  89. Timbrell JA (1998) Biomarkers in toxicology. Toxicology 129(1):1–12. Google Scholar
  90. Turley PA, Fenn RJ, Ritter JC, Callow ME (2005) Pyrithiones as antifoulants: environmental fate and loss of toxicity. Biofouling 21(1):31–40. Google Scholar
  91. Vassault A (1983) Lactate dehydrogenase, UV-method with pyruvate and NADH. Methods Enzym Anal 3:118Google Scholar
  92. Vieira LR, Sousa A, Frasco MF, Lima I, Morgado F, Guilhermino L (2008) Acute effects of benzo [a] pyrene, anthracene and a fuel oil on biomarkers of the common goby Pomatoschistus microps (Teleostei, Gobiidae). Sci Total Environ 395(2–3):87–100Google Scholar
  93. Wilson JM, Bunte RM, Carty AJ (2009) Evaluation of rapid cooling and tricaine methanesulfonate (MS222) as methods of euthanasia in zebrafish (Danio rerio). J Am Assoc Lab Anim Sci 48(6):785–789Google Scholar
  94. Wu RSS, Lam PKS (1997) Glucose-6-phosphate dehydrogenase and lactate dehydrogenase in the green-lipped mussel (Perna viridis): possible biomarkers for hypoxia in the marine environment. Water Res 31(11):2797–2801. Google Scholar
  95. Xuereb B, Lefèvre E, Garric J, Geffard O (2009) Acetylcholinesterase activity in Gammarus fossarum (Crustacea Amphipoda): linking AChE inhibition and behavioural alteration. Aquat Toxicol 94(2):114–122. Google Scholar
  96. Yang T-H, Somero GN (1993) Effects of feeding and food deprivation on oxygen consumption, muscle protein concentration and activities of energy metabolism enzymes in muscle and brain of shallow-living (Scorpaena Guttata) and deep-living (Sebastolobus Alascanus) scorpaenid fishes. J Exp Biol 181:213–232Google Scholar
  97. Yebra DM, Kiil S, Dam-Johansen K (2004) Antifouling technology—past, present and future steps towards efficient and environmentally friendly antifouling coatings. Progress in organic coatings 50(2):75–104Google Scholar

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Authors and Affiliations

  1. 1.Departamento de Biologia/CESAMUniversidade de AveiroAveiroPortugal
  2. 2.Centro de Estudos do Ambiente e do Mar (CESAM)Universidade de AveiroAveiroPortugal

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