Planned intervention: On Thursday 19/09 between 05:30-06:30 (UTC), Zenodo will be unavailable because of a scheduled upgrade in our storage cluster.
Biodiversity Literature Repository
Published November 28, 2018 | Version v1
Journal article Open

Effects of repeated anaesthesia on gill and general health of Atlantic salmon, Salmo salar

Creators

  • 1. Scottish Fish Immunology Research Centre, University of Aberdeen, Aberdeen, UK & Marine Laboratory, Marine Scotland Science, Aberdeen, UK
  • 2. Rowett Institute of Nutrition and Health, University of Aberdeen, Aberdeen, UK Correspondence
  • 3. Marine Laboratory, Marine Scotland Science, Aberdeen, UK
  • 4. Scottish Fish Immunology Research Centre, University of Aberdeen, Aberdeen, UK

Description

Chance, Rachel J., Cameron, Gary A., Fordyce, Mark, Noguera, Patricia, Wang, Tiehui, Collins, Catherine, Secombes, Christopher J., Collet, Bertrand (2018): Effects of repeated anaesthesia on gill and general health of Atlantic salmon, Salmo salar. Journal of Fish Biology 93 (6): 1069-1081, DOI: 10.1111/jfb.13803, URL: http://dx.doi.org/10.1111/jfb.13803

Files

source.pdf

Files (1.5 MB)

Name Size Download all
md5:ef4f9814c3c0eada17406d1b99d687e9
1.5 MB Preview Download

Linked records

Additional details

Identifiers

LSID
urn:lsid:plazi.org:pub:EF4F9814FFC0FFDA17406D1BFFD6FFE9

Cites
Publication: 10.18637/jss.v067.i01 (DOI)
Publication: 10.1016/j.fsi.2018.01.033 (DOI)
Has part
Dataset: http://table.plazi.org/id/CFA001F2FFC4FFDE173A6D9CFB82FF70 (URL)
Figure: 10.5281/zenodo.10928778 (DOI)
Dataset: http://table.plazi.org/id/CFA001F2FFC5FFDF17376D9CFA52FF70 (URL)
Figure: 10.5281/zenodo.10928782 (DOI)
Figure: 10.5281/zenodo.10928784 (DOI)
Figure: 10.5281/zenodo.10928786 (DOI)
Figure: 10.5281/zenodo.10928788 (DOI)
Figure: 10.5281/zenodo.10928790 (DOI)
Figure: 10.5281/zenodo.10928792 (DOI)
Figure: 10.5281/zenodo.10928794 (DOI)

References

  • AQUI-S® New Zealand Ltd. 2018. AQUI-S® ANAESTHETIC. Retrieved from www.aqui-s.com/index.php/aqui-s-products/aqui-s
  • Balamurugan, J., Kumar, T. T. A., Prakash, S., Meenakumari, B., Balasundaram, C., & Harikrishnan, R. (2016). Clove extract: A potential source for stress free transport of fish. Aquaculture, 454, 171-175.
  • Barton, B. A., & Iwama, G. K. (1991). Physiological changes in fish from stress in aquaculture with emphasis on the response and effects of corticosteroids. Annual Review of Fish Diseases, 1, 3-26.
  • Barton, B. A. (2002). Stress in fishes: A diversity of responses with particular reference to changes in circulating corticosteroids. Integrative and Comparative Biology, 42(3), 517-525.
  • Basrur, T. V., Longland, R., & Wilkinson, R. J. (2010). Effects of repeated crowding on the stress response and growth performance in Atlantic salmon (Salmo salar). Fish Physiology and Biochemistry, 36, 445-450.
  • Bates, D., Maechler, M., Bolker, B., & Walker, S. (2015). Fitting linear mixed-effects models using lme4. Journal of Statistical Software, 67, 1-48. https://doi.org/10.18637/jss.v067.i01
  • Boeuf, G., & Prunet, P. (1985). Measurements of gill (Na+ K+)-ATPase activity and plasma thyroid hormones during smoltification in Atlantic salmon (Salmo salar L.). Aquaculture, 45(1-4), 111-119.
  • Bourne, P. K. (1984). The use of MS 222 (tricaine methanesulphonate) as an anaesthetic for routine blood sampling in three species of marine teleost. Aquaculture, 36, 313-321.
  • Braley, H., & Anderson, T. A. (1992). Changes in blood metabolite concentrations in response to repeated capture, anaesthesia and blood sampling in the golden perch, Macquaria ambigua. Comparative Biochemistry and Physiology A, 103, 445-450.
  • Braceland, M., McLoughlin, M. F., Tinsley, J., Wallace, C., Cockerill, D., McLaughlin, M., & Eckersall, P. D. (2015). Serum enolase: a non-destructive biomarker of white skeletal myopathy during pancreas disease (PD) in Atlantic salmon Salmo salar L. Journal of Fish Diseases, 38, 821-831.
  • Bruno, D. W., & Ellis, A. E. (1988). Histopathological effects in Atlantic salmon, Salmo salar L., attributed to the use of tributyltin antifoulant. Aquaculture, 72, 15-20.
  • Burka, J. F., Hammell, K. L., Horsberg, T. E., Johnson, G. R., Rainnie, D. J., & Speare, D. J. (1997). Drugs in salmonid aquaculture-a review. Journal of Veterinary Pharmacology and Therapeutics, 20, 333-349.
  • Chance, R. J., Allcock, Z., Secombes, C. J., Collet, B., & Collins, C. (2018). Effect of repeated exposure to AQUI-S on the viability and growth of Neoparamoeba perurans. Journal of Fish Diseases, 41, 291-298.
  • Collet, B., Urquhart, K., Monte, M., Collins, C., Perez, S. G., Secombes, C. J., & Hall, M. (2015). Individual monitoring of immune response in Atlantic salmon Salmo salar following experimental infection with Infectious Salmon Anaemia Virus (ISAV). PLoS One, 10, e0137767.
  • Davis, K. B., & Griffin, B. R. (2004). Physiological responses of hybrid striped bass under sedation by several anesthetics. Aquaculture, 233 (1-4), 531-548.
  • Davis, M. W., Stephenson, J., & Noga, E. J. (2008). The effect of tricaine on use of the fluorescein test for detecting skin and corneal ulcers in fish. Journal of Aquatic Animal Health, 20(2), 86-95.
  • Durborow, R. M., Crosby, M. D., & Delomas, T. (2015). Proliferative gill disease (Hamburger Gill Disease). Southern Regional Aquaculture Center Publication 475. Washington, DC: US Depatment of Agriculture. Retrieved from www.srac.tamu.edu/serveFactSheet/122
  • Evans, D. H., Piermarini, P. M., & Choe, K. P. (2005). The multifunctional fish gill: Dominant site of gas exchange, osmoregulation, acid-base regulation, and excretion of nitrogenous waste. Physiological Reviews, 85 (1), 97-177.
  • FAO. (2016). The state of world fisheries and aquaculture 2016. Contributing to food security and nutrition for all, (SOFIA). Rome, Italy: Food and Agriculture Organization of the United Nations. Retrieved from http:// www.fao.org/3/a-i5798e.pdf
  • Farbridge, K. J., & Leatherland, J. F. (1992). Plasma growth hormone levels in fed and fasted rainbow trout (Oncorhynchus mykiss) are decreased following handling stress. Fish Physiology and Biochemistry, 10, 67-73.
  • FDA. (2007). Guidance for industry: concerns related to the use of clove oil as an anaesthetic for fish. Center for Veterinary Medicine. VMRCVM Drug Information Laboratory. Washington, DC: U.S. Department of Health and Human Services, Food and Drug Administration. Retrieved from www. fda.gov/downloads/animalveterinary/guidancecomplianceenforcement/ guidanceforindustry/ucm052520.pdf
  • Ferguson, H., Bjerkas, E., & Evensen, O. (2006). Systemic pathology of fish: A text and atlas of normal tissue responses in teleosts and their responses in disease. London, England: Scotian Press.
  • Figueiredo-Fernandes, A., Ferreira-Cardoso, J. V., Garcia-Santos, S., Monteiro, S. M., Carrola, J., Matos, P., & Fontainhas-Fernandes, A. (2007). Histopathological changes in liver and gill epithelium of Nile tilapia, Oreochromis niloticus, exposed to waterborne copper. Pesquisa Veterinaria Brasileira, 27, 103-109.
  • Flecknell, P. (2016). Laboratory animal anaesthesia (4th ed.). Oxford, England: Elsevier.
  • Frances, J., Nowak, B. F., & Allan, G. L. (2000). Effects of ammonia on juvenile silver perch (Bidyanus bidyanus). Aquaculture, 183, 95-103.
  • Gomulka, P., Wlasow, T., Velisek, J., Svobodova, Z., & Chmielinska, E. (2008). Effects of eugenol and MS-222 anaesthesia on Siberian sturgeon Acipenser baerii Brandt. Acta Veterinaria Brno, 77(3), 447-453.
  • Good, C., Davidson, J., Iwanowicz, L., Meyer, M., Dietze, J., Kolpin, D. W., … Summerfelt, S. (2017). Investigating the influence of nitrate nitrogen on post-smolt Atlantic salmon Salmo salar reproductive physiology in freshwater recirculation aquaculture systems.Aquacultural Engineering, 78, 2-8.
  • Hall, M., Collins, C., & Collet, B. (2018). The potential benefits of repeat sampling experiments for fish disease-challenge host-pathogen investigations. Fish & Shellfish Immunology (Online). https://doi.org/10.1016/j. fsi.2018.01.033
  • Hallegraeff, G., Dorantes-Aranda, J. J., Mardones, J., & Seger, A. (2017). Review of progress in our understanding of fish-killing microalgae: Implications for management and mitigation. In L. A. O. Proenca & G. M. Hallegraeff (Eds.), Proceedings of the 17th international conference on harmful algae 2016 (pp. 148-153). Paris, France: Unesco, IOC.
  • HevrOy, E. M., Espe, M., WaagbO, R., Sandnes, K., Ruud, M., & HEMRE, G. I. (2005). Nutrient utilization in Atlantic salmon (Salmo salar L.) fed increased levels of fish protein hydrolysate during a period of fast growth. Aquaculture Nutrition, 11, 301-313.
  • Home Office. (2017). Annual Statistics of Scientific Procedures on Living Animals, Great Britain 2016. Retrieved from https://www.gov.uk/ government/statistics/ statistics-of-scientific-procedures-on-living-animals-great-britain-2016
  • Hong, S., Li, R., Xu, Q., Secombes, C. J., & Wang, T. (2013). Two types of TNF-α exist in teleost fish: Phylogeny, expression, and bioactivity analysis of type-II TNF-α3 in rainbow trout Oncorhynchus mykiss. The Journal of Immunology, 1301584.
  • Hoskonen, P., & Pirhonen, J. (2004). Temperature effects on anaesthesia with clove oil in six temperate-zone fishes. Journal of Fish Biology, 64, 1136-1142.
  • Hoskonen, P., & Pirhonen, J. (2006). Effects of repeated handling, with or without anaesthesia, on feed intake and growth in juvenile rainbow trout, Oncorhynchus mykiss (Walbaum). Aquaculture Research, 37, 409-415.
  • Hunn, J. B., & Allen, J. L. (1974). Movement of drugs across the gills of fishes. Annual Review of Pharmacology, 14, 47-54.
  • Husain, M., Bird, S., van Zwieten, R., Secombes, C. J., & Wang, T. (2012). Cloning of the IL-1β3 gene and IL-1β4 pseudogene in salmonids uncovers a second type of IL-1β gene in teleost fish. Developmental & Comparative Immunology, 38(3), 431-446.
  • Iversen, M., Finstad, B., & Nilssen, K. J. (1998). Recovery from loading and transport stress in Atlantic salmon (Salmo salar L.) smolts. Aquaculture, 168, 387-394.
  • Iversen, M., Finstad, B., McKinley, R. S., & Eliassen, R. A. (2003). The efficacy of metomidate, clove oil, Aqui-S™ and Benzoak as anaesthetics in Atlantic salmon (Salmo salar L.) smolts and their potential stress-reducing capacity. Aquaculture, 221, 549-566.
  • Iversen, M., Finstad, B., McKinley, R. S., Eliassen, R. A., Carlsen, K. T., & Evjen, T. (2005). Stress responses in Atlantic salmon (Salmo salar L.) smolts during commercial well boat transports and effects on survival after transfer to sea. Aquaculture, 243, 373-382.
  • Jiraungkoorskul, W., Upatham, E. S., Kruatrachue, M., Sahaphong, S., Vichasri-Grams, S., & Pokethitiyook, P. (2003). Biochemical and histopathological effects of glyphosate herbicide on Nile tilapia (Oreochromis niloticus). Environmental Toxicology, 18, 260-267.
  • Kibbe, W. A. (2007). OligoCalc: an online oligonucleotide properties calculator. Nucleic Acids Research, 35, W43-W46.
  • Kiessling, A., Johansson,D., Zahl, I. H., & Samuelsen, O. B. (2009). Pharmacokinetics, plasma cortisol and effectiveness of benzocaine, MS-222, and isoeugenol measured in individual dorsal aorta-cannulated Atlantic salmon (Salmo salar) following bath administration.Aquaculture, 286, 301-308.
  • Kiilerich, P., Kristiansen, K., & Madsen, S. S. (2007). Cortisol regulation of ion transporter mRNA in Atlantic salmon gill and the effect of salinity on the signaling pathway. Journal of Endocrinology, 194, 417-427.
  • Kildea, M. A., Allan, G. L., & Kearney, R. E. (2004). Accumulation and clearance of the anaesthetics clove oil and AQUI-S™ from the edible tissue of silver perch (Bidyanus bidyanus). Aquaculture, 232, 265-277.
  • Kolarevic, J., & Terjesen, B. F. (2014). The effect of AQUI-S on nitrogen compound removal efficiency in recirculating aquaculture system (RAS). Nofima Report. TromsO, Norway. Report 48/2014, 1-11. Retrieved from https:// scanvacc.com/wp-content/uploads/2015/09/Nofima-report-032014.pdf
  • Larter, K. F., & Rees, B. B. (2017). Influence of euthanasia method on blood and gill variables in normoxic and hypoxic Gulf killifish Fundulus grandis. Journal of Fish Biology, 90, 2323-2343.
  • Lee, M. H., Yeon, K. Y., Park, C. K., Li, H. Y., Fang, Z., Kim, M. S., … Lee, J. H. (2005). Eugenol inhibits calcium currents in dental afferent neurons. Journal of Dental Research, 84(9), 848-851.
  • Li, H. Y., Park, C. K., Jung, S. J., Choi, S. Y., Lee, S. J., Park, K., … Oh, S. B. (2007). Eugenol inhibits K+ currents in trigeminal ganglion neurons. Journal of Dental Research, 86(9), 898-902.
  • Mallatt, J. (1985). Fish gill structural changes induced by toxicants and other irritants: A statistical review. Canadian Journal of Fisheries and Aquatic Sciences, 42, 630-648.
  • Martinez, C. B. R., Nagae, M. Y., Zaia, C. T. B. V., & Zaia, D. A. M. (2004). Acute morphological and physiological effects of lead in the neotropical fish Prochilodus lineatus. Brazilian Journal of Biology, 64, 797-807.
  • McCormick, S. D., Regish, A., O'Dea, M. F., & Shrimpton, J. M. (2008). Are we missing a mineralocorticoid in teleost fish? Effects of cortisol, deoxycorticosterone and aldosterone on osmoregulation, gill Na+, K +-ATPase activity and isoform mRNA levels in Atlantic salmon. General and Comparative Endocrinology, 157, 35-40.
  • Milligan, C. L., & Wood, C. M. (1982). Disturbances in haematology, fluid volume distribution and circulatory function associated with low environmental pH in the rainbow trout, Salmo gairdneri. Journal of Experimental Biology, 99, 397-415.
  • Mitjana, O., Bonastre, C., Insua, D., Falceto, M. V., Esteban, J., Josa, A., & Espinosa, E. (2014). The efficacy and effect of repeated exposure to 2-phenoxyethanol, clove oil and tricaine methanesulphonate as anesthetic agents on juvenile Angelfish (Pterophyllum scalare). Aquaculture, 433, 491-495.
  • Molinero, A., & Gonzalez, J. (1995). Comparative effects of MS 222 and 2-phenoxyethanol on gilthead sea bream (Sparus aurata L.) during confinement. Comparative Biochemistry and Physiology A, 111, 405-414.
  • Monte, M. M., Urquhart, K., Secombes, C. J., & Collet, B. (2016). Individual monitoring of immune responses in rainbow trout after cohabitation and intraperitoneal injection challenge with Yersinia ruckeri. Fish & Shellfish Immunology, 55, 469-478.
  • Morrison, R. N., Nowak, B. F., & Carson, J. (2001). The histopathological effects of a levamisole-adjuvanted Vibrio anguillarum vaccine on Atlantic salmon (Salmo salar L.). Aquaculture, 195(1-2), 23-33.
  • Morrison, R. N., & Nowak, B. F. (2008). Immunohistochemical detection of anterior gradient-2 in the gills of amoebic gill disease-affected Atlantic salmon, Salmo salar L. Journal of Fish Diseases, 31, 699-705.
  • Murray, L., Rennie, M. D., Enders, E. C., Pleskach, K., & Martin, J. D. (2017). Effect of nanosilver on cortisol release and morphometrics in rainbow trout (Oncorhynchus mykiss). Environmental Toxicology and Chemistry, 36, 1606-1613.
  • Mylonas, C. C., Cardinaletti, G., Sigelaki, I., & Polzonetti-Magni, A. (2005). Comparative efficacy of clove oil and 2-phenoxyethanol as anesthetics in the aquaculture of European sea bass (Dicentrarchus labrax) and gilthead sea bream (Sparus aurata) at different temperatures. Aquaculture, 246, 467-481.
  • NCBI. (2017). Bethesda (MD): National Library of Medicine (US), [1988]. Washington, DC: National Center for Biotechnology Information; Retrieved from https://www.ncbi.nlm.nih.gov/
  • Nilsen, A., Nielsen, K. V., Biering, E., & Bergheim, A. (2017). Effective protection against sea lice during the production of Atlantic salmon in floating enclosures. Aquaculture, 466, 41-50.
  • Oldham, T., Rodger, H., & Nowak, B. F. (2016). Incidence and distribution of amoebic gill disease (AGD)-an epidemiological review. Aquaculture, 457, 35-42.
  • Olsen, Y. A., Einarsdottir, I. E., & Nilssen, K. J. (1995). Metomidate anaesthesia in Atlantic salmon, Salmo salar, prevents plasma cortisol increase during stress. Aquaculture, 134, 155-168.
  • Packer, R. K. (1979). Acid-base balance and gas exchange in brook trout (Salvelinus fontinalis) exposed to acidic environments. Journal of Experimental Biology, 79, 127-134.
  • Palmer, L. M., & Mensinger, A. F. (2004). Effect of the anesthetic tricaine (MS-222) on nerve activity in the anterior lateral line of the oyster toadfish, Opsanus tau. Journal of Neurophysiology, 92, 1034-1041.
  • Park, C. K., Li, H. Y., Yeon, K. Y., Jung, S. J., Choi, S. Y., Lee, S. J., … Oh, S. B. (2006). Eugenol inhibits sodium currents in dental afferent neurons. Journal of Dental Research, 85(10), 900-904.
  • Pelis, R. M., & McCormick, S. D. (2001). Effects of growth hormone and cortisol on Na+-K+-2Cl - cotransporter localization and abundance in the gills of Atlantic salmon. General and Comparative Endocrinology, 124, 134-143.
  • Pettersen, J. M., Bracke, M., Midtlyng, P. J., Folkedal, O., Stien, L. H., Steffenak, H., & Kristiansen, T. S. (2014). Salmon welfare index model 2.0: an extended model for overall welfare assessment of caged Atlantic salmon, based on a review of selected welfare indicators and intended for fish health professionals. Reviews in Aquaculture, 6, 162-179.
  • Pickering, A. D., & Pottinger, T. G. (1988). Lymphocytopenia and the overwinter survival of Atlantic salmon parr, Salmo salar L. Journal of Fish Biology, 32, 689-697.
  • Pirhonen, J., & Schreck, C. B. (2003). Effects of anaesthesia with MS-222, clove oil and CO2 on feed intake and plasma cortisol in steelhead trout (Oncorhynchus mykiss). Aquaculture, 220(1-4), 507-514.
  • Pohlert T. (2014). The pairwise multiple comparison of mean ranks package (PMCMR). Retrieved from http://CRAN.R-project.org/package= PMCMR.
  • Popovic, N. T., Strunjak-Perovic, I., Coz-Rakovac, R., Barisic, J., Jadan, M., Berakovic, A. P., & Klobucar, R. S. (2012). Tricaine methane-sulfonate (MS-222) application in fish anaesthesia. Journal of Applied Ichthyology, 28, 553-564.
  • Posner, L. P., Scott, G. N., & Law, J. M. (2013). Repeated exposure of goldfish (Carassius auratus) to tricaine methanesulfonate (MS-222). Journal of Zoo and Wildlife Medicine, 44, 340-347.
  • Pottinger, T. G. (2008). The stress response in fish-mechanisms, effects and measurement. In E. J. Branson (Ed.), Fish welfare (pp. 32-48). Oxford, England: Blackwell Publishing Ltd.
  • Pretti, C., Chiappe, C., Pieraccini, D., Gregori, M., Abramo, F., Monni, G., & Intorre, L. (2006). Acute toxicity of ionic liquids to the zebrafish (Danio rerio). Green Chemistry, 8, 238-240.
  • R Core Team. (2016). R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing. Retrieved from www.R-project.org/
  • Ramlochansingh, C., Branoner, F., Chagnaud, B. P., & Straka, H. (2014). Efficacy of tricaine methanesulfonate (MS-222) as an anesthetic agent for blocking sensory-motor responses in Xenopus laevis tadpoles. PLoS One, 9(7), e101606.
  • Ranzani-Paiva, M. J. T., Rodrigues, E. L., Veiga, M. L., Eiras, A. C., & Campos, B. E. S. (2003). Differential leucokocyte counts in "dourado", Salminus maxillosus Valenciennes 1840, from the Mogi-GuaCu River, Pirassununga, SP. Brazilian Journal of Biology, 63, 517-525.
  • Readman, G. D., Owen, S. F., Murrell, J. C., & Knowles, T. G. (2013). Do fish perceive anaesthetics as aversive? PLoS One, 8, e73773.
  • Ros, A. F., Bouton, N., Santos, R. S., & Oliveira, R. F. (2006). Alternative male reproductive tactics and the immunocompetence handicap in the Azorean rock-pool blenny, Parablennius parvicornis. Proceedings of the Royal Society B Biological Sciences, 273, 901-909.
  • Rotllant, J., & Tort, L. (1997). Cortisol and glucose responses after acute stress by net handling in the sparid red porgy previously subjected to crowding stress. Journal of Fish Biology, 51, 21-28.
  • Russell, W. M. S., Burch, R. L., & Hume, C. W. (1959). The principles of humane experimental technique. London, England: Methuen.
  • Sanden, M., Bruce, I. J., Rahman, M. A., & Hemre, G. I. (2004). The fate of transgenic sequences present in genetically modified plant products in fish feed, investigating the survival of GM soybean DNA fragments during feeding trials in Atlantic salmon, Salmo salar L. Aquaculture, 237, 391-405.
  • Scott, P. W. (2013). Veterinary work in the field with fish and other aquatic species. Journal of Exotic Pet Medicine, 22, 46-50.
  • de Lima Silva, L., Parodi, T. V., Reckziegel, P., de Oliveira Garcia, V., Burger, M. E., Baldisserotto, B., … Heinzmann, B. M. (2012). Essential oil of Ocimum gratissimum L.: anesthetic effects, mechanism of action and tolerance in silver catfish, Rhamdia quelen. Aquaculture, 350-353, 91-97.
  • Skidmore, J. F., & Tovell, P. W. A. (1972). Toxic effects of zinc sulphate on the gills of rainbow trout. Water Research 217IN1229IN3- 228IN2230IN4,, 6, 217-IN4.
  • Small, B. C., & Chatakondi, N. (2005). Routine measures of stress are reduced in mature channel catfish during and after AQUI-S anesthesia and recovery. North American Journal of Aquaculture, 67, 72-78.
  • Smart, G. (1976). The effect of ammonia exposure on gill structure of the rainbow trout (Salmo gairdneri). Journal of Fish Biology, 8, 471-475.
  • Smith, D. A., Smith, S. A., & Holladay, S. D. (1999). Effect of previous exposure to tricaine methanesulfonate on time to anesthesia in hybrid tilapias. Journal of Aquatic Animal Health, 11, 183-186.
  • Sneddon, L. U., Halsey, L. G., & Bury, N. R. (2017). Considering aspects of the 3Rs principles within experimental animal biology. Journal of Experimental Biology, 220, 3007-3016.
  • Soivio, A., Nyholm, K., & Huhti, M. (1977). Effects of anaesthesia with MS 222, neutralized MS 222 and benzocaine on the blood constituents of rainbow trout, Salmo gairdneri. Journal of Fish Biology, 10, 91-101.
  • Soto, C. G. (1995). Clove oil as a fish anaesthetic for measuring length and weight of rabbitfish (Siganus lineatus). Aquaculture, 136, 149-152.
  • Speare, D. J., & Ferguson, H. W. (1989). Fixation artifacts in rainbow trout (Salmo gairdneri) gills: a morphometric evaluation. Canadian Journal of Fisheries and Aquatic Sciences, 46, 780-785.
  • Thomas, P., & Robertson, L. (1991). Plasma cortisol and glucose stress responses of red drum (Sciaenops ocellatus) to handling and shallow water stressors and anesthesia with MS-222, quinaldine sulfate and metomidate. Aquaculture, 96, 69-86.
  • Treasurer, J., Hannah, F., & Cox, D. (2003). Impact of a phytoplankton bloom on mortalities and feeding response of farmed Atlantic salmon, Salmo salar, in west Scotland. Aquaculture, 218, 103-113.
  • Triebskorn, R., Casper, H., Heyd, A., Eikemper, R., Kohler, H. R., & Schwaiger, J. (2004). Toxic effects of the non-steroidal anti-inflammatory drug diclofenac: Part II. Cytological effects in liver, kidney, gills and intestine of rainbow trout (Oncorhynchus mykiss). Aquatic Toxicology, 68, 151-166.
  • Untergasser, A., Cutcutache, I., Koressaar, T., Ye, J., Faircloth, B. C., Remm, M., & Rozen, S. G. (2012). Primer3--new capabilities and interfaces. Nucleic Acids Research, 40, e115.
  • Urquhart, K., Collins, C., Monte, M., Sokolowska, J., Secombes, C. J., & Collet, B. (2016). Individual measurement of gene expression in blood cells from rainbow trout Oncorhynchus mykiss (Walbaum). Journal Experimental and Applied Animal Science, 2, 1-9.
  • Venables, W. N., & Ripley, B. D. (2002). Modern applied statistics with S (4th ed.). New York, NY: Springer.
  • Wagner, E., Arndt, R., & Hilton, B. (2002). Physiological stress responses, egg survival and sperm motility for rainbow trout broodstock anesthetized with clove oil, tricaine methanesulfonate or carbon dioxide. Aquaculture, 211, 353-366.
  • Wie, M. B., Won, M. H., Lee, K. H., Shin, J. H., Lee, J. C., Suh, H. W., … Kim, Y. H. (1997). Eugenol protects neuronal cells from excitotoxic and oxidative injury in primary cortical cultures. Neuroscience Letters, 225(2), 93-96.
  • Wolf, J. C., Baumgartner, W. A., Blazer, V. S., Camus, A. C., Engelhardt, J. A., Fournie, J. W., … Law, J. M. (2015). Nonlesions, misdiagnoses, missed diagnoses and other interpretive challenges in fish histopathology studies: a guide for investigators, authors, reviewers and readers. Toxicologic Pathology, 43, 297-325.
  • Wong, D., von Keyserlingk, M. A., Richards, J. G., & Weary, D. M. (2014). Conditioned place avoidance of zebrafish (Danio rerio) to three chemicals used for euthanasia and anaesthesia. PLoS One, 9, e88030.