Skip to main content
Log in

Lethal and sublethal effects in Pink salmon (Oncorhynchus gorbuscha) following exposure to five aquaculture chemotherapeutants

  • Published:
Ecotoxicology Aims and scope Submit manuscript

Abstract

Early life stages of Pink salmon (Oncorhynchus gorbuscha) are at risk of exposure to the active ingredients of chemotherapeutant formulations (hydrogen peroxide [HP], azamethiphos [AZ], emamectin benzoate [EB], cypermethrin [CP] and deltamethrin [DM]) used to control sea lice in salmon aquaculture. LC50 values (95% confidence intervals) for acute 48-h water exposures in order of least to most toxic to seawater-adapted pink salmon fry were: HP (227 [138–418] mg/L), EB (1090 [676–2006] µg/L), AZ (80 [52–161] µg/L), CP (5.1 [3.0–10.5] µg/L), and DM (980 [640–1800] ng/L), and in subchronic 10-d lethality sediment exposure tests: EB (2065 [1384–3720] µg/kg), CP (97 [58–190] µg/kg), and DM (1035 [640–2000] ng/kg). Alterations in behaviour varied between chemicals; no chemical attracted pink salmon fry; fish avoided HP to a limited extent at 50 mg/L), as well as EB (300 µg/L), and AZ (50 µg/L). Significant concentration-dependent decreases in olfactory responsiveness to food extract were seen following AZ, CP and DM exposures that occurred at lower concentrations with longer exposure periods (10 µg/L, 0.5 µg/L and 100 ng/L thresholds at 7 d). Following 10-d sediment exposures, olfaction was only affected by CP exposure at 50 µg/kg. Significant decreases in swimming performance (Ucrit) occured for HP, AZ, CP and DM at concentrations as low as 100 mg/L, 10 µg/L, 2 µg/L and 200 ng/L, respectively. This study provides comprehensive data on the lethal and sublethal effects of aquaculture chemotherapeutant exposure in early life stage pink salmon.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Data availability

Data is available upon request from the corresponding author.

References

  • Abgrall JF (1999) Short and medium term impact of aerial application of insecticide against the winter moth (Operophtera brumata L.). Revue Forestière Française 51(3):395–404. https://doi.org/10.4267/2042/5445

    Article  Google Scholar 

  • Alderman SL, Dilkumar CM, Avey SR, Farrell AP, Kennedy CJ, Gillis TE (2020) Effects of diluted bitumen exposure and recovery on the seawater acclimation response of Atlantic salmon smolts. Aquatic Toxicology 221:105419. https://doi.org/10.1016/j.aquatox.2020.105419

    Article  CAS  Google Scholar 

  • Arndt RE, Wagner EJ (1997) The toxicity of hydrogen peroxide to rainbow trout oncorhynchus mykiss and cutthroat trout oncorhynchus clarki fry and fingerlings. Journal of the World Aquaculture Society 28(2):150–157. https://doi.org/10.1111/j.1749-7345.1997.tb00850.x

    Article  Google Scholar 

  • Beaumont MW, Butler PJ, Taylor EW (1995) Exposure of brown trout, Salmo trutta, to sub-lethal copper concentrations in soft acidic water and its effect upon sustained swimming performance. Aquatic Toxicology 33(1):45–63. https://doi.org/10.1016/0166-445X(95)00007-Q

    Article  CAS  Google Scholar 

  • Benchaoui HA, Mckellar QA (1996) Interaction between fenbendazole and piperonyl butoxide: pharmacokinetic and pharmacodynamic implications. Journal of Pharmacy and Pharmacology 48(7):753–759. https://doi.org/10.1111/j.2042-7158.1996.tb03965.x

    Article  CAS  Google Scholar 

  • Bloodworth JW, Baptie MC, Preedy KF, Best J (2019) Negative effects of the sea lice therapeutant emamectin benzoate at low concentrations on benthic communities around Scottish fish farms. Science of the Total Environment 669:91–102. https://doi.org/10.1016/j.scitotenv.2019.02.430

    Article  CAS  Google Scholar 

  • Boesveldt S, Frasnelli J, Gordon AR, Lundström JN (2010) The fish is bad: negative food odors elicit faster and more accurate reactions than other odors. Biological Psychology 84(2):313–317. https://doi.org/10.1016/j.biopsycho.2010.03.006

    Article  CAS  Google Scholar 

  • Bretaud S, Saglio P, Toutant J-P (2001) Effets du Carbofuran sur l’activite de l’acetylcholinesterase cerebrale et sur l’activite de Nage Chez Carassius Auratus (Cyprinidae) par. Cybium 25(1):33–40

  • Brett JR (1964) The respiratory metabolism and swimming performance of young Sockeye Salmon. Journal of the Fisheries Research Board of Canada 21(5):1183–1226. https://doi.org/10.1139/f64-103

    Article  Google Scholar 

  • Bruno DW, Raynard RS (1994) Studies on the use of hydrogen peroxide as a method for the control of sea lice on Atlantic salmon. Aquaculture International (2):10–18

  • Burka JF, Hammell KL, Horsberg TE, Johnson GR, Rainnie DJ, Speare DJ (1997) Drugs in salmonid aquaculture – A review. Journal of Veterinary Pharmacology and Therapeutics 20(5):333–349. https://doi.org/10.1046/j.1365-2885.1997.00094.x

    Article  CAS  Google Scholar 

  • Burr SA, Ray DE (2004) Structure-activity and interaction effects of 14 different pyrethroids on voltage-gated chloride ion channels. Toxicological Sciences 77(2):341–346. https://doi.org/10.1093/toxsci/kfh027

    Article  Google Scholar 

  • Burridge LE (2013) A review of potential environmental risks associated with the use of pesticides to treat Atlantic salmon against infestations of sea lice in southwest New Brunswick, Canada. DFO Canadian Science Advisory Secretariat Research Document pages 2013/050. iv + 25 p

  • Burridge LE, Van Geest JL (2014) A review of potential environmental risks associated with the use of pesticides to treat Atlantic salmon against infestations of sea lice in Canada. DFO Canadian Science Advisory Secretariat Research Document 2014/002 vi + 36p

  • Burridge LE, Haya K, Zitko V, Waddy S (1999) The lethality of Salmosan (azamethiphos) to American lobster (Homarus americanus) larvae, postlarvae, and adults. Ecotoxicology and Environmental Safety 43(2):165–169. https://doi.org/10.1006/eesa.1999.1771

    Article  CAS  Google Scholar 

  • Burridge LE, Lyons MC, Wong DKH, MacKeigan K, VanGeest JL (2014) The acute lethality of three anti-sea lice formulations: AlphaMax®, Salmosan®, and Interox®ParamoveTM50 to lobster and shrimp. Aquaculture 420–421:180–186. https://doi.org/10.1016/j.aquaculture.2013.10.041

    Article  CAS  Google Scholar 

  • Burridge L, Weis JS, Cabello F, Pizarro J, Bostick K (2010) Chemical use in salmon aquaculture: a review of current practices and possible environmental effects. In Aquaculture 306(1–4):7–23. https://doi.org/10.1016/j.aquaculture.2010.05.020

    Article  CAS  Google Scholar 

  • Cabiscol E, Tamarit J, Ros J (2000) Oxidative stress in bacteria and protein damage by reactive oxygen species. International Microbiology 3(1):3–8. https://doi.org/10.2436/im.v3i1.9235

    Article  CAS  Google Scholar 

  • Çalta M, Ural MŞ (2004) Acute toxicity of the synthetic pyrethroid deltamethrin to young mirror carp, Cyprinus Carpio. Fresenius Environmental Bulletin 13(11 A):1179–1183. www.psp-parlar.de

    Google Scholar 

  • Cengiz EI (2006) Gill and kidney histopathology in the freshwater fish Cyprinus carpio after acute exposure to deltamethrin. Environmental Toxicology and Pharmacology 22(2):200–204. https://doi.org/10.1016/j.etap.2006.03.006

    Article  CAS  Google Scholar 

  • Cengiz EI, Unlu E (2006) Sublethal effects of commercial deltamethrin on the structure of the gill, liver and gut tissues of mosquitofish, Gambusia affinis: a microscopic study. Environmental Toxicology and Pharmacology 21(3):246–253. https://doi.org/10.1016/j.etap.2005.08.005

    Article  CAS  Google Scholar 

  • Chukwudebe AC, Andrew N, Drottar K, Swigert J, Wislocki PG (1996) Bioaccumulation Potential of 4′′-epi-(Methylamino)-4′′-deoxyavermectin B1a Benzoate (Emamectin Benzoate) in Bluegill Sunfish. Journal of Agricultural and Food Chemistry 44:2894–2899

    Article  CAS  Google Scholar 

  • Clark JR, Goodman LR, Borthwick PW, Patrick JM, Cripe GM, Moody PM, Moore JC, Lores EM (1989) Toxicity of pyrethroids to marine invertebrates and fish: A literature review and test results with sediment-sorbed chemicals. Environmental Toxicology and Chemistry 8(5):393–401. https://doi.org/10.1002/etc.5620080505

    Article  CAS  Google Scholar 

  • Costello MJ (2009) How sea lice from salmon farms may cause wild salmonid declines in Europe and North America and be a threat to fishes elsewhere. In Proceedings of the Royal Society B: Biological Sciences (Vol. 276, Issue 1672, pp. 3385–3394). https://doi.org/10.1098/rspb.2009.0771

  • Cripe GM, Goodman LR, Hansen DJ (1984) Effect of chronic exposure to EPN and to Guthion on the critical swimming speed and brain acetylcholinesterase activity of Cyprinodon variegatus. Aquatic Toxicology 5(3):255–266. https://doi.org/10.1016/0166-445X(84)90024-9

    Article  CAS  Google Scholar 

  • da Silva HC, Medina HSG, Fanta E, Bacila M (1993) Sub-lethal effects of the organophosphate folidol 600 (methyl parathion) on Callichthys callichthys (pisces:teleostei). Comparative Biochemistry and Physiology. Part C, Comparative 105(2):197–201. https://doi.org/10.1016/0742-8413(93)90194-P

    Article  Google Scholar 

  • De Aguiar LH, Moraes G, Avilez IM, Altran AE, Corrêa CF (2004) Metabolical effects of Folidol 600 on the neotropical freshwater fish matrinxã, Brycon cephalus. Environmental Research 95(2):224–230. https://doi.org/10.1016/S0013-9351(03)00119-1

    Article  CAS  Google Scholar 

  • DFO (Fisheries and Oceans Canada) (2012) Assessment of the fate of emamectin benzoate, the active ingredient in SLICE®, near aquaculture facilities in British Columbia and its effect on the Pacific spot prawn (Pandaulus platyceros). Canadian Science Advisory Secretariat. Science Advisory Report 2011/082

  • ECCC (Environment and Climate Change Canada), 1992. Biological Test Method: Acute Test for Sediment Toxicity Using Marine or Estuarine Amphipods (EPS1/RM/26 December 1992 (including October 1998 amendments)).

  • ECCC (Environment and Climate Change Canada), 2001. Biological Test Method: Test for Survival and Growth in Sediment Using Spionid Polychaete Worms (Polydora cornuta). EPS 1/RM/41. December 2001.

  • ECCC (Environment and Climate Change Canada), 2017. Biological Test Method: Reference method for determining acute lethality using threespine stickleback. In: EPS 1/RM/10 Second Edition December 2017.

  • Ernst W, Doe K, Cook A, Burridge L, Lalonde B, Jackman P, Aubé JG, Page F (2014) Dispersion and toxicity to non-target crustaceans of azamethiphos and deltamethrin after sea lice treatments on farmed salmon, Salmo salar. Aquaculture 424–425:104–112. https://doi.org/10.1016/j.aquaculture.2013.12.017

    Article  CAS  Google Scholar 

  • Ernst W, Jackman P, Doe K, Page F, Julien G, MacKay K, Sutherland T (2001) Dispersion and toxicity to non-target aquatic organisms of pesticides used to treat sea lice on almon in net pen enclosures. Marine Pollution Bulletin 42(6):432–443. https://doi.org/10.1016/S0025-326X(00)00177-6

    Article  Google Scholar 

  • Fairchild EA, Sulikowski JA, Rennels N, Howell WH, Tsang PCW (2010) Effects of moving acclimation cages before release of cultured fish: Alternate release strategies for a juvenile winter flounder Pseudopleuronectes americanus stock enhancement effort. Aquaculture Research 41(4):602–606. https://doi.org/10.1111/j.1365-2109.2009.02343.x

    Article  Google Scholar 

  • Farrell AP (2008) Comparisons of swimming performance in rainbow trout using constant acceleration and critical swimming speed tests. Journal of Fish Biology 72(3):693–710. https://doi.org/10.1111/j.1095-8649.2007.01759.x

    Article  Google Scholar 

  • Folmar LC (1976) Overt avoidance reaction of rainbow trout fry to nine herbicides. Bulletin of Environmental Contamination and Toxicology 15(5):509–514. https://doi.org/10.1007/BF01685696

    Article  CAS  Google Scholar 

  • Fulton MH, Key PB (2001) Acetylcholinesterase inhibition in estuarine fish and invertebrates as an indicator of organophosphorus insecticide exposure and effects. Environmental Toxicology and Chemistry 20(1):37–45. https://doi.org/10.1002/etc.5620200104

    Article  CAS  Google Scholar 

  • Garibaldi A, Turner N (2004) Cultural keystone species: implications for ecological conservation and restoration. Ecology and Society 9(3). https://doi.org/10.5751/ES-00669-090301

  • Gehrke PC (1988) Acute cardio-respiratory responses of spangled perch, leiopotherapon unicolor (Gunther 1859), to sublethal concentrations of zinc, temephos and 2, 4-d. Marine and Freshwater Research 39(6):767–774. https://doi.org/10.1071/MF9880767

    Article  CAS  Google Scholar 

  • Glickman AH, Lech JJ (1982) Differential toxicity of trans-permethrin in rainbow trout and mice. II. Role of target organ sensitivity. Toxicology and Applied Pharmacology 66(2):162–171. https://doi.org/10.1016/0041-008X(82)90281-2

    Article  CAS  Google Scholar 

  • Godin JGJ (1981) Daily patterns of feeding behavior, daily rations, and diets of juvenile pink salmon (oncorhynchus gorbuscha) in two marine bays of british columbia. Canadian Journal of Fisheries and Aquatic Sciences 38(1):10–15. https://doi.org/10.1139/f81-002

    Article  Google Scholar 

  • Golow AA, Godzi TA (1994) Acute toxicity of deltamethrin and dieldrin to Oreochromis niloticus (LIN). Bulletin of Environmental Contamination and Toxicology 52(3):351–354. https://doi.org/10.1007/BF00197820

    Article  CAS  Google Scholar 

  • Goulding AT, Shelley LK, Ross PS, Kennedy CJ (2013) Reduction in swimming performance in juvenile rainbow trout (Oncorhynchus mykiss) following sublethal exposure to pyrethroid insecticides. Comparative Biochemistry and Physiology - C Toxicology and Pharmacology 157(3):280–286. https://doi.org/10.1016/j.cbpc.2013.01.001

    Article  CAS  Google Scholar 

  • Grant AN (2002) Medicines for sea lice. Pest Management Science 58(6):521–527. https://doi.org/10.1002/ps.481

    Article  CAS  Google Scholar 

  • Gross M, Maycock P, Crane M (2008) Environmental assessment report for Alpha Max according to VICH Phase I and II guidance. Unpublished Report WCA Environment Ltd. Oxfordshire UK. 86

  • Guimarães ATB, Silva de Assis HC, Boeger W (2007) The effect of trichlorfon on acetylcholinesterase activity and histopathology of cultivated fish Oreochromis niloticus. Ecotoxicology and Environmental Safety 68(1):57–62. https://doi.org/10.1016/j.ecoenv.2006.08.005

    Article  CAS  Google Scholar 

  • Hansen DJ, Matthews E, Nall SL, Dumas DP (1972) Avoidance of pesticides by untrained mosquitofish, Gambusia affinis. Bulletin of Environmental Contamination and Toxicology 8(1):46–51. https://doi.org/10.1007/BF01684503

    Article  CAS  Google Scholar 

  • Hansen DJ (1969) Avoidance of pesticides by untrained sheepshead minnows. Transactions of the American Fisheries Society 98(3):426–429. https://doi.org/10.1577/1548-8659(1969)98[426:aopbus]2.0.co;2

    Article  CAS  Google Scholar 

  • Haya K (1989) Toxicity of pyrethroid insecticides to fish. Environmental Toxicology and Chemistry 8(5):381–391. https://doi.org/10.1002/etc.5620080504

    Article  CAS  Google Scholar 

  • Haya K (2001) Environmental impact of chemical wastes produced by the salmon aquaculture industry. ICES Journal of Marine Science 58(2):492–496. https://doi.org/10.1006/jmsc.2000.1034

    Article  CAS  Google Scholar 

  • Haya K, Burridge LE, Davies IM, Ervik A (2005) A Review and Assessment of Environmental Risk of Chemicals Used for the Treatment of Sea Lice Infestations of Cultured Salmon. In Environmental Effects of Marine Finfish Aquaculture (Vol. 5, pp. 305–340). Springer-Verlag. https://doi.org/10.1007/b136016

  • Heard WL (1991) Life History of Pink Salmon. In Pacific Salmon Life Histories (pp. 110–230). https://books.google.com/books?hl=en&lr=&id=I_S0xCME0CYC&oi=fnd&pg=PA121&dq=heard+wild+salmon&ots=_yvGAO5ql3&sig=xv8T3EdegB8pPH13YuaCrbZXKLo

  • Hedayati A, Tarkhani R (2014) Hematological and gill histopathological changes in iridescent shark, Pangasius hypophthalmus (Sauvage, 1878) exposed to sublethal diazinon and deltamethrin concentrations. Fish Physiology and Biochemistry. 40(3):715–720

  • Hemmera (Hemmera Envirochem Inc.). 2014. Roberts Bank Terminal 2 Technical Data Report. Coastal Waterbirds – Shorebird Abundance and Foraging Use in the Fraser River Estuary during Migration. Appendix A. Prepared for Port Metro Vancouver. December 2014.

  • Hemmera Envirochem Inc (2017) Boundary Bay Assessment and Monitoring Program: Review and Recommendations Based on Monitoring Results from 2009 to 2015. Commissioned by Metro Vancouver. Burnaby, BC: Metro Vancouver

  • Heuch PA, Bjørn PA, Finstad B, Holst JC, Asplin L, Nilsen F (2005) A review of the Norwegian “National Action Plan Against Salmon Lice on Salmonids”: The effect on wild salmonids. Aquaculture 246(1–4):79–92. https://doi.org/10.1016/j.aquaculture.2004.12.027

    Article  Google Scholar 

  • Hidaka H, Tatsukawa R (1989) Avoidance by olfaction in a fish, medaka (Oryzias latipes), to aquatic contaminants. Environmental Pollution 56(4):299–309. https://doi.org/10.1016/0269-7491(89)90075-4

    Article  CAS  Google Scholar 

  • Howard TE (1975) Swimming performance of juvenile coho salmon (Oncorhynchus kisutch) exposed to bleached kraft pulpmill effluent. Journal of the Fisheries Research Board of Canada 32(6):789–793. https://doi.org/10.1139/f75-103

    Article  CAS  Google Scholar 

  • Intorre L, Soldani G, Cognetti-Varriale AM, Monni G, Meucci V, Pretti C (2004) Safety of azamethiphos in eel, seabass and trout. Pharmacological Research 49(2):171–176. https://doi.org/10.1016/j.phrs.2003.08.002

    Article  CAS  Google Scholar 

  • Kaczynski VW, Feller RJ, Clayton J, Gerke RJ (1973) Trophic analysis of juvenile pink and chum salmon (Otzcoriyncitus gorbuseha and 0. keta) in Puget Sound. J. Fish. Res. Board Can. 30:1003–1008

    Article  Google Scholar 

  • Katharios P, Iliopoulou-Georgudaki J, Kapata-Zoumbos K, Spiropoulos S (2001) Toxicity of intraperitoneally injected ivermectin in sea bream, Sparus aurata. Fish Physiology and Biochemistry 25(2):99–108. https://doi.org/10.1023/A:1020574810332

    Article  CAS  Google Scholar 

  • Kennedy CJ, Farrell AP (2006) Effects of exposure to the water-soluble fraction of crude oil on the swimming performance and the metabolic and ionic recovery postexcercise in pacific herring (Clupea Pallasi). Environmental Toxicology and Chemistry 25(10):2715–2724

  • Kennedy CJ, Tierney KB, Mittelstadt M (2014) Inhibition of P-glycoprotein in the blood-brain barrier alters avermectin neurotoxicity and swimming performance in rainbow trout. Aquatic Toxicology 146:176–185. https://doi.org/10.1016/j.aquatox.2013.10.035

    Article  CAS  Google Scholar 

  • Kiemer MCB, Black KD (1997) The effects of hydrogen peroxide on the gill tissues of Atlantic salmon, Salmo salar L. Aquaculture 153(3–4):181–189. https://doi.org/10.1016/S0044-8486(97)00037-9

    Article  CAS  Google Scholar 

  • Kim Y, Jung J, Oh S, Choi K (2008) Aquatic toxicity of cartap and cypermethrin to different life stages of Daphnia magna and Oryzias latipes. Journal of Environmental Science and Health - Part B Pesticides, Food Contaminants, and Agricultural Wastes 43(1):56–64. https://doi.org/10.1080/03601230701735029

    Article  CAS  Google Scholar 

  • Köprücü SS, Köprücü K, Ural MS (2006) Acute toxicity of the synthetic pyrethroid deltamethrin to fingerling european catfish, Silurus glanis L. Bull. Environ. Contam. Toxicol 76:59–65. https://doi.org/10.1007/s00128-005-0889-3

    Article  CAS  Google Scholar 

  • Krkošek M, Ford JS, Morton A, Lele S, Myers RA, Lewis MA (2007) Declining wild salmon populations in relation to parasites from farm salmon. Science 318(5857):1772–1775. https://doi.org/10.1126/science.1148744

    Article  CAS  Google Scholar 

  • Krkošek M, Lewis MA, Volpe JP (2005) Transmission dynamics of parasitic sea lice from farm to wild salmon. Proceedings of the Royal Society B: Biological Sciences 272(1564):689–696. https://doi.org/10.1098/rspb.2004.3027

  • Kumar A, Chapman JC (1998) Profenofos Toxicity to the Eastern Rainbow Fish (Melanotaenia Duboulayi). Environmental Toxicology and Chemistry 17(9):1799–1806

  • Kumaraguru AK, Beamish FWH (1983) Bioenergetics of acclimation to permethrin (NRDC-143) by rainbow trout. Comparative Biochemistry and Physiology. Part C, Comparative 75(2):247–252. https://doi.org/10.1016/0742-8413(83)90188-3

    Article  CAS  Google Scholar 

  • Kumaraguru AK, Beamish FWH (1986) Effect of permethrin (NRDC-143) on the bioenergetics of rainbow trout, Salmo gairdneri. Aquatic Toxicology 9(1):47–58. https://doi.org/10.1016/0166-445X(86)90005-6

    Article  CAS  Google Scholar 

  • Kynard B (1974) Avoidance Behavior of Insecticide Susceptible and Resistant Populations of Mosquitofish to Four Insecticides. Transactions of the American Fisheries Society 103(3):557–561. https://doi.org/10.1577/1548-8659(1974)103<557:ABOISA>2.0.CO;2

    Article  CAS  Google Scholar 

  • Lin F, Baillon L, Langlois V, Kennedy C (2021) Environmental modulators of diluted bitumen effects in juvenile pink salmon (Oncorhynchus gorbuscha). Mar. Environ. Res. 169:105392

    Article  CAS  Google Scholar 

  • Liou G-Y, Storz P (2010) Reactive oxygen species in cancer. Free Radical Research 44(5):479–496. https://doi.org/10.3109/10715761003667554

    Article  CAS  Google Scholar 

  • Little EE, Archeski RD, Flerov BA, Kozlovskaya VI (1990) Behavioral indicators of sublethal toxicity in rainbow trout. In Arch. Environ. Contam. Toxicol (19)

  • Lumaret J-P, Errouissi F, Floate K, Rombke J, Wardhaugh K (2012) A Review on the toxicity and non-target effects of macrocyclic lactones in terrestrial and aquatic environments. Current Pharmaceutical Biotechnology 13(6):1004–1060. https://doi.org/10.2174/138920112800399257

    Article  CAS  Google Scholar 

  • Mackinnon DL, Farrell AP (1992) The effect of on juvenile Coho salmon (Oncorhynchus kisutch): sublethal toxicity testing 2-(thiocyanomethylthio) benzothiazole. In Environmental Toxicology and Chemistry (11):1541–1548

  • McHenery JG, Mackie CM, (1999). Revised expert report on the potential environmental impacts of emamectin benzoate, formulated as Slice® for salmonids. Cordah Report No. SCH001R5

  • McKenzie DJ, Blasco FR, Belão TC, Killen SS, Martins ND, Taylor EW, Rantin FT (2017) Physiological determinants of individual variation in sensitivity to an organophosphate pesticide in Nile tilapia Oreochromis niloticus. Aquatic Toxicology 189:108–114. https://doi.org/10.1016/j.aquatox.2017.06.001

    Article  CAS  Google Scholar 

  • Mcleese DW, Metcalfe CD, Zitko V (1980) Lethality of permethrin, cypermethrin and fenvalerate to salmon, lobster and shrimp. Bull. Environm. Contam. Toxicol 25:950–955

    Article  CAS  Google Scholar 

  • Moore A, Waring CP (1998) Mechanistic effects of a triazine pesticide on reproductive endocrine function in mature male Atlantic salmon (Salmo salar L.) parr. Pesticide Biochemistry and Physiology 62(1):41–50. https://doi.org/10.1006/pest.1998.2366

    Article  CAS  Google Scholar 

  • Moore A, Waring CP (2001) The effects of a synthetic pyrethroid pesticide on some aspects of reproduction in Atlantic salmon (Salmo salar L.). Aquatic Toxicology 52(1):1–12. https://doi.org/10.1016/S0166-445X(00)00133-8

    Article  CAS  Google Scholar 

  • Mustafa A, Rankaduwa W, Campbell P (2001) Estimating the cost of sea lice to salmon aquaculture in eastern Canada. Canadian Veterinary Journal 42(1):54–56

    CAS  Google Scholar 

  • Nendick L, Grant A, Gardner M, Sackville M, Brauner CJ, Farrell AP (2009) Swimming performance and associated ionic disturbance of juvenile pink salmon Oncorhynchus gorbuscha determined using different acceleration profiles. Journal of Fish Biology 75(7):1626–1638. https://doi.org/10.1111/j.1095-8649.2009.02388.x

    Article  CAS  Google Scholar 

  • Nikl DL, Farrell AP (1993) Reduced swimming performance and gill structural changes in juvenile salmonids exposed to 2-(thiocyanomethylthio)benzothiazole. Aquatic Toxicology 27(3–4):245–263. https://doi.org/10.1016/0166-445X(93)90057-8

    Article  CAS  Google Scholar 

  • Osachoff HL, Osachoff KN, Wickramaratne AE, Gunawardane EK, Venturini FP, Kennedy CJ (2014) Altered burst swimming in rainbow trout Oncorhynchus mykiss exposed to natural and synthetic oestrogens. Journal of Fish Biology 85:210–227. https://doi.org/10.1111/jfb.12403

    Article  CAS  Google Scholar 

  • Overton K, Samsing F, Oppedal F, Dalvin S, Stien LH, Dempster T (2018) The use and effects of hydrogen peroxide on salmon lice and post-smolt Atlantic salmon. Aquaculture 486:246–252. https://doi.org/10.1016/j.aquaculture.2017.12.041

    Article  CAS  Google Scholar 

  • Park A (2013) The biological effects of emamectin benzoate (Slice®) on spot prawn (Pandalus platyceros). University of Victoria

  • Peterson RH (1974) Influence of fenitrothion on swimming velocities of brook trout (Salvelinus fontinalis). Journal of the Fisheries Research Board of Canada 31(11):1757–1762. https://doi.org/10.1139/f74-223

    Article  CAS  Google Scholar 

  • Philip GH, Anuradha J (1996) Role of phosphatases during transport and energy metabolism in Labeo rohita after exposure to cypermethrin. Biomedical and Environmental Sciences: BES 9(1):52–59

    CAS  Google Scholar 

  • Plaut I (2001) Critical swimming speed: Its ecological relevance. Comparative Biochemistry and Physiology - A Molecular and Integrative Physiology 131(1):41–50. https://doi.org/10.1016/S1095-6433(01)00462-7

    Article  CAS  Google Scholar 

  • PMRA (Pest Management Regulatory Agency) (2014) Proposed Registration Document PRD2014-11 : Hydrogen Peroxide. Pest Management Regulatory Agency. Health Canada. Ottawa, ON. 40pp

  • PMRA (Pest Management Regulatory Agency) (2016) Registration Decision RD2016-18, Hyrodgen Peroxide. Retrieved 25, November 2018 from https://www.canada.ca/en/health-canada/services/consumer-product-safety/reports-publications/pesticides-pest-management/decisions-updates/registration-decision/2016/hydrogenperoxide-2016

  • PMRA (Pest Management Regulatory Agency) (2017) Registration Decision RD2017-13, Azamethiphos. Retrieved 25, November 2018 from https://www.canada.ca/en/health-canada/services/consumer-product-safety/reports-publications/pesticides-pest-management/decisions-updates/registration-decision/2017/azamethiphos-2017

  • Quinn TP, Myers KW (2004) Anadromy and the marine migrations of Pacific salmon and trout: Rounsefell revisited. In Reviews in Fish Biology and Fisheries 14(Issue 4):421–442. https://doi.org/10.1007/s11160-005-0802-5

    Article  Google Scholar 

  • Rajotte JW, Couture P (2002) Effects of environmental metal contamination on the condition, swimming performance, and tissue metabolic capacities of wild yellow perch (Perca flavescens). Canadian Journal of Fisheries and Aquatic Sciences 59(8):1296–1304. https://doi.org/10.1139/f02-095

    Article  CAS  Google Scholar 

  • Rand G, Kleerekoper H, Matis J (1975) Interaction of odour and flow perception and the effects of parathion in the locomotor orientation of the goldfish Carassius auratus L. Journal of Fish Biology 7(4):497–504. https://doi.org/10.1111/j.1095-8649.1975.tb04624.x

    Article  CAS  Google Scholar 

  • Reddy VS (2012). Effect of general anesthetics on the developing brain. In Journal of Anaesthesiology Clinical Pharmacology (Vol. 28, Issue 1, pp. 6–10). Wolters Kluwer–Medknow Publications. https://doi.org/10.4103/0970-9185.92426

  • Roy WJ, Sutherland IH, Rodger HDM, Varma KJ (2000) Tolerance of Atlantic salmon, Salmo salar L., and rainbow trout, Oncorhynchus mykiss (Walbaum), to emamectin benzoate, a new orally administered treatment for sea lice. Aquaculture 184(1–2):19–29. https://doi.org/10.1016/S0044-8486(99)00307-5

    Article  CAS  Google Scholar 

  • Saglio P, Olsén KH, Bretaud S (2001) Behavioral and olfactory responses to prochloraz, bentazone, and nicosulfuron-contaminated flows in goldfish. Arch. Environ. Contam. Toxicol 41:192–200. https://doi.org/10.1007/s002440010237

    Article  CAS  Google Scholar 

  • Saha S, Kaviraj A (2003) Acute toxicity of synthetic pyrethroid cypermethrin to some freshwater organisms. Bulletin of Environmental Contamination and Toxicology 80:49–52

    Article  Google Scholar 

  • Saha S, Kaviraj A (2008) Acute toxicity of synthetic pyrethroid cypermethrin to some freshwater organisms. Bulletin of Environmental Contamination and Toxicology 80(1):49–52. https://doi.org/10.1007/s00128-007-9314-4

    Article  CAS  Google Scholar 

  • Saito Y, Nishio K, Ogawa Y, Kimata J, Kinumi T, Yoshida Y, Noguchi N, Niki E (2006) Turning point in apoptosis/necrosis induced by hydrogen peroxide. Free Radical Research 40(6):619–630. https://doi.org/10.1080/10715760600632552

    Article  CAS  Google Scholar 

  • Sandahl JF, Baldwin DH, Jenkins JJ, Scholz NL (2004) Odor-evoked field potentials as indicators of sublethal neurotoxicity in juvenile coho salmon (Oncorhynchus kisutch) exposed to copper, chlorpyrifos, or esfenvalerate. Canadian Journal of Fisheries and Aquatic Sciences 61(3):404–413. https://doi.org/10.1139/F04-011

    Article  CAS  Google Scholar 

  • Scherer E (1975) Avoidance of fenitrothion by goldfish (Carassius auratus). Bulletin of Environmental Contamination and Toxicology 13(4):492–496. https://doi.org/10.1007/BF01721858

    Article  CAS  Google Scholar 

  • Schindler D (2003) Pacific salmon and coastal ecology. Frontiers in Ecology and the Environment 1(1):31–37. https://doi.org/10.1890/1540-9295(2003)001[0031:PSATEO]2.0.CO;2

    Article  Google Scholar 

  • Scholz NL, Truelove NK, French BL, Berejikian BA, Quinn TP, Casillas E, Collier TK (2000) Diazinon disrupts antipredator and homing behaviors in chinook salmon (Oncorhynchus tshawytscha). Canadian Journal of Fisheries and Aquatic Sciences 57:1911–1918

  • SEPA (Scottish Environmental Protection Agency) (1998) SEPA policy on the use of cypermethrin in marine fish farming risk assessment, EQS and recommendations. Policy No. 30

  • Sievers G, Palacios P, Inostroza R, Dölz H (1995) Evaluation of the toxicity of 8 insecticides in Salmo salar and the in vitro effects against the isopode parasite, Ceratothoa gaudichaudii. Aquaculture 134(1–2):9–16

  • Skilbrei O, Espedal P, Nilsen F, Garcia E, Glover K (2015) Evaluation of emamectin benzoate and substance EX against salmon lice in sea-ranched Atlantic salmon smolts. Diseases of Aquatic Organisms 113(3):187–194. https://doi.org/10.3354/dao02832

    Article  CAS  Google Scholar 

  • Stephenson RR (1982) Aquatic toxicology of cypermethrin. I. Acute toxicity to some freshwater fish and invertebrates in laboratory tests. Aquatic Toxicology 2(3):175–185. https://doi.org/10.1016/0166-445X(82)90014-5

    Article  CAS  Google Scholar 

  • Stone J, Sutherland IH, Sommerville CS, Richards RH, Varma KJ (1999) The efficacy of emamectin benzoate as an oral treatment of sea lice, Lepeophtheirus salmonis (Kroyer), infestations in Atlantic salmon, Salmo salar L. Journal of Fish Diseases 22(4):261–270. https://doi.org/10.1046/j.1365-2761.1999.00176.x

    Article  CAS  Google Scholar 

  • Stone J, Roy WJ, Sutherland IH, Ferguson HW, Sommerville C, Endris R (2002) Safety and efficacy of emamectin benzoate administered in-feed to Atlantic salmon, Salmo salar L., smolts in freshwater, as a preventative treatment against infestations of sea lice, Lepeophtheirus salmonis (Krøyer). Aquaculture 210(1–4):21–34. https://doi.org/10.1016/S0044-8486(01)00822-5

    Article  CAS  Google Scholar 

  • Strachan F, Kennedy CJ (2021) The environmental fate and effects of anti-sea lice chemotherapeutants used in salmon aquaculture. Aquaculture. 544:737079

  • Svobodová Z, Lusková V, Drastichová J, Svoboda M, Îlábek V (2003) Effect of Deltamethrin on Haematological Indices of Common Carp (Cyprinus carpio L.). Acta Veterinaria Brno 72:79–85

    Article  Google Scholar 

  • Tarkhani R, Imanpoor MR (2012) Mortality response of Xiphophorus maculatus (Cyprinodontiformes Poeciliidae) to some agricultural pesticides Isolation and Identification of potentially probiotic bacteria from adult Caspian roach intestine and possible effects on roach fry View project Mortality Response of Xiphophorus maculatus (Cyprinodontiformes: Poeciliidae) to Some Agricultural. Pesticides. World Journal of Fish and Marine Sciences 4(5):512–516. https://doi.org/10.5829/idosi.wjfms.2012.04.05.64100

    Article  Google Scholar 

  • Taylor LN, Mcgeer JC, Wood CM, Gordon Mcdonald D (2000) Physiological effects of chronic copper exposure to rainbow trout (Oncorhynchus Mykiss) in hard and soft water: evaluation of chronic indicators. In Environmental Toxicology and Chemistry 19(9), 2298-2308

  • Thomas CR, Hose GC, Warne MSJ, Lim RP (2008) Effects of river water and salinity on the toxicity of deltamethrin to freshwater shrimp, cladoceran, and fish. Archives of Environmental Contamination and Toxicology 55(4):610–618. https://doi.org/10.1007/s00244-008-9147-0

    Article  CAS  Google Scholar 

  • Thomaz JM, Martins ND, Monteiro DA, Rantin FT, Kalinin AL (2009) Cardio-respiratory function and oxidative stress biomarkers in Nile tilapia exposed to the organophosphate insecticide trichlorfon (NEGUVON®). Ecotoxicology and Environmental Safety 72(5):1413–1424. https://doi.org/10.1016/j.ecoenv.2008.11.003

    Article  CAS  Google Scholar 

  • Tierney K, Casselman M, Takeda S, Farrell T, Kennedy, C (2007) The relationship between cholinesterase inhibition and two types of swimming performance in chlorpyrifos-exposed coho salmon (Oncorhynchus Kisutch). Environmental Toxicology and Chemistry (26, 5). http://www.cerc.usgs.gov/pubs/center/pdfDocs/

  • Tierney KB, Sekela MA, Cobbler CE, Xhabija B, Gledhill M, Ananvoranich S, Zielinski BS (2011) Evidence for behavioral preference toward environmental concentrations of urban-use herbicides in a model adult fish. Environmental Toxicology and Chemistry 30(9):2046–2054. https://doi.org/10.1002/etc.588

    Article  CAS  Google Scholar 

  • Tierney KB (2016) Chemical avoidance responses of fishes. In Aquatic Toxicology 174:228–241. https://doi.org/10.1016/j.aquatox.2016.02.021. Elsevier B.V

    Article  CAS  Google Scholar 

  • Tierney KB, Baldwin DH, Hara TJ, Ross PS, Scholz NL, Kennedy CJ (2010) Olfactory toxicity in fishes. In Aquatic Toxicology 96(1):2–26. https://doi.org/10.1016/j.aquatox.2009.09.019. Elsevier

    Article  CAS  Google Scholar 

  • Tomlin C (Ed.) (1994) The pesticide manual: A world compendium.10th ed. Incorporating the Agrochemicals handbook. British Crop Protection Council and Royal Society of Chemistry, Thornton Heath, UK

    Google Scholar 

  • Tomlin CDS ed. (1997) The pesticide manual - A world compendium. British Crop Protection Council, Surrey

    Google Scholar 

  • Tryfonos M, Papaefthimiou C, Antonopoulou E, Theophilidis G (2009) Comparing the inhibitory effects of five protoxicant organophosphates (azinphos-methyl, parathion-methyl, chlorpyriphos-methyl, methamidophos and diazinon) on the spontaneously beating auricle of Sparus aurata: An in vitro study. Aquatic Toxicology 94(3):211–218. https://doi.org/10.1016/j.aquatox.2009.07.003

    Article  CAS  Google Scholar 

  • US EPA (2002) Methods for Measuring the Acute Toxicity of Effluents and Receiving Waters to Freshwater and Marine Organisms, Firth Edition. Office of Water. EPA-821-R-02-012, Washington, DC

    Google Scholar 

  • US EPA (2021) Technical overview of Ecological Risk Assessment: Risk characterization. Accessed 25 April 2021. Available at: https://www.epa.gov/pesticide-science-and-assessing-pesticide-risks/technical-overview-ecological-risk-assessment-risk#main-content

  • Ural MŞ, Saǧlam N (2005) A study on the acute toxicity of pyrethroid deltamethrin on the fry rainbow trout (Oncorhynchus mykiss Walbaum, 1792). Pesticide Biochemistry and Physiology 83(2–3):124–131. https://doi.org/10.1016/j.pestbp.2005.04.004

    Article  CAS  Google Scholar 

  • Van Geest JL, Burridge LE, Fife FJ, Kidd KA (2014) Feeding response in marine copepods as a measure of acute toxicity of four anti-sea lice pesticides. Marine Environmental Research 101(1):145–152. https://doi.org/10.1016/j.marenvres.2014.09.011

    Article  CAS  Google Scholar 

  • Velíšek J, Jurčíková J, Dobšíková R, Svobodová Z, Piačková V, Máchová J, Novotný L (2007) Effects of deltamethrin on rainbow trout (Oncorhynchus mykiss). Environmental Toxicology and Pharmacology 23(3):297–301. https://doi.org/10.1016/j.etap.2006.11.006

    Article  CAS  Google Scholar 

  • Vera LM, Migaud H (2016) Hydrogen peroxide treatment in Atlantic salmon induces stress and detoxification response in a daily manner. Chronobiology International 33(5):530–542. https://doi.org/10.3109/07420528.2015.1131164

    Article  CAS  Google Scholar 

  • Vijverberg HPM, Van Den Bercken J (1979) Frequency-dependent effects of the pyrethroid insecticide decamethrin in frog myelinated nerve fibres. European Journal of Pharmacology 58(4):501–504. https://doi.org/10.1016/0014-2999(79)90325-X

    Article  CAS  Google Scholar 

  • Vijverberg HPM, Ruigt GF, van den Bercken J (1982) Structure-related effects of pyrethroid insecticides on the lateral-line sense organ and on peripheral nerves of the clawed frog, Xenopus laevis. Pesticide Biochemistry and Physiology 18(3):315–324. https://doi.org/10.1016/0048-3575(82)90072-4

    Article  CAS  Google Scholar 

  • Viran R, Erkoç FÜ, Polat H, Koçak O (2003) Investigation of acute toxicity of deltamethrin on guppies (Poecilia reticulata). Ecotoxicology and Environmental Safety 55(1):82–85. https://doi.org/10.1016/S0147-6513(02)00096-9

    Article  CAS  Google Scholar 

  • Waiwood KG, Beamish FWH (1978) Effects of copper, pH and hardness on the critical swimming performance of rainbow trout (Salmo gairdneri Richardson). Water Research 12(8):611–619. https://doi.org/10.1016/0043-1354(78)90141-0

    Article  CAS  Google Scholar 

  • Webb PW (1971) The swimming energetics of trout ii. oxygen consumption and swimming efficiency. Experimentalis Biology (55):521–540

  • Werner I, Moran K (2008) Effects of pyrethroid insecticides on aquatic organisms. ACS Symposium Series 991:310–334. https://doi.org/10.1021/bk-2008-0991.ch014

    Article  CAS  Google Scholar 

  • Wood AW, Johnston BD, Farrell AP, Kennedy CJ (1996) Effects of didecyldimethylammonium chloride (DDAC) on the swimming performance, gill morphology, disease resistance, and biochemistry of rainbow trout (Oncorhynchus mykiss). Canadian Journal of Fisheries and Aquatic Sciences (53):2424–2432

  • Woof L, Kennedy CJ (submitted). The lethal and sublethal effects of anti-sea lice chemotherapeutants in marine benthic invertebrates. Archives of Environmental Contamination and Toxicology

  • Woof L (2021) The lethal and sublethal effects of anti-sea lice chemotherapeutants in marine benthic and pelagic invertebrates [Master’s thesis]. Simon Fraser University

  • Xie X, Gong S, Wang X, Wu Y, Zhao L (2011) Simplified RP-HPLC method for multi-residue analysis of abamectin, emamectin benzoate and ivermectin in rice. Food Additives and Contaminants 28(1):19–25. https://doi.org/10.1080/19440049.2010.527377

    Article  CAS  Google Scholar 

  • Xuereb B, Lefèvre E, Garric J, Geffard O (2009) Acetylcholinesterase activity in Gammarus fossarum (Crustacea Amphipoda): Linking AChE inhibition and behavioural alteration. Aquatic Toxicology 94(2):114–122. https://doi.org/10.1016/j.aquatox.2009.06.010

    Article  CAS  Google Scholar 

  • Zitko V, Mcleese DW, Metcalfe CD, Carson WG (1979) Toxicity of Permethrin, Decamethrin, and Related Pyrethroids to Salmon and Lobster. Bulletin Environmental Contamination Toxicology (21):338–343

Download references

Acknowledgements

We thank Bruce Leighton (Simon Fraser University) for experimental support with animal husbandry and the staff at the Tenderfoot Creek hatchery.

Author contributions:

C.S., K.H. and B.S. conducted research; C.S., K.H. and B.S. review and editing; C.J.K. provided funding acquisition, project design and administration, and resources; C.J.K. wrote the paper.

Funding

This work was supported by grants from the National Contaminants Advisory Group at Fisheries and Oceans Canada to CJK.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Christopher J. Kennedy.

Ethics declarations

Conflict of interest

The authors declare no competing interests.

Ethical approval

This project was approved by the Simon Fraser University University Animal Care Committee according to the guidelines outlined by the Canadian Council on Animal Care

Consent to participate

All authors consent to participate.

Consent for publication

All authors consent to publication.

Additional information

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Sahota, C., Hayek, K., Surbey, B. et al. Lethal and sublethal effects in Pink salmon (Oncorhynchus gorbuscha) following exposure to five aquaculture chemotherapeutants. Ecotoxicology 31, 33–52 (2022). https://doi.org/10.1007/s10646-021-02473-8

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10646-021-02473-8

Keywords

Navigation