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Water, Air, & Soil Pollution

, 230:231 | Cite as

Increased Mortality, Delayed Hatching, Development Aberrations and Reduced Activity in Brown Trout (Salmo trutta) Exposed to Phenethyl Isothiocyanate

  • Asa B. WhiteEmail author
  • Angelo P. Pernetta
  • Chris B. Joyce
  • Neil Crooks
Article

Abstract

Plants of the order Brassicaceae have evolved a chemical defence against herbivory: the glucosinolate-myrosinase system. Mechanical damage to plant tissues, such as grazing, initiates the production of phenethyl isothiocyanate (PEITC), a compound toxic to invertebrates. Mechanical damage caused during biofumigation and the harvesting and washing of watercress presents routes for PEITC release into waterbodies, such as the chalk stream spawning sites of brown trout (Salmo trutta). This laboratory study exposed developing S. trutta embryos to PEITC at concentrations of 0.01, 0.1 and 1 μg/L. S. trutta exposed to 1 μg/L PEITC during embryonic development resulted in 100% mortality after four dose days. Exposure to 0.1 μg/L PEITC resulted in an approximate fourfold increase in mortality relative to the controls, while exposure to 0.01 μg/L PEITC had a negligible effect on embryo mortality. Embryos exposed to 0.1 μg/L PEITC showed a significant delay in hatching and produced alevins with significantly shorter total lengths, lighter body weights and an approximate threefold increase in spinal deformities relative to those exposed to the controls and 0.01 μg/L PEITC. The results of a motor activity assay demonstrate that alevins exposed to PEITC showed a significant decrease in swimming activity compared with control animals during periods of illumination. The increased mortality, teratogenic effects and impaired behaviour in S. trutta following embryonic exposure to relatively low concentrations of PEITC highlight a need to accurately quantify and monitor environmental levels of PEITC.

Keywords

PEITC Watercress Biofumigation Chalk stream 

Notes

Acknowledgements

We would like to thank Allenbrook Trout Farm, Dorset and The Berkshire Trout Farm, Berkshire, for the supply of Salmo trutta gametes that were used in this study.

Funding Information

This study was financially supported by The Vitacress Conservation Trust and a University of Brighton PhD Studentship.

Compliance with Ethical Standards

Conflict of Interest

The authors have no conflicts of interest to declare.

References

  1. Abbaoui, B., Lucas, C. R., Riedl, K. M., Clinton, S. K., & Mortazavi, A. (2018). Cruciferous vegetables, isothiocyanates, and bladder cancer prevention. Molecular Nutrition & Food Research, 62(18), 1800079.  https://doi.org/10.1002/mnfr.201800079.CrossRefGoogle Scholar
  2. Antunes, M., & Lopes Da Cunha, P. (2002). Skeletal anomalies in Gobius niger (Gobiidae) from Sado estuary, Portugal. Cybium, 26(3), 179–184 http://www.scopus.com/inward/record.url?eid=2-s2.0-0037201828&partnerID=tZOtx3y1. Accessed 5 May 2017.
  3. Bagenal, T. B. (1969). Relationship between egg size and fry survival in brown trout Salmo trutta L. Journal of Fish Biology, 1(4), 349–353.  https://doi.org/10.1111/j.1095-8649.1969.tb03882.x.CrossRefGoogle Scholar
  4. Bams, R. (1969). Adaptations of sockeye salmon associated with incubation in stream gravels. In T. G. Northcote (Ed.), (symposium., pp. 71–87). The University of British Columbia, Vancouver: Institute of Fisheries.Google Scholar
  5. Boglione, C., Gagliardi, F., Scardi, M., & Cataudella, S. (2001). Skeletal descriptors and quality assessment in larvae and post-larvae of wild-caught and hatchery-reared gilthead sea bream (Sparus aurata L. 1758). Aquaculture, 192(1), 1–22.  https://doi.org/10.1016/S0044-8486(00)00446-4.CrossRefGoogle Scholar
  6. Bossus, M. C., Guler, Y. Z., Short, S. J., Morrison, E. R., & Ford, A. T. (2014). Behavioural and transcriptional changes in the amphipod Echinogammarus marinus exposed to two antidepressants, fluoxetine and sertraline. Aquatic Toxicology, 151, 46–56.  https://doi.org/10.1016/j.aquatox.2013.11.025.CrossRefGoogle Scholar
  7. Brown, D. R., Bailey, J. M., Oliveri, A. N., Levin, E. D., & Di Giulio, R. T. (2016). Developmental exposure to a complex PAH mixture causes persistent behavioral effects in naive Fundulus heteroclitus (killifish) but not in a population of PAH-adapted killifish. Neurotoxicology and Teratology, 53, 55–63.  https://doi.org/10.1016/j.ntt.2015.10.007.CrossRefGoogle Scholar
  8. Carey, W. E., & Noakes, D. L. G. (1981). Development of photobehavioural responses in young rainbow trout, Salmo gairdneri Richardson. Journal of Fish Biology, 19(3), 285–296.  https://doi.org/10.1111/j.1095-8649.1981.tb05832.x.CrossRefGoogle Scholar
  9. Cargnelli, L. M., & Gross, M. R. (1996). The temporal dimension in fish recruitment: birth date, body size, and size-dependent survival in a sunfish (bluegill: Lepomis macrochirus). Canadian Journal of Fisheries and Aquatic Sciences, 53(2), 360–367.  https://doi.org/10.1139/cjfas-53-2-360.CrossRefGoogle Scholar
  10. Chapman, D. W. (1962). Aggressive behavior in juvenile coho salmon as a cause of emigration. Journal of the Fisheries Research Board of Canada, 19(6), 1047–1080.  https://doi.org/10.1139/f62-069.CrossRefGoogle Scholar
  11. Chen, C.-W., & Ho, C.-T. (1998). Thermal degradation of allyl isothiocyanate in aqueous solution. Journal of Agricultural and Food Chemistry, 46(1), 220–223 EP.  https://doi.org/10.1021/jf990082e Accessed 5 Dec 2016.CrossRefGoogle Scholar
  12. Chen, T.-H., Wang, Y.-H., & Wu, Y.-H. (2011). Developmental exposures to ethanol or dimethylsulfoxide at low concentrations alter locomotor activity in larval zebrafish: implications for behavioral toxicity bioassays. Aquatic Toxicology, 102(3–4), 162–166.CrossRefGoogle Scholar
  13. Coe, T. S., Söffker, M. K., Filby, A. L., Hodgson, D., & Tyler, C. R. (2010). Impacts of early life exposure to estrogen on subsequent breeding behavior and reproductive success in Zebrafish. Environmental Science and Technology, 44(16), 6481–6487.  https://doi.org/10.1021/es101185b.CrossRefGoogle Scholar
  14. Cox, J. (2009). Watercress growing and its environmental impacts on chalk rivers in England (NECR 027). www.naturalengland.org.uk (pp. 1–52).
  15. Crisp, D. T. (1993). The environmental requirements of salmon and trout in fresh water. Freshwater Forum, 3(3), 176–202 http://aquaticcommons.org/4542/. .Google Scholar
  16. Dahlberg, M. D. (1970). Frequencies of abnormalities in Georgia estuarine fishes. Transactions of the American Fisheries Society, 99(1), 95–97.  https://doi.org/10.1577/1548-8659(1970)99<95:FOAIGE>2.0.CO;2.CrossRefGoogle Scholar
  17. Dinkova-Kostova, A. T., & Kostov, R. V. (2012). Glucosinolates and isothiocyanates in health and disease. Trends in Molecular Medicine.  https://doi.org/10.1016/j.molmed.2012.04.003.
  18. Dixon, M. J. (2010). The sustainable use of water to mitigate the impact of watercress farms on chalk streams in southern England. University of Southampton. Retrieved from https://eprints.soton.ac.uk/195397/. Accessed 16 Feb 2018.
  19. Dixon, M. J., & Shaw, P. J. (2011). Watercress and water quality: the effect of phenethyl isothiocyanate on the mating behaviour of Gammarus pulex. International Journal of Zoology.  https://doi.org/10.1155/2011/328749.
  20. Doheny-Adams, T., Lilley, C. J., Barker, A., Ellis, S., Wade, R., Atkinson, H. J., et al. (2018). Constant isothiocyanate-release potentials across biofumigant seeding rates. Journal of Agricultural and Food Chemistry, 66(20), 5108–5116.  https://doi.org/10.1021/acs.jafc.7b04610.CrossRefGoogle Scholar
  21. Dunham, R. A., Smitherman, R. O., & Bondari, K. (1991). Lack of inheritance of stumpbody and taillessness in channel catfish. The Progressive Fish-Culturist, 53(2), 101–105.  https://doi.org/10.1577/1548-8640(1991)053<0101:LOIOSA>2.3.CO;2.CrossRefGoogle Scholar
  22. Einum, S., Fleming, I. A., Einum, S., & Fleming, I. A. N. A. (2014). Selection against late emergence and small offspring in Atlantic salmon (Salmo salar). Evolution, 54(2), 628–639.CrossRefGoogle Scholar
  23. Elliott, J. M. (1986). Spatial distribution and behavioural movements of migratory trout Salmo trutta in a lake district stream. Journal of Animal Ecology, 55(3), 907–922.  https://doi.org/10.2307/4424.CrossRefGoogle Scholar
  24. Elliott, J. M. (1989). Wild brown trout Salmo trutta: an important national and international resource. Freshwater Biology, 21(1), 1–5.  https://doi.org/10.1111/j.1365-2427.1989.tb01343.x.CrossRefGoogle Scholar
  25. Elliott, J. M., & Hurley, M. A. (1998). Predicting fluctuations in the size of newly emerged sea-trout fry in a Lake District stream. Journal of Fish Biology, 53(5), 1120–1133.  https://doi.org/10.1111/j.1095-8649.1998.tb00468.x.CrossRefGoogle Scholar
  26. Fast, D. E., & Stober, Q. J. J. (1984). Intragravel behavior of salmonid alevins in response to environmental changes. Fisheries Research Institute. https://digital.lib.washington.edu/researchworks/bitstream/handle/1773/4040/8414.pdf?sequence=1. .
  27. Fenwick, G. R., Heaney, R. K., Mullin, W. J., & VanEtten, C. H. (1983). Glucosinolates and their breakdown products in food and food plants. C R C Critical Reviews in Food Science and Nutrition, 18(2), 123–201.  https://doi.org/10.1080/10408398209527361.CrossRefGoogle Scholar
  28. Finn, R. N. (2007). The physiology and toxicology of salmonid eggs and larvae in relation to water quality criteria in relation to water quality criteria. Aquatic Toxicology, 81(81), 337–354.  https://doi.org/10.1016/j.aquatox.2006.12.021.CrossRefGoogle Scholar
  29. Gimsing, A. L., & Kirkegaard, J. A. (2009). Glucosinolates and biofumigation: Fate of glucosinolates and their hydrolysis products in soil. Phytochemistry Reviews.  https://doi.org/10.1007/s11101-008-9105-5.
  30. Green, J., & Wheeler, J. R. (2013). The use of carrier solvents in regulatory aquatic toxicology testing: practical, statistical and regulatory considerations. Aquatic Toxicology, 144–145, 242–249.  https://doi.org/10.1016/J.AQUATOX.2013.10.004.CrossRefGoogle Scholar
  31. Halkier, B. A., & Gershenzon, J. (2006). Biology and biochemistry of glucosinolates. Annual Reiew. Plant Biology, 57, 303–333.  https://doi.org/10.1146/annurev.arplant.57.032905.105228.CrossRefGoogle Scholar
  32. Hallare, A., Nagel, K., Köhler, H. R., & Triebskorn, R. (2006). Comparative embryotoxicity and proteotoxicity of three carrier solvents to zebrafish (Danio rerio) embryos. Ecotoxicology and Environmental Safety, 63(3), 378–388.  https://doi.org/10.1016/j.ecoenv.2005.07.006.CrossRefGoogle Scholar
  33. Hamilton, P. B., Cowx, I. G., Oleksiak, M. F., Griffiths, A. M., Grahn, M., Stevens, J. R., et al. (2016). Population-level consequences for wild fish exposed to sublethal concentrations of chemicals—a critical review. Fish and Fisheries.  https://doi.org/10.1111/faf.12125.
  34. Houde, E. (1987). Fish early life dynamics and recruitment variability. In American Fisheries Society Symposium (p. 2: 17-29).Google Scholar
  35. Hua, J., Vijver, M. G., Richardson, M. K., Ahmad, F., & Peijnenburg, W. J. G. M. (2014). Particle-specific toxic effects of differently shaped zinc oxide nanoparticles to zebrafish embryos (Danio rerio). Environmental Toxicology and Chemistry, 33(12), 2859–2868.  https://doi.org/10.1002/etc.2758.CrossRefGoogle Scholar
  36. Hunt, R. L. (1969). Overwinter survival of wild fingerling brook trout in Lawrence Creek, Wisconsin. Journal of the Fisheries Research Board of Canada, 26(6), 1473–1483.  https://doi.org/10.1139/f69-138.CrossRefGoogle Scholar
  37. Hutchinson, T. H., Shillabeer, N., Winter, M. J., & Pickford, D. B. (2006). Acute and chronic effects of carrier solvents in aquatic organisms: a critical review. Aquatic Toxicology.  https://doi.org/10.1016/j.aquatox.2005.09.008.
  38. Jezierska, B., Ługowska, K., & Witeska, M. (2009). The effects of heavy metals on embryonic development of fish (a review). Fish Physiology and Biochemistry, 35(4), 625–640 http://www.ncbi.nlm.nih.gov/pubmed/19020985.. Accessed 20 Jan 2017.
  39. Ji, Y., Kuo, Y., & Morris, M. E. E. (2005). Pharmacokinetics of dietary phenethyl isothiocyanate in rats. Pharmaceutical Research, 22(10), 1658–1666.  https://doi.org/10.1007/s11095-005-7097-z.CrossRefGoogle Scholar
  40. Kerfoot, W. C., Newman, R. M., & Hanscom, Z. (1998). Snail reaction to watercress leaf tissues: reinterpretation of a mutualistic “alarm” hypothesis. Freshwater Biology, 40(2), 201–213.  https://doi.org/10.1046/j.1365-2427.1998.00334.x.CrossRefGoogle Scholar
  41. Klemetsen, A., Amundsen, P.-A., Dempson, J. B., Jonsson, B., Jonsson, N., O’Connell, M. F., & Mortensen, E. (2003). Atlantic salmon Salmo salar L., brown trout Salmo trutta L. and Arctic charr Salvelinus alpinus (L.): a review of aspects of their life histories. Ecology of Freshwater Fish, 12(1), 1–59.  https://doi.org/10.1034/j.1600-0633.2003.00010.x.CrossRefGoogle Scholar
  42. Kristensen, P. (1994). Sensitivity of embryos and larvae in relation to other stages in the life cycle of fish: a literature review. In Sublethal and chronic effects of pollutants on freshwater fish (pp. 155–166). Oxford: Fishing News Books.Google Scholar
  43. Kroger, R. L., & Guthrie, J. F. (1971). Incidence of crooked vertebral columns in juvenile Atlantic menhaden, Brevoortia tyrannus. Chesapeake Science, 12(4), 276–278.  https://doi.org/10.2307/1350917.CrossRefGoogle Scholar
  44. Kvellestad, A., Høie, S., Thorud, K., Tørud B, Lyngøy A.. (2000). Platyspondyly and shortness of vertebral column in farmed Atlantic salmon Salmo salar in Norway—description and interpretation of pathologic changes. int-res.com, 39, 97–108. https://www.int-res.com/abstracts/dao/v39/n2/p97-108/. Accessed 1 November 2018.
  45. Laegdsmand, M., Gimsing, A. L., Strobel, B. W., Sørensen, J. C., Jacobsen, O. H., & Hansen, H. C. B. (2007). Leaching of isothiocyanates through intact soil following simulated biofumigation. Plant and Soil, 291(1–2), 81–92.  https://doi.org/10.1007/s11104-006-9176-2.CrossRefGoogle Scholar
  46. Maes, J., Verlooy, L., Buenafe, O. E., de Witte, P. A. M., Esguerra, C. V., & Crawford, A. D. (2012). Evaluation of 14 organic solvents and carriers for screening applications in zebrafish embryos and larvae. PLoS One, 7(10).  https://doi.org/10.1371/journal.pone.0043850.
  47. Mainstone, C. P. (1999). Chalk rivers: nature conservation and management. Water Reseach Centre.  https://doi.org/10.1017/CBO9781107415324.004.
  48. Malbrouck, C., & Kestemont, P. (2006). Effects of microcystins on fish. Environmental Toxicology and Chemistry, 25(1), 72–86.  https://doi.org/10.1897/05-029R.1.CrossRefGoogle Scholar
  49. Mann, R., Blackburn, J., & Beaumont, W. (1989). The ecology of brown trout Salmo trutta in English chalk streams. Freshwater Biology, 21(1), 57–70.CrossRefGoogle Scholar
  50. Matthiessen, J. N., & Kirkegaard, J. A. (2006). Biofumigation and enhaces biodegradation: opportunity and challenge in soilborne pest and disease managemente. Plant Science, 25(3), 235–265. http://www.tandfonline.com/doi/abs/10.1080/07352680600611543. Accessed 5 December 2016.
  51. Messaoudi, I., Deli, T., Kessabi, K., Barhoumi, S., Kerkeni, A., & Saïd, K. (2009). Association of spinal deformities with heavy metal bioaccumulation in natural populations of grass goby, Zosterisessor ophiocephalus Pallas, 1811 from the Gulf of Gabès (Tunisia). Environmental Monitoring and Assessment, 156(1–4).  https://doi.org/10.1007/s10661-008-0504-2.
  52. Newman, R. M., Kerfoot, W. C., & Hanscom, Z. (1990). Watercress and amphipods potential chemical defense in a spring stream macrophyte. Journal of Chemical Ecology, 16(1), 245–259.  https://doi.org/10.1007/BF01021282.CrossRefGoogle Scholar
  53. Newman, R. M., Kerfoot, W. C., & Hanscom, Z. (1996). Watercress allelochemical defends high-nitrogen foliage against consumption: effects on freshwater invertebrate herbivores. Ecology, 77(8), 2312–2323.  https://doi.org/10.2307/2265733.CrossRefGoogle Scholar
  54. Ntalli, N., Caboni, P., & Ntalli Pierluigi Caboni, N. (2017). A review of isothiocyanates biofumigation activity on plant parasitic nematodes. Phytochemistry Reviews, 1–8.  https://doi.org/10.1007/s11101-017-9491-7.
  55. OECD. (1992). OECD Guidline for testing chemicals Zahn-Wellens/EMPA1 Test 302B. www.oecd.org
  56. Ojanguren, A. F., & Braña, F. (2003). Thermal dependence of embryonic growth and development in brown trout. Journal of Fish Biology, 62(3), 580–590.CrossRefGoogle Scholar
  57. Pan, J. H., Abernathy, B., Kim, Y. J., Lee, J. H., Kim, J. H., Shin, E. C., & Kim, J. K. (2018). Cruciferous vegetables and colorectal cancer prevention through microRNA regulation: a review. Critical Reviews in Food Science and Nutrition, 58(12), 2026–2038.  https://doi.org/10.1080/10408398.2017.1300134.CrossRefGoogle Scholar
  58. Petersen, J., Belz, R., Walker, F., & Hurle, K. (2001). Weed suppression by release of isothiocyanates from turnip-rape mulch. In Agronomy Journal, 93, 37–43.  https://doi.org/10.2134/agronj2001.93137x.CrossRefGoogle Scholar
  59. Powell, M. D., Jones, M. A., & Lijalad, M. (2009). Effects of skeletal deformities on swimming performance and recovery from exhaustive exercise in triploid Atlantic salmon. Diseases of Aquatic Organisms, 85(1), 59–66.  https://doi.org/10.3354/dao02056.CrossRefGoogle Scholar
  60. Power, M. (1994). Quantitative ecology and the brown trout. Transactions of the American Fisheries Society, 123(6), 1006–1008.  https://doi.org/10.1577/1548-8659-123.6.1006.CrossRefGoogle Scholar
  61. Réalis-Doyelle, E., Pasquet, A., De Charleroy, D., Fontaine, P., & Teletchea, F. (2016). Strong effects of temperature on the early life stages of a cold stenothermal fish species, brown trout (Salmo trutta L.). PLoS ONE, 11(5), e0155487.  https://doi.org/10.1371/journal.pone.0155487.CrossRefGoogle Scholar
  62. Rhodes, J. S., & Quinn, T. P. (1998). Factors affecting the outcome of territorial contests between hatchery and naturally reared coho salmon parr in the laboratory. Journal of Fish Biology, 53(6), 1220–1230.  https://doi.org/10.1006/jfbi.1998.0787.CrossRefGoogle Scholar
  63. Rice, J. A., Miller, T. J., Rose, K. A., Crowder, L. B., Marschall, E. A., Trebitz, A. S., & DeAngelis, D. L. (1993). Growth rate variation and larval survival: inferences from an individual-based size-dependent predation model. Canadian Journal of Fisheries and Aquatic Sciences, 50(1), 133–142.  https://doi.org/10.1139/f93-015.CrossRefGoogle Scholar
  64. Roddie, B., Kedwards, T., & Crane, M. (1992). Potential impact of watercress farm discharges on the freshwater amphipod, Gammarus pulex L. Bulletin of Environmental Contamination and Toxicology, 48(1), 63–69.  https://doi.org/10.1007/BF00197484.CrossRefGoogle Scholar
  65. Rodrigues, L., Silva, I., Poejo, J., Serra, A. T., Matias, A. A., Simplício, A. L., et al. (2016). Recovery of antioxidant and antiproliferative compounds from watercress using pressurized fluid extraction. RSC Advances, 6(37), 30905–30918.  https://doi.org/10.1039/C5RA28068K.CrossRefGoogle Scholar
  66. Rumberger, A., & Marschner, P. (2003). 2-Phenylethyl isothiocyanate concentration and microbial community composition in the rhizosphere of canola. Soil Biology and Biochemistry, 35(3), 445–452. http://www.sciencedirect.com/science/article/pii/S0038071702002961. Accessed 5 December 2016.
  67. Schubert, S., Peter, A., Schönenberger, R., Suter, M. J. F., Segner, H., & Burkhardt-Holm, P. (2014). Transient exposure to environmental estrogen affects embryonic development of brown trout (Salmo trutta fario). Aquatic Toxicology, 157, 141–149.  https://doi.org/10.1016/j.aquatox.2014.10.007.CrossRefGoogle Scholar
  68. Schultz, E. T., Conover, D. O., & Ehtisham, A. (1998). The dead of winter: size-dependent variation and genetic differences in seasonal mortality among Atlantic silverside (Atherinidae: Menidia menidia) from different latitudes. Canadian Journal of Fisheries and Aquatic Sciences, 55(5), 1149–1157.  https://doi.org/10.1139/cjfas-55-5-1149.CrossRefGoogle Scholar
  69. Sfakianakis, D. G., Renieri, E., Kentouri, M., & Tsatsakis, A. M. (2015). Effect of heavy metals on fish larvae deformities: a review. Environmental Research.  https://doi.org/10.1016/j.envres.2014.12.014.
  70. Shelton, A. L. (2005). Within-plant variation in glucosinolate concentrations of Raphanus sativus across multiple scales. Journal of Chemical Ecology, 31(8), 1711–1732.  https://doi.org/10.1007/s10886-005-5922-9.CrossRefGoogle Scholar
  71. Skoglund, H., & Barlaup, B. T. (2006). Feeding pattern and diet of first feeding brown trout fry under natural conditions. Journal of Fish Biology, 68(2), 507–521.  https://doi.org/10.1111/j.0022-1112.2006.00938.x.CrossRefGoogle Scholar
  72. Sloman, K. A., & Mcneil, P. L. (2012). Using physiology and behaviour to understand the responses of fish early life stages to toxicants. Journal of Fish Biology.  https://doi.org/10.1111/j.1095-8649.2012.03435.x.
  73. Smith, B. J., & Kirkegaard, J. A. (2002). In vitro inhibition of soil microorganisms by 2-phenylethyl isothiocyanate. Plant Pathology, 51(5), 585–593.  https://doi.org/10.1046/j.1365-3059.2002.00744.x.CrossRefGoogle Scholar
  74. Strähle, U., Geisler, R., Greiner, P., Hollert, H., Rastegar, S., Schumacher, A., et al. (2012). Zebrafish embryos as an alternative to animal experiments—a commentary on the definition of the onset of protected life stages in animal welfare regulations. Reproductive Toxicology, 33(2), 128–132.  https://doi.org/10.1016/J.REPROTOX.2011.06.121.CrossRefGoogle Scholar
  75. Tave, D., Bartels, J. E., & Smitherman, R. O. (1982). Stumpbody Sarotherodon aureus (Steindachner)(= Tilapia aurea) and tail-less S. niloticus (L.)(= T. niloticd): two vertebral anomalies and their effects on body length. Journal of Fish Diseases, 5(6), 487–494.CrossRefGoogle Scholar
  76. Taylor, E. B., & McPhail, J. D. (1985). Burst swimming and size-related predation of newly emerged coho salmon Oncorhynchus kisutch. Transactions of the American Fisheries Society, 8487(114), 546–551.  https://doi.org/10.1577/1548-8659(1985)114.CrossRefGoogle Scholar
  77. Traka, M., & Mithen, R. (2009). Glucosinolates, isothiocyanates and human health. Phytochemistry Reviews.  https://doi.org/10.1007/s11101-008-9103-7.
  78. Von Westernhagen, H. (1988). Sublethal effects of pollutants on fish eggs and larvae. Fish physiology (Vol. 11). Elsevier BV. doi: https://doi.org/10.1016/s1546-5098(08)60201-0.
  79. Wankowski, J. W. J. (1979). Spatial distribution and feeding in Atlantic salmon, L. juveniles. Journal of Fish Biology, 30(3), 787–247.  https://doi.org/10.1111/j.1095-8649.1979.tb03515.x.CrossRefGoogle Scholar
  80. Weis, P., & Weis, J. S. (1976). Abnormal locomotion associated with skeletal malformations in the sheepshead minnow, Cyprinodon variegatus, exposed to malathion. Environmental Research, 12(2), 196–200.  https://doi.org/10.1016/0013-9351(76)90024-4.CrossRefGoogle Scholar
  81. Woltering, D. M. (1984). The growth response in fish chronic and early life stage toxicity tests: a critical review. Aquatic Toxicology, 5(1), 1–21.  https://doi.org/10.1016/0166-445X(84)90028-6.CrossRefGoogle Scholar
  82. Woodhead, P. M. J. (1957). Reaction of salmonid larvae to light. Journal of Experimental Biology, 34(1954), 402–416.Google Scholar
  83. Worgan, A. D., & Tyrell, R. (2005). Monitoring behavioural responses of Gammarus pulex to watercress oils. Centre for Ecology and Hydrology, CO2786NEW.Google Scholar
  84. Wu, R. S., Zhou, B. S., Randall, D. J., Woo, N. Y., & Lam, P. K. (2003). Aquatic hypoxia is an endocrine disruptor and impairs fish reproduction. Environmental Science and Technology, 37(6), 1137–1141.  https://doi.org/10.1021/es02.CrossRefGoogle Scholar

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© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.Centre for Aquatic Environments, School of Pharmacy and Biomolecular SciencesUniversity of BrightonBrightonUK
  2. 2.Centre for Aquatic Environments, School of Environment and TechnologyUniversity of BrightonBrightonUK

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