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Optical quality changes of the ocular lens during induced parr-to-smolt metamorphosis in Rainbow Trout (Oncorhynchus mykiss)

Ocular lens optical quality during induced salmonid metamorphosis

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Abstract

The effect of an induced salmonid parr-to-smolt metamorphosis (‘smoltification’) on the optical quality of the ocular lens was studied. In two separate experiments, rainbow trout (Oncorhynchus mykiss) parr were fed thyroxine in their diet to induce the metamorphosis. Lenses were excised at regular samplings during the treatment period and optically scanned using a custom scanning laser monitor. Radioimmunoassay was used to measure serum titers of thyroxine and 3,5,3′-triiodo-L-thyronine. It was found that lens optical quality was consistently negatively correlated with 3,5,3′-triiodo-L-thyronine levels, but not with thyroxine levels. To test if thyroid hormones are directly responsible for the change in optical quality, rainbow trout lenses were cultured for 72 h in a medium containing 3,5,3′-triiodo-L-thyronine, but no effect was observed. The significance of these findings in the contexts of the fishes’ visual capabilities and smolting physiology is discussed.

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Abbreviations

BVD:

Back vertex distance

RIA:

Radioimmunoassay

SLM:

Scanning laser monitor

References

  • Age-Related Eye Disease Study Research Group (2001) Risk factors associated with age-related nuclear and cortical cataract: a case-control study in the age-related eye disease study, AREDS report no. 5. Ophthalmology 108:1400–1408

    Article  PubMed  Google Scholar 

  • Allen DM (1977) Measurements of serum thyroxine and the proportions of rhodopsin and porphyropsin in rainbow trout. Can J Zool 55:836–842

    CAS  PubMed  Google Scholar 

  • Allison WE, Dann SG, Helvik J-V, Bradley C, Moyer H, Hawryshyn CW (2003) Ontogeny of ultraviolet-sensitive cones in the retina of rainbow trout (Oncorhynchus mykiss). J Comp Neurol 461:294–306

    Article  PubMed  Google Scholar 

  • Beatty DD (1966) A study of the succession of visual pigments in Pacific salmon (Oncorhynchus). Can J Zool 44:429–455

    CAS  PubMed  Google Scholar 

  • Beatty DD (1972) Visual pigment changes in salmonid fishes in response to exogenous L-thyroxine, bovine TSH and 3-dehydroretinol. Vision Res 12:1947–1960

    Article  CAS  PubMed  Google Scholar 

  • Bjerkås E, Waagbø R, Sveier H, Breck O, Bjerkås I, Bjørnestad E, Maage A (1996) Cataract development in Atlantic salmon (Salmo salar L.) in fresh water. Acta Vet Scand 37:351–360

    PubMed  Google Scholar 

  • Bjerkås E, Holst JC, Bjerkås I, Ringvold A (2003) Osmotic cataract causes reduced vision in wild Atlantic salmon postsmolts. Aquaculture 55:151–159

    Google Scholar 

  • Boeuf G (1993) Salmonid smolting: a pre-adaptation to the oceanic environment. In: Rankin JC, Jensen FB (eds) Fish ecophysiology. Chapman & Hall, London, pp 105–135

    Google Scholar 

  • Breck O, Sveier H (2001) Growth and cataract development in two groups of Atlantic salmon (Salmo salar L) post smolts transferred to sea with a four week interval. Bull Eur Assoc Fish Pathol 26:91–103

    Google Scholar 

  • Browman HI, Hawryshyn CW (1992) Thyroxine induces a precocial loss of ultraviolet photosensitivity in rainbow trout (Oncorhynchus mykiss, Teleostei). Vis Res 32:2303–2312

    Article  CAS  PubMed  Google Scholar 

  • Browman HI, Hawryshyn CW (1994) The developmental trajectory of ultraviolet photosensitivity in rainbow trout is altered by thyroxine. Vis Res 34:1397–1406

    Article  CAS  PubMed  Google Scholar 

  • Browman HI, Novales-Flamarique I, Hawryshyn CW (1993) Ultraviolet photoreception contributes to prey search behavior in two species of zooplanktivorous fishes. J Exp Biol 192:187–198

    Google Scholar 

  • Carew LB, McMurtry JP, Alster FA (2003) Effects of methionine deficiencies on plasma levels of thyroid hormones, insulin-like growth factors-I and-II, liver and body weights, and feed intake in growing chickens. Poul Sci 82:1932–1938

    CAS  Google Scholar 

  • Clarke WC, Shelbourn JE, Brett JR (1978) Growth and adaptation to sea water in “underyearling” sockeye (Oncorhynchus nerka) and coho (Oncorhynchus kisutch) salmon subject to regimes of constant or changing temperature and day length. Can J Zool 56:2413–2421

    Google Scholar 

  • Clarke WC, Shelbourn JE, Brett JR (1981) Effect of artificial photoperiod cycles, temperature, and salinity on growth and smolting in underyearling coho (Oncorhynchus kisutch), chinook (O. tshawytscha) and sockeye (O. nerka) salmon. Aquaculture 22:105–116

    Article  Google Scholar 

  • Clarke WC, Shelbourn JE, Ogasawara T, Hirano T (1989) Effect of initial daylength on growth, seawater adaptability and plasma growth hormone levels in underyearling coho, chinook and chum salmon. Aquaculture 82:51–62

    Article  CAS  Google Scholar 

  • Cowey CB, Cho CY, Sivak JG, Weerheim JA, Stuart DD (1992) Methionine intake in rainbow trout (Oncorhynchus mykiss), relationship to cataract formation and the metabolism of methionine. J Nutr 122:1154–1163

    CAS  PubMed  Google Scholar 

  • Dickhoff WW, Folmar LC, Mighell JL, Mahnken VW (1982) Plasma thyroid hormones during smoltification of yearling and underyearling coho salmon and yearling chinook salmon and steelhead trout. Aquaculture 28:39–48

    Article  CAS  Google Scholar 

  • Dodd MHI, Dodd JM (1976) The biology of metamorphosis. In: Lofts B (ed) Physiology of the amphibia, vol 3. Academic, New York, pp 467–599

    Google Scholar 

  • Dorfman-Hecht JE, Sivak JG, Doughty MJ, Moccia RD (1994) Acute effects of NUVAN on the optical and biochemical properties of cultured Atlantic salmon (Salmo salar) lenses. In Vitro Toxicol 7:339–349

    CAS  Google Scholar 

  • Duker GJ (1982) Instream orientation and species recognition by Pacific salmon. In: Brannon EL, Salo EO (eds) Proceedings of the salmon and trout migratory behavior symposium. School of Fisheries, University of Washington, Seattle, pp 286–295

  • Duston J (1994) Effect of salinity on survival and growth of Atlantic salmon (Salmo salar) parr and smolts. Aquaculture 121:115–124

    Article  CAS  Google Scholar 

  • Eales JG (1979) Thyroid in cyclostomes and fishes. In: Barrington EJW (ed) Hormones and evolution, vol 1. Academic, London, pp 341–436

    Google Scholar 

  • Eales JG (1997) Iodine metabolism and thyroid-related functions in organisms lacking thyroid follicles: are thyroid hormones also vitamins? Proc Soc Exp Biol Med 214:302–317

    CAS  PubMed  Google Scholar 

  • Edelhauser HF (1968) Sodium and water permeability of salt-water fish corneas. Comp Biochem Physiol 24:665–667

    Article  CAS  PubMed  Google Scholar 

  • Eriksson L-O, Lundqvist H (1982) Circannual rhythms and photoperiod regulation of growth and smolting in Baltic salmon (Salmo salar L.). Aquaculture 28:113–121

    Article  Google Scholar 

  • Ersdal C, Midtlyng PJ, Jarp J (2001) An epidemiological study of cataracts in seawater farmed Atlantic salmon Salmo salar. Dis Aquat Organ 45:229–236

    CAS  PubMed  Google Scholar 

  • Farbridge KJ, Leatherland JF (1991) Biweekly patterns of change in food-consumption, plasma thyroid-hormone and growth-hormone levels, and in vitro hepatic monodeiodination of T4 in rainbow trout, Oncorhynchus mykiss. J Interdiscipl Cycle Res 22:237–248

    CAS  Google Scholar 

  • Fernald RD (1988) Aquatic adaptations in fish eyes. In: Atema J, Fay RR, Popper AN, Tavolga WN (eds) Sensory biology of aquatic animals. Springer, New York, pp 435–466

    Google Scholar 

  • Finnson KW, Eales JG (1999) Effect of T3 treatment and food ration on hepatic deiodination and conjugation of thyroid hormones in rainbow trout, Oncorhynchus mykiss. Gen Comp Endocrinol 115:379–386

    Article  CAS  PubMed  Google Scholar 

  • Galton VA (1983) Thyroid hormone action in amphibian metamorphosis. In: Oppenheimer JH, Samuels HH (eds) Molecular basis of thyroid hormone action. academic, New York, pp 445–483

    Google Scholar 

  • Groves AB, Collins GB, Trefethen PS (1968) Roles of olfaction and vision in choice of spawning site by homing adult chinook salmon (Oncorhynchus tsawytscha). J Fish Res Bd Can 25:867–876

    Google Scholar 

  • Hawryshyn CW, Bolger AE (1990) Spatial orientation of trout to partially polarized light. J Comp Physiol A 167:691–697

    Article  Google Scholar 

  • Hikida M, Iwata S (1987) In vitro subacute cataractogenic study in rainbow trout lenses. J Pharmacobiol dynam 10:443–448

    CAS  Google Scholar 

  • Hoar WS (1939) The thyroid gland of the Atlantic salmon. J Morphol 65:257–295

    Article  Google Scholar 

  • Hoar WS (1951) Hormones in fish. Pub Ontario Dish Res Lab 71. Univ Toronto Biol Ser 59:1–111

    Google Scholar 

  • Hoar WS (1958) The evolution of migratory behaviour among juvenile salmon of the genus Oncorhynchus. J Fish Res Bd Can 15:391–428

    Google Scholar 

  • Hoar WS (1988) The physiology of smolting salmonids. In: Hoar WS, Randall DJ (eds) Fish Physiology, vol XIB. Academic, New York, pp 275–343

    Google Scholar 

  • Hutchison MJ, Iwata M (1998). Effect of thyroxine on the decrease of aggressive behaviour of four salmonids during the parr-smolt transformation. Aquaculture 168:169–175

    Article  CAS  Google Scholar 

  • Iwata M (1995) Downstream migratory behavior of salmonids and its relationship with cortisol and thyroid hormones: a review. Aquaculture 135:131–139

    Article  CAS  Google Scholar 

  • Iwata M, Komatsu S, Collie NL, Nishioka RS, Bern HA (1987) Ocular cataract and seawater adaptation in salmonids. Aquaculture 66:315–327

    Article  Google Scholar 

  • Kato F (1991) Life histories of masu and amago salmon (Oncorhynchus masou and Oncorhynchus rhodurus). In: Groot C, Margolis L (eds) Pacific Salmon Life Histories. UBC Press, Vancouver, pp 447–520

    Google Scholar 

  • Menzies FD, Crockford T, Breck O, Midtlyng PJ (2002) Estimation of direct costs associated with cataracts in farmed Atlantic salmon (Salmo salar). Bull Eur Ass Fish Pathol 22:27–32

    Google Scholar 

  • Miwa S, Inui Y (1987) Effects of various doses of thyroxine and triiodothyronine on the metamorphosis of flounder (Paralichthys olivaceus). Gen Comp Endocrinol 67:356–363

    Article  CAS  PubMed  Google Scholar 

  • Miwa S, Tagawa M, Inui Y, Hirano T (1988) Thyroxine surge in metamorphosing flounder larvae. Gen Comp Endocrinol 70:158–163

    Article  CAS  PubMed  Google Scholar 

  • Morin PP, Dodson JJ, Doré FY (1989) Cardiac responses to a natural odorant as evidence of a sensitive period for olfactory imprinting in young Atlantic salmon, Salmo salar. Can J Fish Aquat Sci 46:122–130

    Google Scholar 

  • Nicol JAC (1989) The eyes of fishes. Oxford University Press, New York, p 308

    Google Scholar 

  • Oppenheimer JH (1983) The nuclear receptor-triiodothyronine complex: relationship to thyroid hormone distribution, metabolism, and biological action. In: Oppenheimer JH, Samuels HH (eds) Molecular basis of thyroid hormone action. Academic, New York, pp 1–34

    Google Scholar 

  • Parkyn DC, Austin J, Hawryshyn CW (2003) Orientation of salmonids to polarized light: laboratory studies. Anim Behav 65:893–904

    Article  Google Scholar 

  • Plate EM, Adams BA, Allison WE, Martens G, Hawryshyn CW, Eales JG (2002) The effects of thyroxine or a GnRH analogue on thyroid hormone deiodination in the olfactory epithelium and retina of rainbow trout, Oncorhynchus mykiss, and sockeye salmon, O. nerka. Gen Comp Endocrinol 127:59–65

    Article  CAS  PubMed  Google Scholar 

  • Ramsden DB (1977) Peripheral Metabolism and Action of Thyroid Hormones, vol 2. Eden Inc., Montréal

    Google Scholar 

  • Sivak JG (1990) Optical variability of the fish lens. In: Douglas RH, Djamgoz MBA (eds) The Visual system of fish. Chapman and Hall, London, pp 63–80

    Google Scholar 

  • Sklower A (1930) Die bedeutung der schilddruse fur die metamorphose des aales und der plattfische. Forsch Fortschr Dtsch Wiss 6:435–436

    Google Scholar 

  • Snyder AW, Bossomaier TRJ, Hughes A (1986) Optical image quality and the cone mosaic. Science 231:499–501

    CAS  PubMed  Google Scholar 

  • Tagawa M, Iwata M (1991) Effect of thyroxine surge on kokanee salmon migration: 1. Dietary thyroxine treatment. Zoolog Sci 8:1172

    Google Scholar 

  • Weerheim JA, Sivak JG (1992) Scanning laser measure of optical quality of the cultured crystalline lens. Ophthalmic Physiol Opt 12:72–79

    Article  CAS  PubMed  Google Scholar 

  • Weinsieder A, Worgul BV, Rosenbaum D, Rothstein H (1972) Enhancement of mitotic activity by thyroxin and triiodothyronine. J Cell Biol 55:275A

    Google Scholar 

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Acknowledgements

We kindly thank Vladimir Bantseev, Nancy Gibson, Robin Jones, Kelley Moran and Martin Ryan of the University of Waterloo for their practical insights and technical support during the course of this research. Special thanks are offered to Drs. Munehico Iwata and Geoff Eales for methodological assistance. We would finally like to thank two anonymous reviewers for raising points which allowed us to improve the manuscript. This research was funded by the Natural Sciences and Engineering Research Council of Canada. These experiments comply with the ”Principles of animal care“, publication no. 86–23, revised 1985 of the National Institute of Health, and also with the current laws of Canada.

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Correspondence to Kevin L. H. van Doorn.

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van Doorn, K.L.H., Sivak, J.G. & Vijayan, M.M. Optical quality changes of the ocular lens during induced parr-to-smolt metamorphosis in Rainbow Trout (Oncorhynchus mykiss). J Comp Physiol A 191, 649–657 (2005). https://doi.org/10.1007/s00359-005-0615-y

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