Advertisement

Journal of Comparative Physiology A

, Volume 200, Issue 11, pp 949–957 | Cite as

Differences in lens optical plasticity in two gadoid fishes meeting in the Arctic

  • Mikael Jönsson
  • Øystein Varpe
  • Tomasz Kozłowski
  • Jørgen Berge
  • Ronald H. H. Kröger
Original Paper

Abstract

Arctic and boreal/temperate species are likely to be evolutionary adapted to different light regimes. Currently, the boreal/temperate Atlantic cod (Gadus morhua) is coexisting with the native polar cod (Boreogadus saida) in the Arctic waters around Svalbard, Norway. Here, we studied light/dark adaptative optical plasticity of their eye lenses by exposing fish to bright light during the polar night. Schlieren photography, high-definition laser scanning and ray tracing were used to determine the optical properties of excised crystalline lenses. Both species have multifocal lenses, an optical adaptation for improved color vision. In polar cod, the optical properties of the lens were independent of light exposure. In the more southern Atlantic cod, the optical properties of the lens changed within hours upon exposure to light, even after months of darkness. Such fast optical adjustment has previously only been shown in a tropical cichlid. During the polar night the Atlantic cod lens seems to be unregulated and dysfunctional since it had an unsuitable focal length and severe spherical aberration. We present a system, to our knowledge unique, for studying visual plasticity on different timescales in relation to evolutionary history and present the first study on the polar cod visual system.

Keywords

Experiment Fish Multifocal lens Visual plasticity Global warming 

Abbreviations

BCD

Back center distance

BEP

Beam entrance position

LSA

Longitudinal spherical aberration

R

Lens radius

RIG

Refractive index gradient

RMM

Retinomotor movement

Notes

Acknowledgments

We thank Anne Christine Utne-Palm for connecting Øystein Varpe with the Vision Group at Lund University. The work was supported by Grants to Øystein Varpe from the Fram Centre in Tromsø and to Ronald Kröger from Knut and Alice Wallenberg foundation, and is part of the Research Council of Norway funded projects CircA (project number 214271/F20) and Marine Night (project number 226417). Experiments followed local legislation and were approved by the regional ethics committee for animal research, Malmö/Lund Ethical Committee on Animal Experiments (Dnr: M141-13).

References

  1. Aksnes DL, Nejstgaard J, Soedberg E, Sornes T (2004) Optical control of fish and zooplankton populations. Limnol Oceanogr 49(1):233–238CrossRefGoogle Scholar
  2. Anthony PD, Hawkins AD (1983) Spectral sensitivity of the cod Gadus morhua L. Mar Behav Physiol 10(2):145–165CrossRefGoogle Scholar
  3. Berge J, Batnes AS, Johnsen G, Blackwell SM, Moline MA (2012) Bioluminescence in the high Arctic during the polar night. Mar Biol 159(1):231–237. doi: 10.1007/s00227-011-1798-0 PubMedPubMedCentralCrossRefGoogle Scholar
  4. Bowmaker JK (2008) Evolution of vertebrate visual pigments. Vision Res 48(20):2022–2041. doi: 10.1016/j.visres.2008.03.025 PubMedCrossRefGoogle Scholar
  5. Burnside B, Nagle BW (1983) Retinomotor movements of photoreceptors and retinal pigment epithelium: mechanisms and regulation. Prog Retin Eye Res 2:67–109CrossRefGoogle Scholar
  6. Campbell MCW (1984) Measurement of refractive-index in an intact crystalline lens. Vision Res 24 (5):409. doi: 10.1016/0042-6989(84)90039-7
  7. Chapman CJ, Johnston ADF (1974) Some auditory discrimination experiments on marine fish. J Exp Biol 61(2):521–528PubMedGoogle Scholar
  8. Cook RM, Sinclair A, Stefansson G (1997) Potential collapse of North Sea cod stocks. Nature 385(6616):521–522. doi: 10.1038/385521a0 CrossRefGoogle Scholar
  9. Dahl TM, Lydersen C, Kovacs KM, Falk-Petersen S, Sargent J, Gjertz I, Gulliksen B (2000) Fatty acid composition of the blubber in white whales (Delphinapterus leucas). Polar Biol 23(6):401–409. doi: 10.1007/s003000050461 CrossRefGoogle Scholar
  10. DeWitt TJ, Sih A, Wilson DS (1998) Costs and limits of phenotypic plasticity. Trends Ecol Evol 13(2):77–81. doi: 10.1016/s0169-5347(97)01274-3 PubMedCrossRefGoogle Scholar
  11. Donner K (1987) Adaptation-related changes in the spatial and temporal summation of frog retinal ganglion cells. Acta Physiol Scand 131(4):479–487. doi: 10.1111/j.1748-1716.1987.tb08267.x PubMedCrossRefGoogle Scholar
  12. Douglas RH (1982) The function of photomechanical movements in the retina of rainbow trout (Salmo gairdneri). J Exp Biol 96 (FEB):389-403 Google Scholar
  13. Duke-Elder S (1958) The eye in evolution. In: Duke-Elder S (ed) System of ophthalmology, vol 1. Klimpton, London, pp 303–304Google Scholar
  14. Evans BI, Fernald RD (1993) Retinal transformation at metamorphosis in the winter flounder (Pseudopleuronectes americanus). Visual Neurosci 10(6):1055–1064CrossRefGoogle Scholar
  15. Gagnon Y, Söderberg B, Kröger R (2012) Optical advantages and function of multifocal spherical fish lenses. J Opt Soc Am A-Opt Image Sci Vis 29(9):1786–1793PubMedCrossRefGoogle Scholar
  16. Hawkins AD, Sand O (1977) Directional hearing in the median vertical plane by the cod. J Comp Physiol 122(1):1–8CrossRefGoogle Scholar
  17. Hop H, Gjøsæter H (2013) Polar cod (Boreogadus saida) and capelin (Mallotus villosus) as key species in marine food webs of the Arctic and the Barents Sea. Mar Biol Res 9(9):878–894. doi: 10.1080/17451000.2013.775458 CrossRefGoogle Scholar
  18. Hutchings JA, Myers RA (1994) What can be learned from the collapse of a renewable resource? Atlantic cod, Gadus morhua, of Newfoundland and Labrador. Can J Fish Aquat Sci 51(9):2126–2146. doi: 10.1139/f94-214 CrossRefGoogle Scholar
  19. Johnsen S (2012) The optics of life : a biologist’s guide to light in nature. Princeton University Press, Princeton, NJGoogle Scholar
  20. Kaartvedt S (2008) Photoperiod may constrain the effect of global warming in arctic marine systems. J Plankton Res 30(11):1203–1206. doi: 10.1093/plankt/fbn075 CrossRefGoogle Scholar
  21. Karpestam B, Gustafsson J, Shashar N, Katzir G, Kroger RHH (2007) Multifocal lenses in coral reef fishes. J Exp Biol 210(16):2923–2931. doi: 10.1242/jeb.002956 PubMedCrossRefGoogle Scholar
  22. Kröger RHH (2011) Physiological Optics in Fishes. In: Farrell AP (ed) Encyclopedia of fish physiology: From genome to environment, vol 1. Academic Press, San Diego, pp 102–109CrossRefGoogle Scholar
  23. Kröger RHH (2013) Optical plasticity in fish lenses. Prog Retin Eye Res 34:78–88. doi: 10.1016/j.preteyeres.2012.12.001 PubMedCrossRefGoogle Scholar
  24. Kröger RHH, Campbell MCW, Munger R, Fernald RD (1994) Refractive index distribution and spherical abberation in the crystalline lens of the African cichlid fish Haplochromis burtoni. Vision Res 34(14):1815–1822. doi: 10.1016/0042-6989(94)90306-9 PubMedCrossRefGoogle Scholar
  25. Kröger RHH, Campbell MCW, Fernald RD, Wagner HJ (1999) Multifocal lenses compensate for chromatic defocus in vertebrate eyes. J Comp Physiol A-Sens Neural Behav Physiol 184(4):361–369. doi: 10.1007/s003590050335 CrossRefGoogle Scholar
  26. Kröger RHH, Campbell MCW, Fernald RD (2001) The development of the crystalline lens is sensitive to visual input in the African cichlid fish Haplochromis burtoni. Vision Res 41(5):549–559. doi: 10.1016/s0042-6989(00)00283-2 PubMedCrossRefGoogle Scholar
  27. Labansen AL, Lydersen C, Haug T, Kovacs KM (2007) Spring diet of ringed seals (Phoca hispida) from northwestern Spitsbergen Norway. Ices J Mar Sci 64(6):1246–1256. doi: 10.1093/icesjms/fsm090 Google Scholar
  28. Land MF, Nilsson D-E (2012) Animal eyes. Oxford University Press, OxfordCrossRefGoogle Scholar
  29. Malkki PE, Kröger RHH (2005) Visualization of chromatic correction of fish lenses by multiple focal lengths. J Opt A-Pure Appl Op 7(11):691–700. doi: 10.1088/1464-4258/7/11/012 CrossRefGoogle Scholar
  30. Marcoux M, McMeans BC, Fisk AT, Ferguson SH (2012) Composition and temporal variation in the diet of beluga whales, derived from stable isotopes. Mar Ecol Prog Ser 471:283–291. doi: 10.3354/meps10029 CrossRefGoogle Scholar
  31. Matley JK, Fisk AT, Dick TA (2012) Seabird predation on Arctic cod during summer in the Canadian Arctic. Mar Ecol Prog Ser 450:219–228. doi: 10.3354/meps09561 CrossRefGoogle Scholar
  32. Maxwell JC (1854) Solutions of problems. The Cambridge and Dublin Mathematical Journal 9:9–11Google Scholar
  33. Meager JJ, Solbakken T, Utne-Palm AC, Oen T (2005) Effects of turbidity on the reactive distance, search time, and foraging success of juvenile Atlantic cod (Gadus morhua). Can J Fish Aquat Sci 62(9):1978–1984. doi: 10.1139/f05-104 CrossRefGoogle Scholar
  34. Mehlum F, Hunt GL, Klusek Z, Decker MB, Nordlund N (1996) The importance of prey aggregations to the distribution of Brunnich’s guillemots in Storfjorden Svalbard. Polar Biol 16(8):537–547CrossRefGoogle Scholar
  35. Nahrgang J, Varpe O, Korshunova E, Murzina S, Hallanger IG, Vieweg I, Berge J (2014) Gender Specific Reproductive Strategies of an Arctic Key Species (Boreogadus saida) and Implications of Climate Change. PLoS One 9 (5). doi: 10.1371/journal.pone.0098452
  36. Nicol JAC (1989) The eyes of fishes. Oxford University Press, OxfordGoogle Scholar
  37. Niven JE, Laughlin SB (2008) Energy limitation as a selective pressure on the evolution of sensory systems. J Exp Biol 211(11):1792–1804. doi: 10.1242/jeb.017574 PubMedCrossRefGoogle Scholar
  38. Orlova EL, Dolgov AV, Rudneva GB, Oganin IA, Konstantinova LL (2009) Trophic relations of capelin Mallotus villosus and polar cod Boreogadus saida in the Barents Sea as a factor of impact on the ecosystem. Deep-Sea Res Pt II 56(21–22):2054–2067. doi: 10.1016/j.dsr2.2008.11.016 CrossRefGoogle Scholar
  39. Parry JWL, Carleton KL, Spady T, Carboo A, Hunt DM, Bowmaker JK (2005) Mix and match color vision: Tuning spectral sensitivity by differential opsin gene expression in Lake Malawi Cichlids. Curr Biol 15(19):1734–1739. doi: 10.1016/j.cub.2005.08.010 PubMedCrossRefGoogle Scholar
  40. Perry AL, Low PJ, Ellis JR, Reynolds JD (2005) Climate change and distribution shifts in marine fishes. Science 308(5730):1912–1915. doi: 10.1126/science.1111322 PubMedCrossRefGoogle Scholar
  41. Pierscionek BK, Regini JW (2012) The gradient index lens of the eye: An opto-biological synchrony. Prog Ret Eye Res 31(4):332–349. doi: 10.1016/j.preteyeres.2012.03.001 CrossRefGoogle Scholar
  42. Reed TE, Waples RS, Schindler DE, Hard JJ, Kinnison MT (2010) Phenotypic plasticity and population viability: the importance of environmental predictability. P Roy Soc Lond B Biol 277(1699):3391–3400. doi: 10.1098/rspb.2010.0771 CrossRefGoogle Scholar
  43. Schartau JM, Sjögreen B, Gagnon YL, Kröger RHH (2009) Optical Plasticity in the Crystalline Lenses of the Cichlid Fish Aequidens pulcher. Curr Biol 19(2):122–126. doi: 10.1016/j.cub.2008.11.062 PubMedCrossRefGoogle Scholar
  44. Schartau JM, Kröger RHH, Sjögreen B (2010) Short-term culturing of teleost crystalline lenses combined with high-resolution optical measurements. Cytotechnology 62(2):167–174. doi: 10.1007/s10616-010-9268-y PubMedPubMedCentralCrossRefGoogle Scholar
  45. Varpe O, Fiksen O (2010) Seasonal plankton-fish interactions: light regime, prey phenology, and herring foraging. Ecology 91(2):311–318. doi: 10.1890/08-1817.1 PubMedCrossRefGoogle Scholar
  46. Wagner HJ, Kröger RHH (2005) Adaptive plasticity during the development of colour vision. Prog Retin Eye Res 24(4):521–536. doi: 10.1016/j.preteyeres.2005.01.002 PubMedCrossRefGoogle Scholar
  47. Walls GL (1942) The vertebrate eye and its adaptive radiation. McGraw-Hill, New YorkCrossRefGoogle Scholar
  48. Webster CN, Varpe Ø, Falk-Petersen S, Berge J, Stübner E, Brierley AS (2013) Moonlit swimming: vertical distributions of macrozooplankton and nekton during the polar night. Polar Biol. doi: 10.1007/s00300-013-1422-5 Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Mikael Jönsson
    • 1
  • Øystein Varpe
    • 2
    • 3
  • Tomasz Kozłowski
    • 1
  • Jørgen Berge
    • 3
    • 4
  • Ronald H. H. Kröger
    • 1
  1. 1.Lund Vision Group, Functional Zoology, Department of BiologyLund UniversityLundSweden
  2. 2.Akvaplan-nivaTromsøNorway
  3. 3.The University Centre in SvalbardLongyearbyenNorway
  4. 4.Faculty of Biosciences, Fisheries and EconomyUniversity of TromsøTromsøNorway

Personalised recommendations