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.
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Abbreviations
- BCD:
-
Back center distance
- BEP:
-
Beam entrance position
- LSA:
-
Longitudinal spherical aberration
- R:
-
Lens radius
- RIG:
-
Refractive index gradient
- RMM:
-
Retinomotor movement
References
Aksnes DL, Nejstgaard J, Soedberg E, Sornes T (2004) Optical control of fish and zooplankton populations. Limnol Oceanogr 49(1):233–238
Anthony PD, Hawkins AD (1983) Spectral sensitivity of the cod Gadus morhua L. Mar Behav Physiol 10(2):145–165
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
Bowmaker JK (2008) Evolution of vertebrate visual pigments. Vision Res 48(20):2022–2041. doi:10.1016/j.visres.2008.03.025
Burnside B, Nagle BW (1983) Retinomotor movements of photoreceptors and retinal pigment epithelium: mechanisms and regulation. Prog Retin Eye Res 2:67–109
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
Chapman CJ, Johnston ADF (1974) Some auditory discrimination experiments on marine fish. J Exp Biol 61(2):521–528
Cook RM, Sinclair A, Stefansson G (1997) Potential collapse of North Sea cod stocks. Nature 385(6616):521–522. doi:10.1038/385521a0
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
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
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
Douglas RH (1982) The function of photomechanical movements in the retina of rainbow trout (Salmo gairdneri). J Exp Biol 96 (FEB):389-403
Duke-Elder S (1958) The eye in evolution. In: Duke-Elder S (ed) System of ophthalmology, vol 1. Klimpton, London, pp 303–304
Evans BI, Fernald RD (1993) Retinal transformation at metamorphosis in the winter flounder (Pseudopleuronectes americanus). Visual Neurosci 10(6):1055–1064
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):1786–1793
Hawkins AD, Sand O (1977) Directional hearing in the median vertical plane by the cod. J Comp Physiol 122(1):1–8
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
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
Johnsen S (2012) The optics of life : a biologist’s guide to light in nature. Princeton University Press, Princeton, NJ
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
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
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 102–109
Kröger RHH (2013) Optical plasticity in fish lenses. Prog Retin Eye Res 34:78–88. doi:10.1016/j.preteyeres.2012.12.001
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
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
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
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
Land MF, Nilsson D-E (2012) Animal eyes. Oxford University Press, Oxford
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
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
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
Maxwell JC (1854) Solutions of problems. The Cambridge and Dublin Mathematical Journal 9:9–11
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
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):537–547
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
Nicol JAC (1989) The eyes of fishes. Oxford University Press, Oxford
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
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
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
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
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
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
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
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
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
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
Walls GL (1942) The vertebrate eye and its adaptive radiation. McGraw-Hill, New York
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
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).
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Jönsson, M., Varpe, Ø., Kozłowski, T. et al. Differences in lens optical plasticity in two gadoid fishes meeting in the Arctic. J Comp Physiol A 200, 949–957 (2014). https://doi.org/10.1007/s00359-014-0941-z
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DOI: https://doi.org/10.1007/s00359-014-0941-z