Colour Vision of the Amphipod Chaetogammarus olivia H. Milne Edwards, 1830 under Acute Light Exposure

V. A. Grintsov1,*, A. V. Kuznetsov1,2, S. N. Zheleznova1, V. I. Ryabushko1

1 Kovalevsky Institute of Biology of Southern Seas of RAS, Sevastopol, Russia

2 Sevastopol State University, Sevastopol, Russia

* e-mail: vgrintsov@gmail.com

Abstract

Light pollution in urbanized industrial areas disrupts the biological rhythms in animals. Artificial light penetrates the coastal zone, even to the bottom. The study of marine invertebrates' colour vision expands our understanding of animal perception of signals from the environment and is useful in urban landscape planning with artificial lighting. Amphipods are common in the seas and fresh waters, as well as on land; some live in the surf zone, which has led to the development of specific sensory systems, because air transmits light and sound differently than water. We studied colour perception in invertebrates living near the water's edge. The amphipods Chaetogammarus olivii H. Milne Edwards, 1830 were placed in a long narrow channel, part of which was closed from direct sunlight. C. olivii preferred to remain in the shade, where males formed dense clusters and females with eggs more often kept apart despite the active movement through the channel. Experiments revealed a similarity between the distribution of C. olivii in channels with colourful gradient LED lighting and the response to the laser beam. Animals avoided intense white, blue, and purple light, to a lesser extent green light, and did not respond to red light, while running away from light sources in complete darkness. Light pulses with durations and pauses of 1 s each, which may correspond in frequency characteristics to a weak surf, had no effect on C. olivii in contrast to random flashes of light. Perhaps the coastal inhabitants' ability to swiftly locate themselves in water or air is caused by their photoreception of blue and violet light. Modern light pollution is capable of disorienting animals in the dark, which may negatively affect the ecological situation of the splash zone.

Keywords

Amphipoda, colour vision, opsins, light smog, behavior

Acknowledgments

The authors are grateful to M. I. Silakov for drawing our attention to the light pollution issue, to A. V. Pirkova, E. V. Lisitskaya and R. G. Gevorgiz for discussion of the manuscript, and to Prof. I. V. Dovgal and Prof. Randy Nelson for useful suggestions. The work was performed under state assignment of FRC IBSS on topics: “Regularities of formation and anthropogenic transformation of biodiversity and bioresources of the Azov-Black Sea basin and other regions of the World Ocean” (state registration no. 118020890074-2) and “Study of control systems of biotechnological complex production processes aimed at development of scientific basis for obtaining biologically active agents and technical products of marine origin” (state registration no. 121030300149-0).

For citation

Grintsov, V.A., Kuznetsov, A.V., Zheleznova, S.N. and Ryabushko, V.I., 2022. Colour Vision of the Amphipod Chaetogammarus olivia H. Milne Edwards, 1830 under Acute Light Exposure. Ecological Safety of Coastal and Shelf Zones of Sea, (4), pp. 104–116. doi:10.22449/2413-5577-2022-4-104-116

DOI

10.22449/2413-5577-2022-4-104-116

References

  1. Yasukouchi, A. and Ishibashi, K., 2005. Non-Visual Effects of the Color Temperature of Fluorescent Lamps on Physiological Aspects in Humans. Journal of Physiological Anthropology and Applied Human Science, 24(1), pp. 41–43. doi:10.2114/jpa.24.41
  2. Chellappa, S.L., Steiner, R., Blattner, P., Oelhafen, P., Götz, T. and Cajochen, C., 2011. Non-Visual Effects of Light on Melatonin, Alertness and Cognitive Performance: Can Blue-Enriched Light Keep us Alert? PLoS One, 6(1). e16429. doi:10.1371/journal.pone.0016429
  3. Stefani, O., Freyburger, M., Veitz, S., Basishvili, T., Meyer, M., Weibel, J., Kobayashi, K., Shirakawa, Y. and Cajochen, C., 2021. Changing Color and Intensity of LED Lighting across the Day Impacts on Circadian Melatonin Rhythms and Sleep in Healthy Men. Journal of Pineal Research, 70(3), e12714. doi:10.1111/jpi.12714
  4. Xiao, H., Cai, H. and Li, X., 2021. Non-Visual Effects of Indoor Light Environment on Humans: A Review. Physiology and Behavior, 228, 113195. doi:10.1016/j.physbeh.2020.113195
  5. Fonken, L.K., Finy, M.S., Walton, J.C., Weil, Z.M., Workman, J.L., Ross, J. and Nelson, R.J., 2009. Influence of Light at Night on Murine Anxiety- and Depressive-Like Responses. Behavioral Brain Research, 205(2), pp. 349–354. doi:10.1016/j.bbr.2009.07.001
  6. Aulsebrook, A.E., Connelly, F., Johnsson, R.D., Jones, T.M., Mulder, R.A., Hall, M.L., Vyssotski, A.L. and Lesku, J.A., 2020. White and Amber Light at Night Disrupt Sleep Physiology in Birds. Current Biology, 30(18), pp. 3657–3663.e5. doi: 10.1016/j.cub.2020.06.085
  7. Briolat, E.S., Gaston, K.J., Bennie, J., Rosenfeld, E.J. and Troscianko, J. Artificial Nighttime Lighting Impacts Visual Ecology Links between Flowers, Pollinators and Predators. Nature Communications, 12, 4163. doi:10.1038/s41467-021-24394-0
  8. Forsburg, Z.R., Guzman, A., Gabor, C.R., 2021. Artificial Light at Night (ALAN) Affects the Stress Physiology but not the Behavior or Growth of Rana berlandieri and Bufo valliceps. Environmental Pollution, 277, 116775. doi:10.1016/j.envpol.2021.116775
  9. Tsujimura, T., 2020. Mechanistic Insights into the Evolution of the Differential Expression of Tandemly Arrayed Cone Opsin Genes in Zebrafish. Development, Growth, Differentiation, 62(7–8), pp. 465–475. doi:10.1111/dgd.12690
  10. Baden T. Circuit Mechanisms for Colour Vision in Zebrafish. Current Biology, 31(12), pp. R807–R820. doi:10.1016/j.cub.2021.04.053
  11. Henze, M.J. and Oakley, T.H., 2015. The Dynamic Evolutionary History of Pancrustacean Eyes and Opsins. Integrative and Comparative Biology, 55(5), pp. 830–842. doi:10.1093/icb/icv100
  12. Ullrich-Lüter, E.M., Dupont, S., Arboleda, E., Hausen, H. and Arnone, M.I., 2011. Unique System of Photoreceptors in Sea Urchin Tube Feet. Proceedings of the National Academy of Sciences of the USA, 108(20), pp. 8367–8372. doi:10.1073/pnas.1018495108
  13. Delroisse, J., Ullrich-Lüter, E., Ortega-Martinez, O., Dupont, S., Arnone, M.-I., Mallefet, J. and Flammang, P., 2014. High Opsin Diversity in a Non-Visual Infaunal Brittle Star. BMC Genomics, 15, 1035. doi:10.1186/1471-2164-15-1035
  14. Sergeeva, E.V, Fadeeva, M.V., Khavronyuk, I.S., Mamontov, A.A., Ershov, A.B. and Kuznetsov, A.V., 2022. Opsins of the Ctenophore Mnemiopsis leidyi and a Network of Protein-Protein Interactions. Russian Journal of Biological Physics and Chemistry, 7(2), pp. 222–229. doi:10.29039/rusjbpc.2022.0506
  15. Karaman, G.G., 1982. Genus Echinogammarus Stebbing. 1899. The Amphipoda of the Mediterranean. Memoires de l’Institut Oceanographique, 13, pp. 271–282.
  16. Makarov, Yu.N., 2004. [Fauna of Ukraine. Malacostraca]. Vol. 26, iss. 1–2. Kiev: Naukova Dumka, 430 p. (in Russian).
  17. Drozdova, P., Kizenko, A., Saranchina, A., Gurkov, A., Firulyova, M., Govorukhina, E. and Timofeyev, M., 2021. The Diversity of Opsins in Lake Baikal Amphipods (Amphipoda: Gammaridae). BMC Ecology and Evolution, 21(1), 81. doi:10.1186/s12862-021-01806-9
  18. Poynton, H.C., Hasenbein, S., Benoit, J.B., Sepulveda, M.S., Poelchau, M.F., Hughes, D.S.T., Murali, S.C., Chen, S., Glastad, K.M. et al., 2018. The Toxicogenome of Hyalella azteca: A Model for Sediment Ecotoxicology and Evolutionary Toxicology. Environmental Science and Technology, 52(10), pp. 6009–6022. doi:10.1021/acs.est.8b00837
  19. Karaman, G.G., 1982. Genus Eriopisa Stebbing, 1890. The Amphipoda of the Mediterranean. Memoires de l’Institut oceanographique, 1982, 13, pp. 291–293.
  20. Thurston, M.H. and Bett, B.J., 1993. Eyelessness in Marine Gammaridean Amphipoda (Crustacea): Geographical, Bathymetric and Taxonomic Considerations. Journal of Natural History, 27(4), pp. 861–881. doi:10.1080/00222939300770531
  21. Fong, D.W., 1989. Morphological Evolution of the Amphipod Gammarus minus in Caves: Quantitative Genetic Analysis. The American Midland Naturalist, 121(2), pp. 361–378. doi:10.2307/2426041
  22. Drozdova, P.B., Saranchina, A.E. and Timofeyev, M.A., 2020. Spectral Sensitivity of the Visual System of Endemic Baikal Amphipods. Limnology and Freshwater Biology, (4), pp. 781–782. doi:10.31951/2658-3518-2020-A-4-781
  23. Feuda, R., Hamilton, S.C., McInerney, J.O. and Pisani, D., 2012. Metazoan Opsin Evolution Reveals a Simple Route to Animal Vision. Proceedings of the National Academy of Sciences of the USA, 109(46), pp. 18868–18872. doi:10.1073/pnas.1204609109
  24. Ramos, A.P., Gustafsson, O., Labert, N., Salecker, I., Nilsson, D.E. and Averof, M., 2019. Analysis of the Genetically Tractable Crustacean Parhyale hawaiensis Reveals the Organisation of a Sensory System for Low-Resolution Vision. BMC Biology, 17(1), 67. doi:10.1186/s12915-019-0676-y
  25. Polinski, J.M., Zimin, A.V., Clark, K.F., Kohn, A.B., Sadowski, N., Timp, W., Ptitsyn, A., Khanna, P., Romanova, D.Y. et al., 2021. The American Lobster Genome Reveals Insights on Longevity, Neural, and Immune Adaptations. Science Advances, 7(26), eabe8290. doi:10.1126/sciadv.abe8290
  26. Schnitzler, C.E., Pang, K., Powers, M.L., Reitzel, A.M., Ryan, J.F., Simmons, D., Tada, T., Park, M., Gupta, J. et al., 2012. Genomic Organization, Evolution, and Expression of Photoprotein and Opsin Genes in Mnemiopsis leidyi: a New View of Ctenophore Photocytes. BMC Biology, 10, 107. doi:10.1186/1741-7007-10-107
  27. Kamm, K., Osigus, H.J., Stadler, P.F., DeSalle, R. and Schierwater, B., 2018. Trichoplax Genomes Reveal Profound Admixture and Suggest Stable Wild Populations without Bisexual Reproduction. Scientific Reports, 8(1), 11168. doi:10.1038/s41598-018-29400-y
  28. Khavroyuk, I.S., Mamontov, A.A., Bulkov, V.A., Voronin, D.P. and Kuznetsov, A.V., 2021. Assignment of Functions to Opsins of Trichoplax adhaerens and Trichoplax sp. H2. Russian Journal of Biological Physics and Chemistry, 6(4), pp. 686–694.
  29. Hubel, D.H. and Wiesel, T.N., 1979. Brain Mechanisms of Vision. Scientific American, 241, pp. 150–162. doi:10.1038/scientificamerican0979-150
  30. Hart, N.S., Lamb, T.D., Patel, H.R., Chuah, A., Natoli, R.C., Hudson, N.J., Cutmore, S.C., Davies, W.I.L., Collin, S.P. et al., 2020. Visual Opsin Diversity in Sharks and Rays. Molecular Biology and Evolution, 37(3), pp. 811–827. doi:10.1093/molbev/msz269
  31. Fernald, R.D., 2006. Casting a Genetic Light on the Evolution of Eyes. Science, 313(5795), pp. 1914–1918. doi:10.1126/science.1127889

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