Fitness costs and benefits of ultraviolet radiation exposure in marine pelagic copepods

Functional Ecology

Volumn 28, Issue 1, 2014, Pages 149-158

  Hylander, Samuel ^a   Grenvald, Julie Cornelius ^a   Kiørboe, Thomas ^a  

^a TECHNICAL UNIVERSITY OF DENMARK   (Denmark)

Author keywords

Calanoid copepod; Carotenoids; Life history; Mycosporine like amino acids; Phenotypic plasticity; Pigments; Ultraviolet radiation; Zooplankton

Indexed keywords

AMINO ACID; ANTIOXIDANT; CAROTENOID; CRUSTACEAN; FITNESS; IRRADIATION; LIFE HISTORY THEORY; LIFE HISTORY TRAIT; PELAGIC ECOSYSTEM; PHENOTYPIC PLASTICITY; RESOURCE ALLOCATION; ULTRAVIOLET RADIATION; ZOOPLANKTON;

ACARTIA TONSA; CALANOIDA; COPEPODA;

EID: 84892860565     PISSN: 02698463     EISSN: 13652435     Source Type: Journal    
DOI: 10.1111/1365-2435.12159     Document Type: Article

References (65)

1. Bandaranayake, W.M. (1998) Mycosporines: are they nature's sunscreens? Natural Product Reports, 15, 159-172.
2. Berggreen, U., Hansen, B. & Kiørboe, T. (1988) Food size spectra, ingestion and growth of the copepod Acartia-Tonsa during development - implications for determination of copepod production. Marine Biology, 99, 341-352.
3. Borgeraas, J. & Hessen, D.O. (2002) Variations of antioxidant enzymes in Daphnia species and populations as related to ambient UV exposure. Hydrobiologia, 477, 15-30.
4. Browman, H.I., Rodriguez, C.A., Beland, F., Cullen, J.J., Davis, R.F., Kouwenberg, J.H.M. et al. (2000) Impact of ultraviolet radiation on marine crustacean zooplankton and ichthyoplankton: a synthesis of results from the estuary and Gulf of St. Lawrence, Canada. Marine Ecology-Progress Series, 199, 293-311.
5. Cooke, S.L. & Williamson, C.E. (2006) Positive effects of UV radiation on a calanoid copepod in a transparent lake: do competition, predation or food availability play a role? Journal of Plankton Research, 28, 171-179.
6. Cooke, S.L., Williamson, C.E. & Saros, J.E. (2006) How do temperature, dissolved organic matter and nutrients influence the response of Leptodiaptomus ashlandi to UV radiation in a subalpine lake? Freshwater Biology, 51, 1827-1837.
7. Dahms, H.U., Dobretsov, S. & Lee, J.S. (2011) Effects of UV radiation on marine ectotherms in polar regions. Comparative Biochemistry and Physiology C-Toxicology & Pharmacology, 153, 363-371.
8. Garcia, P.E., Perez, A.P., Dieguez, M.D.C., Ferraro, M.A. & Zagarese, H.E. (2008) Dual control of the levels of photoprotective compounds by ultraviolet radiation and temperature in the freshwater copepod Boeckella antiqua. Journal of Plankton Research, 30, 817-827.
9. Goodwin, T.W. (1986) Metabolism, nutrition, and function of carotenoids. Annual Review of Nutrition, 6, 273-297.
10. Hairston, N.G. (1979a) Adaptive significance of color polymorphism in 2 species of Diaptomus (Copepoda). Limnology and Oceanography, 24, 15-37.
11. Hairston, N.G. (1979b) Relationship between pigmentation and reproduction in 2 species of Diaptomus (Copepoda). Limnology and Oceanography, 24, 38-44.
12. Hansson, L.A. (2000) Induced pigmentation in zooplankton: a trade-off between threats from predation and ultraviolet radiation. Proceedings of the Royal Society of London Series B-Biological Sciences, 267, 2327-2331.
13. Hansson, L.A. (2004) Plasticity in pigmentation induced by conflicting threats from predation and UV radiation. Ecology, 85, 1005-1016.
14. Hansson, L.A. & Hylander, S. (2009) Effects of ultraviolet radiation on pigmentation, photoenzymatic repair, behavior, and community ecology of zooplankton. Photochemical & Photobiological Sciences, 8, 1266-1275.
15. Hansson, L.A., Hylander, S. & Sommaruga, R. (2007) Escape from UV threats in zooplankton: a cocktail of behavior and protective pigmentation. Ecology, 88, 1932-1939.
16. Helbling, E.W. & Zagarese, H. (eds) (2003) UV Effects in Aquatic Organisms and Ecosystems. The Royal Society of Chemistry, Cambridge.
17. Hessen, D.O. (2008) Solar radiation and the evolution of life. Solar Radiation and Human Health (ed. E. Bjertness), pp. 123-136. The Norwegian Academy of Science and Letters, Oslo.
18. Hirst, A.G., Bonnet, D., Conway, D.V.P. & Kiørboe, T. (2010) Does predation control adult sex ratios and longevities in marine pelagic copepods? Limnology and Oceanography, 55, 2193-2206.
19. Holeton, C., Lindell, K., Holmborn, T., Hogfors, H. & Gorokhova, E. (2009) Decreased astaxanthin at high feeding rates in the calanoid copepod Acartia bifilosa. Journal of Plankton Research, 31, 661-668.
20. Hylander, S. & Jephson, T. (2010) UV protective compounds transferred from a marine dinoflagellate to its copepod predator. Journal of Experimental Marine Biology and Ecology, 389, 38-44.
21. Hylander, S., Larsson, N. & Hansson, L.A. (2009) Zooplankton vertical migration and plasticity of pigmentation arising from simultaneous UV and predation threats. Limnology and Oceanography, 54, 483-491.
22. Hylander, S., Boeing, W.J., Graneli, W., Karlsson, J., von Einem, J., Gutseit, K. et al. (2009) Complementary UV protective compounds in zooplankton. Limnology and Oceanography, 54, 1883-1893.
23. Hylander, S., Souza, M.S., Balseiro, E., Modenutti, B. & Hansson, L.A. (2012) Fish-mediated trait compensation in zooplankton. Functional Ecology, 26, 608-615.
24. Ianora, A. (1998) Copepod life history traits in subtemperate regions. Journal of Marine Systems, 15, 337-349.
25. Jonasdottir, S.H. & Kiørboe, T. (1996) Copepod recruitment and food composition: do diatoms affect hatching success? Marine Biology, 125, 743-750.
26. Juhl, A.R., Ohman, M.D. & Goericke, R. (1996) Astaxanthin in Calanus pacificus: assessment of pigment-based measures of omnivory. Limnology and Oceanography, 41, 1198-1207.
27. Karentz, D., Mceuen, F.S., Land, M.C. & Dunlap, W.C. (1991) Survey of mycosporine-like amino-acid compounds in antarctic marine organisms - potential protection from ultraviolet exposure. Marine Biology, 108, 157-166.
28. Kiørboe, T. (2008) A Mechanistic Approach to Plankton Ecology. Princeton University Press, Princeton and Oxford.
29. Kiørboe, T. & Hirst, A.G. (2008) Optimal development time in pelagic copepods. Marine Ecology-Progress Series, 367, 15-22.
30. Klein Breteler, W.C.M., Fransz, H.G. & Gonzalez, S.R. (1982) Growth and development of four calanoid copepod species under experimental and natural conditions. Netherlands Journal of Sea Research, 16, 195-207.
31. Kleppel, G.S., Frazel, D., Pieper, R.E. & Holliday, D.V. (1988) Natural diets of zooplankton off Southern-California. Marine Ecology-Progress Series, 49, 231-241.
32. Kuhn, P.S., Browman, H.I., Davis, R.F., Cullen, J.J. & McArthur, B.L. (2000) Modeling the effects of ultraviolet radiation on embryos of Calanus finmarchicus and Atlantic cod (Gadus morhua) in a mixing environment. Limnology and Oceanography, 45, 1797-1806.
33. Laurion, I., Lami, A. & Sommaruga, R. (2002) Distribution of mycosporine-like amino acids and photoprotective carotenoids among freshwater phytoplankton assemblages. Aquatic Microbial Ecology, 26, 283-294.
34. Leech, D.M. & Williamson, C.E. (2000) Is tolerance to UV radiation in zooplankton related to body size, taxon, or lake transparency? Ecological Applications, 10, 1530-1540.
35. Liu, Z.W., Hader, D.P. & Sommaruga, R. (2004) Occurrence of mycosporine-like amino acids (MAAs) in the bloom-forming cyanobacterium Microcystis aeruginosa. Journal of Plankton Research, 26, 963-966.
36. Llewellyn, C.A. & Airs, R.L. (2010) Distribution and abundance of MAAs in 33 species of microalgae across 13 classes. Marine Drugs, 8, 1273-1291.
37. Lotocka, M., Styczynska-Jurewicz, E. & Bledzki, L.A. (2004) Changes in carotenoid composition in different developmental stages of copepods: Pseudocalanus acuspes Giesbrecht and Acartia spp. Journal of Plankton Research, 26, 159-166.
38. Luecke, C. & Obrien, W.J. (1981) Photo-toxicity and fish predation - selective factors in color morphs in heterocope. Limnology and Oceanography, 26, 454-460.
39. MacFadyen, E.J., Williamson, C.E., Grad, G., Lowery, M., Jeffrey, W.H. & Mitchell, D.L. (2004) Molecular response to climate change: temperature dependence of UV-induced DNA damage and repair in the freshwater crustacean Daphnia pulicaria. Global Change Biology, 10, 408-416.
40. Malloy, K.D., Holman, M.A., Mitchell, D. & Detrich, H.W. (1997) Solar UVB-induced DNA damage and photoenzymatic DNA repair in Antarctic zooplankton. Proceedings of the National Academy of Sciences of the United States of America, 94, 1258-1263.
41. Moeller, R.E., Gilroy, S., Williamson, C.E., Grad, G. & Sommaruga, R. (2005) Dietary acquisition of photoprotective compounds (mycosporine-like amino acids, carotenoids) and acclimation to ultraviolet radiation in a freshwater copepod. Limnology and Oceanography, 50, 427-439.
42. Morris, D.P., Zagarese, H., Williamson, C.E., Balseiro, E.G., Hargreaves, B.R., Modenutti, B. et al. (1995) The attenuation of solar UV radiation in lakes and the role of dissolved organic carbon. Limnology and Oceanography, 40, 1381-1391.
43. Oren, A. & Gunde-Cimerman, N. (2007) Mycosporines and mycosporine-like amino acids: UV protectants or multipurpose secondary metabolites? Fems Microbiology Letters, 269, 1-10.
44. Palozza, P. & Krinsky, N.I. (1992) Antioxidant effects of carotenoids invivo and invitro - an overview. Methods in Enzymology, 213, 403-420.
45. Perez, A.P., Ferraro, M.A. & Zagarese, H.E. (2012) The relative contributions of diet and associated microbiota to the accumulation of UV-absorbing mycosporine-like amino acids in the freshwater copepod Boeckella antiqua. Freshwater Biology, 57, 993-1004.
46. Persaud, A.D., Moeller, R.E., Williamson, C.E. & Burns, C.W. (2007) Photoprotective compounds in weakly and strongly pigmented copepods and co-occurring cladocerans. Freshwater Biology, 52, 2121-2133.
47. Rautio, M., Bonilla, S. & Vincent, W.F. (2009) UV photoprotectants in arctic zooplankton. Aquatic Biology, 7, 93-105.
48. Rautio, M. & Tartarotti, B. (2010) UV radiation and freshwater zooplankton: damage, protection and recovery. Freshwater Reviews, 3, 105-131.
49. Ringelberg, J., Keyser, A.L. & Flik, B.J.G. (1984) The mortality effect of ultraviolet-radiation in a translucent and in a red morph of Acanthodiaptomus-Denticornis (Crustacea, Copepoda) and its possible ecological relevance. Hydrobiologia, 112, 217-222.
50. Sancar, A. (1994) Structure and function of DNA photolyase. Biochemistry, 33, 2-9.
51. Schneider, T., Herzig, A., Koinig, K.A. & Sommaruga, R. (2012) Copepods in Turbid Shallow Soda lakes accumulate unexpected high levels of carotenoids. PLoS ONE, 7, 1-11.
52. Sinha, R.P., Singh, S.P. & Hader, D.P. (2007) Database on mycosporines and mycosporine-like amino acids (MAAs) in fungi, cyanobacteria, macroalgae, phytoplankton and animals. Journal of Photochemistry and Photobiology B-Biology, 89, 29-35.
53. Sommaruga, R. (2010) Preferential accumulation of carotenoids rather than of mycosporine-like amino acids in copepods from high altitude Himalayan lakes. Hydrobiologia, 648, 143-156.
54. Sommer, F., Agurto, C., Henriksen, P. & Kiørboe, T. (2006) Astaxanthin in the calanoid copepod Calanus helgolandicus: dynamics of esterification and vertical distribution in the German Bight, North Sea. Marine Ecology-Progress Series, 319, 167-173.
55. Stearns, S.C. (1992) The Evolution of Life Histories. Oxford University Press, Oxford.
56. Tartarotti, B., Laurion, I. & Sommaruga, R. (2001) Large variability in the concentration of mycosporine-like amino acids among zooplankton from lakes located across an altitude gradient. Limnology and Oceanography, 46, 1546-1552.
57. Tartarotti, B. & Sommaruga, R. (2002) The effect of different methanol concentrations and temperatures on the extraction of mycosporine-like amino acids (MAAs) in algae and zooplankton. Archiv Fuer Hydrobiologie, 154, 691-703.
58. Tartarotti, B., Baffico, G., Temporetti, P. & Zagarese, H.E. (2004) Mycosporine-like amino acids in planktonic organisms living under different UV exposure conditions in Patagonian lakes. Journal of Plankton Research, 26, 753-762.
59. Tedetti, M. & Sempere, R. (2006) Penetration of ultraviolet radiation in the marine environment. A review. Photochemistry and Photobiology, 82, 389-397.
60. Vega, M.P. & Pizarro, R. (2000) Lethal effect induced by ultraviolet-B in a planktonic copepod: role of the post-irradiation time on mortality measurements. Journal of Freshwater Ecology, 15, 1-5.
61. Warton, D.I. & Hui, F.K.C. (2011) The arcsine is asinine: the analysis of proportions in ecology. Ecology, 92, 3-10.
62. Williamson, C.E., Fischer, J.M., Bollens, S.M., Overholt, E.P. & Breckenridge, J.K. (2011) Toward a more comprehensive theory of zooplankton diel vertical migration: integrating ultraviolet radiation and water transparency into the biotic paradigm. Limnology and Oceanography, 56, 1603-1623.
63. Yasui, H. & Sakurai, H. (2000) Chemiluminescent detection and imaging of reactive oxygen species in live mouse skin exposed to UVA. Biochemical and Biophysical Research Communications, 269, 131-136.
64. Zaret, T.M. (1972) Predators, invisible prey, and nature of polymorphism in Cladocera (Class Crustacea). Limnology and Oceanography, 17, 171-184.
65. Zengling, M.A., Wei, L.I. & Kunshan, G.A.O. (2010) Horizontal migration of Acartia pacifica Steuer (copepoda) in response to UV-radiation. Journal of Photochemistry and Photobiology B-Biology, 101, 233-237.