REPRODUCTIVE CONDITION ASSOCIATED TO CHANGES IN THE LIPID-SOLUBLE ANTIOXIDANT CAPACITY AND DAMAGE TO LIPIDS IN THE SEA URCHINS LOXECHINUS ALBUS (ECHINODERMATA: ECHINOIDEA)
DOI:
https://doi.org/10.15359/revmar.3.14Keywords:
α-tocopherol, β-carotene, echinenone, lipid peroxidation, reproductive conditionsAbstract
The hypothesis of this study was that oxidative damage in the lipid phase of the gonad of the sea urchin Loxechinus albus increased during gametogenesis. Six different male and female reproductive conditions (reproductive stages) were described: (a) immature, (b) growing, (c) premature I, (d) premature II, (e) mature, and (f) spawned. The content of the lipid-soluble antioxidants, as well as the damage to lipids (assessed as the content of 2-thiobarbituric acid reactive substances (TBARS) and the content of lipid radicals) were analyzed. The content of the lipid-soluble antioxidants α-tocopherol (α-TH), β-carotene, and echinenone decreased during gametogenesis. In contrast, the content of both TBARS and lipid radicals increased. However, the consumption of lipid-soluble antioxidants was not sufficient to efficiently control lipid damage since the ratio of TBARS content/ α-TH content, taken as an index of damage/protection ratio, significantly increased during the mature stage. Therefore, an active food intake to incorporate antioxidants to the diet is required to adequately prepare the gonad for the next reproductive cycle.
References
Abele, D. & Puntarulo, S. (2004). Formation of reactive species and induction of antioxidant defence systems in polar and temperate marine invertebrates and fish. Comp. Biochem. Physiol. A., 138, 405-415.
Alonso-Álvarez, C., Bertrand, S., Devevey, G., Prost, J., Faivre, B., & Sorci, G. (2004). Increased susceptibility to oxidative stress as a proximate cost of reproduction. Ecol. Lett., 7(5), 363-368.
Alonso-Álvarez, C., Bertrand, S., Devevey, G., Prost, J., Faivre, B., Chastel, O., & Sorci, G. (2006). An experimental manipulation of life history trajectories and resistance to oxidative stress. Evolution, 60(9), 1913-1924.
Bernasconi, I. (1953). Monografía de los Equinoideos argentinos. An. Mus. His. Nat., Montevideo, 2nd Series 6(2), 23-25.
Bertrand, S., Alonso-Alvarez, C., Devevey, G., Faivre, B., Prost, J., & Sorci, G. (2006). Carotenoids modulate the trade-off between egg production and resistance to oxidative stress in zebra finches. Oecologia, 147, 576-584.
Borisovets, E. E., Zadorozhny, P. A., Kalinini, M. V., Lepskaya, N. V., & Yakush, E. V. (2002). Change of major carotenoids in gonads of sea urchins (Strongylocentrotus intermedius and S. nudus) at maturation. Comp. Biochem. Physiol. B., 132(4), 779-790.
Brazão, S., Morais, S., Boaventura, D., Ré, P., Narciso, L., & Hawkins, S. J. (2003). Spatial and temporal variation of the fatty acid composition of Patella spp. (Gastropoda: Prosobranchia) soft bodies and gonads. Comp. Biochem. Physiol. B., 136, 425-441.
Brewster, N. K. & Wheldrake, J. F. (1989). Free radical scavenging agents during the development of Dictyostelium discoideum. Biochem. Int., 19, 439-444.
Buchecker, R. (1982). A chemist’s view of animal carotenoids. In G. Britton & T. W. Goodwin (Eds.), Carotenoid chemistry and biochemistry. (pp. 175-193). Oxford, England.: Pergamon Press.
Buettner, G. R. (1987). Spin trapping: ESR parameters of spin adducts. Free Radic. Biol. Med., 3, 259-303.
Dayton, P. K. (1985). The structure and regulation of some South American kelp communities. Ecol. Monographs, 55(4), 447-468.
Desai, I. (1984). Vitamin E analysis methods for animal tissues. Meth. Enzymol., 105, 138-147.
Galleano, M., Aimo, L., & Puntarulo, S. (2002). Ascorbyl radical/ascorbate ratio in plasma from iron overloaded rats as oxidative stress indicator. Toxicol. Lett., 133(2, 3), 193-201.
George, S. B., Lawrence, J. M., Lawrence, A. L., Smiley, J., & Plank, L. (2001). Carotenoids in the adult diet enhance egg and juvenile production in the sea urchin Lytechinus Variegatus. Aquaculture, 199(3, 4), 353-369.
Gonor, J. J. (1972). Gonad growth in the sea urchin Strongylocentrotus purpuratus (Stimpson) (Echinodermata: Echinoidea) and the assumptions of gonad index methods. J. Exp. Mar. Biol. Ecol., 10(2), 89-103.
Goodwin, T. W. (1980). The biochemistry of the carotenoids. Vol. I, Plants. 2nd ed. London, England.: Chapman and Hall.
Halliwell, B. & Gutteridge, J. M. C. (1989). Free radicals in biology and medicine. 2nd ed. Oxford.: Clarendon Press.
Hernando, M. P. (2006). Efectos de la radiación solar sobre el fitoplancton de aguas Antárticas y sub-Antárticas. Unpublished doctoral thesis, Universidad de Buenos Aires, Facultad de Ciencias Exactas y Naturales, Buenos Aires, Argentina.
Karnaukhov, V. N. (2000). Functions of carotenoids as a subject of biophysical investigation. Biophysics, 45, 355-377.
Kawakami, T., Tsushima, M., Katabami, Y., Mine, M., Ishida, A., & Matsuno, T. (1998). Effect of ß,ß-carotene, ß-echinenone, astaxanthin, fucoxanthin, vitamin A and E on the biological defense of the sea urchin in Pseudocentrotus depressus. J. Exp. Mar. Biol. Ecol., 226(2), 165-174.
Kotake, Y., Tanigawa, T., Tanigawa, M., Ueno, I., Allen, D. R., & Lai, C. (1996). Continuous monitoring of cellular nitric oxide generation by spin trapping with an iron–dithiocarbamate complex. Biochim. Biophys. Acta, 1289(3), 362-368.
Krinsky, N. I. (1989). Antioxidant functions of carotenoids. Free Radic. Biol. Med., 7(6), 617-635.
Lai, E. K., Crossley, C., Sridhar, R., Misra, H. P., Janzen, E. G., & McCay, P. B. (1986). In vivo spin trapping of free radicals generated in brain, spleen, and liver during gamma radiation of mice. Arch. Biochem. Biophys., 244(1), 156-160.
Lamare, M. D. & Hoffman, J. (2004). Natural variation of carotenoids in the eggs and gonads of the echinoid genus, Strongylocentrotus: implications for their role in ultraviolet radiation photoprotection. J. Exp. Mar. Biol. Ecol., 312(2), 215-233.
Lattuca, M. E., Malanga, G., Aguilar Hurtado, C., Pérez, A. F., Calvo, J., & Puntarulo, S. (2009). Main features of the oxidative metabolism in gills and liver of Odontesthes nigricans Richardson (Pisces, Atherinopsidae). Comp. Biochem. Physiol. B, 154(4), 406-411.
Lukyanova, O. N. & Khotimchenko, J. S. (1995). Lipid-peroxidation in organs of the scallop Mizuhopecten yessoensis and sea-urchin Strongylocentrotus intermedius during the reproductive cycle. Biol. Scien., 110 (2), 371-377.
Lushchak, V. I. & Bagnyukova, T. (2006). Effects of different environmental oxygen levels on free radical processes in fish. Comp. Biochem. Physiol. B Biochem Mol Biol., 144(3), 283-289.
Malanga, G., Estevez, M. S., Calvo, J., & Puntarulo, S. (2004). Oxidative stress in limpets exposed to different environmental conditions in the Beagle Channel. Aquat. Toxicol., 69(4), 299-309.
Malanga, G., Estevez, M. S., Calvo, J., Abele, D., & Puntarulo S. (2007). The effect of seasonality on oxidative metabolism in Nacella (Patinigera) magellanica. Comp. Biochem. Physiol. A, 146, 551-558.
Malanga, G., Pérez, A. F., Calvo, J., & Puntarulo, S. (2009). The effect of seasonality on oxidative metabolism in the sea urchin Loxechinus albus. Mar. Biol., 156, 763-770.
Martin, I. & Grotewiel, M. S. (2006). Oxidative damage and age-related functional declines. Mech. Ageing Dev., 127(5), 411-423.
Matsuno, T. & Tsushima, M. (2001). Carotenoids in sea urchins. In J. M. Lawrence (Ed.), Edible sea urchins: biology and ecology. (pp. 115-138). Amsterdam, The Netherlands.: Elsevier Science.
Miller, N. J., Sampson, J., Candeias, L. P., Bramley, P. M., & Rice-Evans, C. A. (1996). Antioxidant activities of carotenes and xanthophylls. FEBS Lett., 384(3), 240-242.
Mortensen, A., Skibsted, L. H., Sampson, J., Rice-Evans, C. A., & Everett, S. A. (1997). Comparative mechanisms and rates of free radical scavenging by carotenoid antioxidants. FEBS Lett., 418(1, 2), 91-97.
Pérez, A. F., Morriconi, E., Boy, C., & Calvo, J. (2008). Energetic variation of the sea urchin Loxechinus albus at the southernmost limit of their distribution range (Beagle Channel, Tierra del Fuego). Polar Biol., 31, 443-449.
Pérez, A. F., Boy, C., Morriconi, E., & Calvo, J. (2010). Reproductive cycle and reproductive output of the sea urchin Loxechinus albus (Echinodermata: Echinoidea) from Beagle Channel, Tierra del Fuego, Argentina. Polar Biol., 33, 271-280.
Plank, L. R., Lawrence, J. M., Lawrence, A. L., & Montoya Olvera, R. (2002). The effect of dietary carotenoids on gonad production and carotenoid profiles in the sea urchin Lytechinus variegatus. J. World Aquacul. Soc., 33(2), 127-137.
Power, A. & Sheehan, D. (1996). Seasonal variations in the antioxidant defense systems of gill and digestive gland of the blue mussel, Mytilus edulis. Comp. Biochem. Physiol. C, 114(2), 99-103.
Sokal, R. & Rohlf, F. J. (1995). Biometry: The principles and practice of statistics in biological research. New York, USA.: W. H. Freeman and Company.
Speakman, J. R. (2008). The physiological costs of reproduction in small mammals. Phill. Trans. R. Soc. Lond. B Biol. Sci., 363, 375-398.
Tsushima, M. & Matsuno, T. (1990). Comparative biochemical studies of carotenoids in sea urchins-I. Comp. Biochem. Physiol. B, 96(4), 801-810.
Tsushima, M., Kawakami, T., & Matsuno, T. (1993). Metabolism of carotenoids in sea urchin Pseudocentrotus depressus. Comp. Biochem. Physiol. B, 106(3), 737-741.
Tsushima, M., Kawakami, T., Mine, M., & Matsuno, T. (1997). The role of carotenoids in the development of the sea urchin Pseudocentrotus depressus. Invert. Reprod. Develop., 32, 149-153.
Tsushima, M. & Matsuno, T. (1998). The role of beta-carotene on growth and survival of juvenile Japanese abalone Haliotis discus. Fish. Sci., 64(4), 660-661.
Tummeleht, L., Mägi, M., Kilgas, P., Mänd, R., & Hõrak, P. (2006). Antioxidant protection and plasma carotenoids of incubating great tits (Parus major L.) in relation to health state and breeding conditions. Comp. Biochem. Phys. C, 144(2), 166-172.
Viarengo, A., Canesi, L., Pertica, M., & Livingstone, D. R. (1991). Seasonal variations in the antioxidant defence enzymes and lipid peroxidation of the digestive gland of mussels. Comp. Biochem. Physiol. C, 100, 187-190.
Walker, C. W., Unuma, T., McGinn, N. A., Harrington, L. M., & Lesser, M. P. (2001). Reproduction of sea urchins. In J. M. Lawrence (Ed.), Edible sea urchins: biology and ecology (pp. 5-26). Amsterdam, The Netherlands.: Elsevier Science.
Wiersma, P., Selman, C., Speakman, J. R., & Verhulst, S. (2004). Birds sacrifice oxidative protection for reproduction. Proc. R. Soc. Lond. B Biol., 271, S360-S363.
Wilhelm Filho, D., Tribess, T. B., Gáspari, C., Claudio, F. D., Torres, M. A., & Magalhães, A. R. M. (2001). Seasonal changes in antioxidant defenses of the digestive gland of the brown mussel (Perna perna). Aquaculture, 203(1, 2), 149-158.
Yamamoto, M., Ishine, M., & Yoshida, M. (1988). Gonadal maduration independient of photic conditions in laboratory-reared sea urchins, Pseudocentrotus depressus and Hemicentrotus pulcherrimus. Zool. Sci. (Tokyo), 5(5), 979-988.
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