Abstract
In this study, we examine changes in fatty acid composition of polar and neutral lipids in gill, liver, and muscle of freshwater alewives (Alosa pseudoharengus) after temperature challenges in the laboratory. Alewives experienced either a warm or cold challenge in which temperatures were raised or lowered 0.5°C day−1 over 4–6 weeks. In alewives experiencing the cold challenge, gill polar lipids showed evidence of significant remodeling, including decreases in palmitic acid and saturated fatty acids and increases in n-3 and n-6 highly unsaturated fatty acids including docosahexaenoic acid (DHA) and arachidonic acid. In alewives experiencing the warm challenge, we observed significant increases in saturated fatty acids (due mainly to increased palmitic acid) and decreases in polyunsaturated fatty acids in polar lipids of muscle and liver tissue. Fish that died during the cold challenge had significantly higher levels of palmitic acid in muscle polar lipids compared to fish that survived; fish that died during the warm challenge displayed complex changes in fatty acid composition. Based on theoretical considerations, the changes in polar lipids we observed during thermal acclimation are likely to promote appropriate membrane fluidity under each thermal regime. The increased incorporation of highly unsaturated fatty acids during cold acclimation could have significant physiological and ecological implications. In particular, since highly unsaturated fatty acids are typically scarce in freshwater food webs, dietary deficiencies in these essential fatty acids may be a significant factor in winter mortality of freshwater alewives.



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Abbreviations
- ARA:
-
Arachidonic acid (C20:4n-6)
- DHA:
-
Docosahexaenoic acid (C22:6n-3)
- EPA:
-
Eicosapentaenoic acid (C20:5n-3)
- HUFA:
-
Highly unsaturated fatty acids
- MUFA:
-
Monounsaturated fatty acids
- n-3:
-
Omega-3 series fatty acids
- n-6:
-
Omega-6 series fatty acids
- PUFA:
-
Polyunsaturated fatty acids
- SAFA:
-
Saturated fatty acids
References
Adams SM (1999) Ecological role of lipids in the health and success of fish populations. In: Arts MT, Wainman BC (eds) Lipids in freshwater ecosystems. Springer, New York, pp 132–160
Arts MT, Kohler CC (2009) Health and condition in fish: the influence of lipids on membrane competency and immune response. In: Arts MT, Brett MT, Kainz MJ (eds) Lipids in aquatic ecosystems. Springer, New York, pp 237–255
Bell JG, Farndale BM, Dick JR, Sargent JR (1996) Modification of membrane fatty acid composition, eicosanoid production, and phospholipase a activity in Atlantic Salmon (Salmo salar) gill and kidney by dietary lipid. Lipids 31:1163–1171
Colby PJ (1973) Response of the alewives, Alosa pseudoharengus, to environmental change. In: Chavin W (ed) Responses of fish to environmental changes. CC Thomas, Springfield, pp 163–198
Cossins AR, Sinensky M (1986) Adaptation of membranes to temperature, pressure, and exogenous lipids. In: Shinitzky M (ed) Physiology of membrane fluidity. CRC Press, Boca Raton, pp 1–20
Craig SR, Neill WH, Gatlin DM III (1995) Effects of dietary lipid and environmental salinity on growth, body composition, and cold tolerance of juvenile red drum (Sciaenops ocellatus). Fish Physiol Biochem 14:49–61
Crockett EL, Londraville RL (2006) Temperature. In: Evans DH, Claiborne JB (eds) Physiology of fishes, 3rd edn. CRC Press, Boca Raton, pp 231–269
Dey I, Buda C, Wiik T, Halver JE, Farkas T (1993) Molecular and structural composition of phospholipid membranes in livers of marine and freshwater fish in relation to temperature. Proc Natl Acad Sci USA 90:7498–7502
Farkas T, Csengeri I (1976) Biosynthesis of fatty acids by the carp. Cyprinus carpio L., in relation to environmental temperature. Lipids 11:401–407
Farkas T, Fodor E, Kitajka K, Halver JE (2001) Response of fish membranes to environmental temperature. Aquac Res 32:645–655
Folch J, Lees M, Stanley GHS (1957) A simple method for the isolation and purification of total lipids from animal tissues. J Biol Chem 226:497–509
Fountoulaki E, Alexis MN, Nengas I, Venou B (2003) Effects of dietary arachidonic acid (20:4n–6), on growth, body composition, and tissue fatty acid profile of gilthead bream fingerlings (Sparus aurata L.). Aquaculture 225:309–323
Hazel JR (1979) The influence of thermal acclimation on membrane lipid composition of rainbow trout liver. Am J Physiol 236:R91–R101
Hazel JR (1993) Thermal biology. In: Evans DH (ed) The physiology of fishes. CRC Press, Boca Raton, pp 427–467
Hazel JR, Williams EE (1990) The role of alterations in membrane lipid composition in enabling physiological adaptation of organisms to their physical environment. Prog Lipid Res 29:167–227
Henderson RJ, Tocher DR (1987) The composition and biochemistry of freshwater fish. Prog Lipid Res 26:281–347
Higgs DA, Macdonald JS, Levings CD, Dosanjh BS (1995) Nutrition and feeding habits in relation to life history stage. In: Groot C, Margolis L, Clarke WC (eds) Physiological ecology of pacific salmon. UBC Press, Vancouver, pp 159–315
Juaneda P, Rocquelin G (1985) Rapid and convenient separation of phospholipids and non-phosphorus lipids from rat heart using silica cartridges. Lipids 30:40–41
Kelly AM, Kohler CC (1999) Cold tolerance and fatty acid composition of striped bass, white bass, and their hybrids. N Am J Aquac 61:278–285
Murry BA, Connerton MJ, O’Gorman R, Stewart DJ, Ringler NH (2010) Lakewide estimates of alewife biomass and Chinook salmon abundance and consumption in Lake Ontario, 1989–2005: implications for prey fish sustainability. Trans Am Fish Soc 139:223–240
O’Gorman R, Schneider CP (1986) Dynamics of alewives in Lake Ontario following a mass mortality. Trans Am Fish Soc 115:1–14
Olsen Y (1999) Lipids and essential fatty acids in aquatic food webs: what can freshwater ecologists learn from mariculture? In: Arts MT, Wainman BC (eds) Lipids in freshwater ecosystems. Springer, New York, pp 161–202
Person-Le Ruyet J, Skalli A, Dulau B, Le Bayon N, Le Delliou H, Robin JH (2004) Does dietary n-3 highly unsaturated fatty acids level influence the European sea bass (Dicentrachus labrax) capacity to adapt to a high temperature? Aquaculture 242:571–588
Roberts RJ (2002) Nutritional pathology. In: Halver JE, Hardy RW (eds) Fish nutrition, 3rd edn. Academic Press, New York, pp 453–504
Sargent JR, Tocher DR, Bell JG (2002) The lipids. In: Halver JE, Hardy RW (eds) Fish nutrition, 3rd edn. Academic Press, New York, pp 181–257
Sinensky M (1974) Homeoviscous adaptation—a homeostatic process that regulates viscosity of membrane lipids in Escherichia coli. Proc Natl Acad Sci USA 71:522–525
Skalli A, Robin JH, Le Bayon N, Le Delliou H, Person-Le Ruyet J (2006) Impact of essential fatty acid deficiency and temperature on tissues’ fatty acid composition of European sea bass (Dicentrachus labrax). Aquaculture 255:223–232
Snyder RJ, Hennessey TM (2003) Cold tolerance and homeoviscous adaptation in freshwater alewives (Alosa pseudoharengus). Fish Physiol Biochem 29:117–126
Stanley JG, Colby PJ (1971) Effects of temperature on electrolyte balance and osmoregulation in alewife (Alosa pseudoharengus) in fresh and sea water. Trans Am Fish Soc 100:624–638
Stillwell W, Wassall SR (2003) Docosahexaenoic acid: membrane properties of a unique fatty acid. Chem Phys Lipids 126:1–27
Tocher DR (2003) Metabolism and functions of lipids and fatty acids in teleost fish. Rev Fish Sci 11:107–184
Tocher DR, Sargent JR (1990) Effect of temperature on the incorporation into phospholipid classes and the metabolism via desaturation and elongation of (n-3) and (n-6) polyunsaturated fatty acids in fish cells in culture. Lipids 25:435–442
Wallaert C, Babin PJ (1994) Thermal adaptation affects the fatty acid composition of plasma phospholipids in trout. Lipids 29:373–376
Zabelinskii SA, Chebotareva MA, Brovtsyna NB, Krivchenko AI (1995) On adaptive specialization of the composition and conformational state of fatty acids in membrane lipids of fish gills. J Evol Biochem Physiol 31:18–22
Acknowledgments
This study was supported by a grant from the SUNY Research Foundation to RJS. We wish to thank two anonymous reviewers for their helpful comments on an earlier version of this manuscript.
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Snyder, R.J., Schregel, W.D. & Wei, Y. Effects of thermal acclimation on tissue fatty acid composition of freshwater alewives (Alosa pseudoharengus). Fish Physiol Biochem 38, 363–373 (2012). https://doi.org/10.1007/s10695-011-9513-0
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DOI: https://doi.org/10.1007/s10695-011-9513-0


