Temporal dynamics of amino and fatty acid composition in the razor clam Ensis siliqua (Mollusca: Bivalvia)

Springer Science and Business Media LLC - Tập 68 - Trang 465-482 - 2014
Miguel Baptista1, Tiago Repolho1, Ana Luísa Maulvault2, Vanessa M. Lopes1, Luis Narciso1, António Marques2, Narcisa Bandarra2, Rui Rosa1
1Laboratório Marítimo da Guia, Centro de Oceanografia, Faculdade de Ciências, Universidade de Lisboa, Cascais, Portugal
2Divisão de Aquacultura e Valorização, IPMA, Lisbon, Portugal

Tóm tắt

Few studies have been conducted on the temporal dynamics of both amino acid (AA) and fatty acid (FA) profiles in marine bivalves. We investigated the seasonal variation of these compounds in the pod razor clam Ensis siliqua in relation to food availability, salinity, water temperature and reproductive cycle. AA content varied between 46.94 and 54.67 % dry weight (DW), and the AAs found in greater quantity were glutamic acid, glycine and aspartic acid. FA content varied between 34.02 and 87.94 mg g−1 DW and the FAs found in greater quantity were 16:0 and 22:6n-3. Seasonal trends were observed for AAs and FAs. FAs increased with gametogenesis and decreased with spawning while AA content increased throughout spawning. The effect of increasing temperature and high food availability during the spawning season masked the loss of AAs resulting from gamete release. Still, a comparatively greater increase in the contents of glutamic acid and leucine with spawning indicate their possible involvement in a post-spawning gonad recovery mechanism. A post-spawning decrease in 14:0, 16:0, 16:1n-7, 18:1n-7 and 18:1n-9 is indicative of the importance of these FAs in bivalve eggs. An increase in 18:3n-3, 18:4n-3, 20:1n-9 and 20:2n-6 during gametogenesis suggests their involvement in oocyte maturation. The FA 22:4n-6, while increasing with spawning, appears to play a role in post-spawning gonad recovery. Salinity did not have an effect on the AA composition. None of the environmental parameters measured had an effect on FA composition.

Tài liệu tham khảo

Allen K (1961) Amino acids in the Mollusca. Am Zool 1:253–261 AOAC (2005) Official methods of analysis of the Association of Official Analytical Chemists International. Gaithersburg, MD, AOAC Baginski RM, Pierce SK (1977) The time course of intracellular free amino acid accumulation in tissues of Modiolus demissus during high salinity adaptations. Comp Biochem Physiol A 57:407–412 Baptista M, Lopes VM, Pimentel MS, Bandarra N, Marques A, Rosa R (2012) Temporal fatty acid dynamics of the octocoral Veretillum cynomorium. Comp Biochem Physiol B 161:178–187 Barber BJ, Blake NJ (1981) Energy storage and utilization in relation to gametogenesis in Argopecten irradians concentricus (say). J Exp Mar Biol Ecol 52:121–134 Barbour Wood SL, Krause J, Richard A, Kowalewski M, Wehmiller J, Simões MG (2006) Aspartic acid racemization dating of Holocene brachiopods and bivalves from the southern Brazilian shelf, South Atlantic. Quat Res 66:323–331 Bayne BL, Holland DL, Moore MN, Lowe DM, Widdows J (1978) Further studies on the effects of stress in the adult on the eggs of Mytilus edulis. J Mar Biol Assoc U K 58:825–841 Beninger PG, Stephan G (1985) Seasonal variations in the fatty acids of the triacylglycerols and phospholipids of two populations of adult clam (Tapes decussatus L. and T. Philippinarum) reared in a common habitat. Comp Biochem Physiol B 81:591–601 Besnard J-Y, Lubet P, Nouvelot A (1989) Seasonal variations of the fatty acid content of the neutral lipids and phospholipids in the female gonad of Pecten maximus L. Comp Biochem Physiol B 93:21–26 Beukema JJ, De Bruin W (1977) Seasonal changes in dry weight and chemical composition of the soft parts of the tellinid bivalve Macoma balthica in the Dutch Wadden Sea. Neth J Sea Res 11:42–55 Breen M, Howell T, Copland P (2011) A report on electrical fishing for razor clams (Ensis sp.) And its likely effects on the marine environment. Marine Scotland Science Report 03/11, Scotland Bressan M, Marin MG (1985) Seasonal variations in biochemical composition and condition index of cultured mussels (Mytilus galloprovincialis Lmk) in the Lagoon of Venice (North Adriatic). Aquaculture 48:13–21 Cohen Z, Von Shak A, Richmond A (1988) Effect of environmental conditions on fatty acid composition of the red algae Porphyridium cruentum: correlation to growth rate. J Phycol 24:328–332 da Costa F (2009) Optimización del cultivo en criadero de navaja (Ensis arcuatus Jeffreys, 1865), longueirón (E. siliqua Linneo, 1758) y longueirón vello (Solen marginatus Pennánt, 1777): composición bioquímica y de ácidos grasos en los desarrollos larvarios. Dissertation, University of Santiago de Compostela da Costa F, Martínez-Patiño D, Ojea J, Nóvoa S (2010) Larval rearing and spat production of the razor clam Ensis siliqua (Bivalvia: Pharidae). J Shellfish Res 29:347–351 Darriba S, San Juan F, Guerra A (2005a) Energy storage and utilization in relation to the reproductive cycle in the razor clam Ensis arcuatus (Jeffreys, 1865). ICES J Mar Sci 62:886–896 Darriba S, San Juan F, Guerra A (2005b) Gametogenic cycle of Ensis Siliqua (Linnaeus, 1758) in the Ría De Corcubión, Northwestern Spain. J Molluscan Stud 71:47–51 Davis JP, Wilson JG (1983) Seasonal changes in tissue weight and biochemical composition of the bivalve Nucula turgida in Dublin Bay with reference to gametogenesis. Neth J Sea Res 17:84–95 Dussart GBJ (1983) The amino acid composition of freshwater mollusc shells in relation to phylogeny and environment. J Molluscan Stud 49:213–223 Ellis LL, Burcham JM, Paynter KT, Bishop SH (1985) Amino acid metabolism in euryhaline bivalves: regulation of glycine accumulation in ribbed mussel gills. J Exp Zool 233:347–358 Fatima M (1996) Growth indices, nutritive value and chemical significance of the green mussel. Dissertation, University of Karachi Fernández-Tajes J, Gaspar M, Martínez-Patiño D, McDonough N, Roberts D, González-Tizón A, Martínez-Lage A, Méndez J (2007) Genetic variation of the razor clam Ensis siliqua (Jeffreys, 1875) along the European coast based on random amplified polymorphic DNA markers. Aquac Res 38:1205–1212 Fernández-Tajes J, Arias-Pérez A, Fernández-Moreno M, Méndez J (2012) Sharp decrease of genetic variation in two Spanish localities of razor clam Ensis siliqua: natural fluctuation or Prestige oil spill effects? Ecotoxicol 21:225–233 Gabbott PA (1983) Developmental and seasonal metabolic activities in marine molluscs. Mollusca, Vol 2. Academic Press, New York Gaspar MB, Monteiro CC (1998) Reproductive cycles of the razor clam Ensis siliqua and the clam Venus striatula off Vilamoura, Southern Portugal. J Mar Biol Assoc U K 78:1247–1258 Gaspar MB, Castro M, Monteiro CC (1999) Effect of tooth spacing and mesh size on the catch of the Portuguese clam and razor clam dredge. ICES J Mar Sci 56:103–110 Goodfriend GA, Flessa KW, Hare PE (1997) Variation in amino acid epimerization rates and amino acid composition among shell layers in the bivalve Chione from the Gulf of California. Geochim Cosmochim Acta 61:1487–1493 Hamdani A, Soltani-Mazouni N (2011) Changes in biochemical composition of the gonads of Donax trunculus L. (Mollusca, Bivalvia) from the Gulf of Annaba (Algeria) in relation to reproductive events and pollution. Jordan J Biol Sci 4:149–156 Hauton C, Atkinson RJA, Moore PG (2003) The impact of hydraulic blade dredging on a benthic megafaunal community in the Clyde Sea area, Scotland. J Sea Res 50:45–56 Hayward A, Gillooly J (2011) The cost of sex: quantifying energetic investment in gamete production by males and females. PLoS ONE 6(1):e16557 Helm MM, Holland DL, Stephenson RR (1973) The effect of supplementary algal feeding of a hatchery breeding stock of Ostrea Edulis L. on larval vigour. J Mar Biol Assoc U K 53:673–684 Henderson JW, Ricker RD, Bidlingmeyer BA, Woodward C (2000) Rapid, accurate, sensitive and reproducible analysis of amino acids. Agilent Publication Number 5980-1193ENAgilent Technologies, Palo Alto, CA Holland DL (1978) Lipid reserves and energy metabolism in the larvae of benthic marine invertebrates. In: Sargent DC, Malins JR (eds) Biochemical and biophysical perspectives in Marine Biology. Academic Press, London, pp 85–123 IMAR (2008–2011) Relatorio do Programa de Monitorizacao Ambiental do projecto da Marina e novo Cais dos “ferries” do Troiaresort. Lisboa, Portugal, p 303 Jarzebski A, Wenne R, Habermehl G (1986) Anatomical distribution of lipids and sterols in Macoma balthica (L.). Comp Biochem Physiol B 85:135–137 Joaquim S, Matias D, Lopes B, Arnold WS, Gaspar MB (2008) The reproductive cycle of white clam Spisula solida (L.) (Mollusca: Bivalvia): implications for aquaculture and wild stock management. Aquaculture 281:43–48 Kasschau MR, McCommas SA (1982) Glycine concentration as a biochemical indicator of sex and maturation in the sea anemone Bunodosoma cavernata. Comp Biochem Physiol A 72:595–597 Kluytmans JH, Boot JH, Oudejans RCHM, Zandee DI (1985) Fatty acid synthesis in relation to gametogenesis in the mussel Mytilus edulis L. Comp Biochem Physiol B 81:959–963 Knauer J, Southgate PC (1999) A review of the nutritional requirements of bivalves and the development of alternative and artificial diets for bivalve aquaculture. Rev Fish Sci 7:241–280 Kube S, Sokolowski A, Jansen JM, Schiedek D (2007) Seasonal variability of free amino acids in two marine bivalves, Macoma balthica and Mytilus spp., in relation to environmental and physiological factors. Comp Biochem Physiol A 147:1015–1027 Lebour MV (1938) Notes on the breeding of some lamellibranchs from Plymouth and their larvae. J Mar Biol Assoc UK 23:119–145 Lee RF, Heffernan PB (1991) Lipids and proteins in eggs of eastern oysters (Crassostrea virginica (Gmelin, 1791)) and northern quahogs (Mercenaria mercenaria (Linnaeus, 1758)). J Shellfish Res 10:203–206 Lewin J, C-h Chen, Hruby T (1979) Blooms of surf-zone diatoms along the coast of the Olympic Peninsula, Washington. X. Chemical composition of the surf diatom Chaetoceros armatum and its major herbivore, the Pacific razor clam Siliqua patula. Mar Biol 51:259–265 Linnaeus C (1758) Tomus I. Systema naturae per regna tria naturae, secundum classes, ordines, genera, species, cum characteribus, differentiis, synonymis, locis. Holmiae (Laurentii Salvii) Massapina C, Joaquim S, Matias D, Devauchelle N (1999) Oocyte and embryo quality in Crassostrea gigas (Portuguese strain) during a spawning period in Algarve, South Portugal. Aquat Living Resour 12:327–333 Matsushima O, Hayashi YS (1988) Uptake and accumulation of amino acids in the brackish-water bivalve Corbicula japonica Prime during high salinity acclimation. J Exp Mar Biol Ecol 123:201–210 Monteiro C, Gaspar MB (1993) Bivalves do litoral oceânico algarvio: breve notícia sobre a situação dos principais bancos (julho 1993). Relat Técn Cien, vol 65. INIP, Lisboa 65:19 O’Brien DM, Boggs CL, Fogel ML (2005) The amino acids used in reproduction by butterflies: a comparative study of dietary sources using compound-specific stable isotope analysis. Physiol Biochem Zool 78:819–827 Ojea J, Pazos AJ, Martínez D, Novoa S, Sánchez JL, Abad M (2004) Seasonal variation in weight and biochemical composition of the tissues of Ruditapes decussatus in relation to the gametogenic cycle. Aquac 238:451–468 Özden Ö, Erkan N (2011) A preliminary study of amino acid and mineral profiles of important and estimable 21 seafood species. Br Food J 113:457–469 Park K-I, Choi K-S (2004) Application of enzyme-linked immunosorbent assay for studying of reproduction in the Manila clam Ruditapes philippinarum (Mollusca: Bivalvia): I Quantifying eggs. Aquaculture 241:667–687 Park K-I, Choi J-W, Choi K-S (2003) Quantification of reproductive output of the butter clam, Saxidomus purpuratus (Sowerby, 1852) using enzyme-linked immunosorbent assay (ELISA). Ocean Polar Res 25:249–256 Pazos AJ, Ruíz C, García-Martin O, Abad M, Sánchez JL (1996) Seasonal variations of the lipid content and fatty acid composition of Crassostrea gigas cultured in El Grove, Galicia, N.W Spain. Comp Biochem Physiol B 114:171–179 Pieters H, Kluitmans JH, Zandee DI, Cadée GC (1980) Tissue composition and reproduction of Mytilus edulis in relation to food availability. Neth J Sea Res 14:349–361 Rosa R, Nunes ML (2003) Seasonal changes in nucleic acids, amino acids and protein content in juvenile Norway lobster (Nephrops norvegicus). Mar Biol 143:565–572 Rosa R, Nunes L, Reis CS (2002) Seasonal changes in the biochemical composition of Octopus vulgaris Cuvier, 1797, from three areas of the Portuguese coast. Bull Mar Sci 71:739–751 Sidwell VD, Loomis AL, Grodner RM (1979) Geographic and monthly variation in composition of oysters, Crassostrea virginica. Mar Fish Rev 41:13–17 Sokolowski A, Wolowicz M, Hummel H (2003) Free amino acids in the clam Macoma balthica L. (Bivalvia, Mollusca) from brackish waters of the southern Baltic Sea. Comp Biochem Physiol A 134:579–592 Tarnowska K, Wołowicz M, Chenuil A, Feral J-P (2009) Comparative studies on the morphometry and physiology of European populations of the lagoon specialist Cerastoderma glaucum (Bivalvia). Oceanol 51:437–458 Taylor AG, Savage C (2006) Fatty acid composition of New Zealand green-lipped mussels, Perna canaliculus: implications for harvesting for n-3 extracts. Aquac 261:430–439 Taylor AC, Venn TJ (1979) Seasonal variation in weight and biochemical composition of the tissues of the queen scallop, Chlamys opercularis, from the Clyde Sea Area. J Mar Biol Assoc U K 59:605–621 Tebble N (1966) British bivalve seashells: a handbook for identification. British Museum, Edinburgh Teshima S, Kanazawa A, Koshio S, Mukai H, Yamasaki S, Hirata H (1990) Fatty acid details for bivalves, Tapes philippinarum and Corbicula japonica, and marine types of algae, Nannochloropsis sp. and Chlorella sp. Mem Fac Fish Kagoshima Univ 39:137–149 Trytek RE, Allen WV (1980) Synthesis of essential amino acids by bacterial symbionts in the gills of the shipworm Bankia setacea (tryon). Comp Biochem Physiol A 67:419–427 Tuck ID, Bailey N, Harding M, Sangster G, Howell T, Graham N, Breen M (2000) The impact of water jet dredging for razor clams, Ensis spp., in a shallow sandy subtidal environment. J Sea Res 43:65–81 von Cosel R, Gofas S (2011) Ensis siliqua (Linnaeus, 1758). World register of marine species. http://www.marinespecies.org/aphia.php?p=taxdetails&id=140735. Accessed 13 August 2011 Wenne R, Polak L (1992) Lipid storage strategy in the clam Macoma (Bivalvia). Proceedings of the 12th Baltic Marine Biologists Symposium 179–183 Wenne R, Styczyńska-Jurewicz E (1987) Gross biochemical composition of the bivalve Macoma balthica from the Gulf of Gdańsk (Southern Baltic). Mar Biol 96:73–78 Wootton EC, Dyrynda EA, Ratcliffe NA (2003) Bivalve immunity: comparisons between the marine mussel (Mytilus edulis), the edible cockle (Cerastoderma edule) and the razor-shell (Ensis siliqua). Fish Shellfish Immunol 15:195–210 Wu G, Bazer F, Davis T, Kim S, Li P, Marc Rhoads J, Carey Satterfield M, Smith S, Spencer T, Yin Y (2008) Arginine metabolism and nutrition in growth, health and disease. Amino Acids 37:153–168 Yang H-S, Kang D-H, Park H-S, Choi K-S (2011) Seasonal changes in reproduction and biochemical composition of the cockle, Fulvia mutica Reeve (1884), in Cheonsu Bay off the west coast of Korea. J Shellfish Res 30:95–101 Zurburg W, De Zwaan A (1981) The role of amino acids in anaerobiosis and osmoregulation in bivalves. J Exp Zool 215:315–325