Abstract
Environmental stressors are known to play an important role in determining the distribution and abundance of intertidal species. Marine molluscs are particularly susceptible to changes in water temperature and salinity in inter-tidal zones. Ruditapes decussatus and Ruditapes philippinarum are marine intertidal clams, constantly exposed to salinity variations in their intertidal habitat. The goal of this study was to investigate whether these species would handle salinity increase as well as salinity decrease, given the general paucity of data on R. decussatus and R. philippinarum exposed to salinity changes. In this context, leucine aminopeptidase (LAP) activity changes following exposure to salinity change were investigated in clams from Tunisia and from Brittany. Samples of R. decussatus from Tunisia were maintained in salinity of l0%0, 20%0, 30%0, 45%0 and 55%0 for four weeks. Effects of salinity on LAP activity are also investigated in R. decussatus and in R. philippinarum from Brittany in salinities of 5%0, l0%0, 15%0, 17%0, 25%0, 30%0, 40%0, 45 %0 and 55%0. Three sets of experiments were conducted: Short (20 h), medium (96 h) and long-term (four weeks). During salinity trials, LAP activity of R. decussatus ranged from 0.07 ± 0.04 to 0.2 ± 0.05 μmol of paranitroanilide mg protein–1 min−1 and from 0.15 ± 0.015 to 0.56 ± 0.41 mg protein–1 min–1 for clams from Tunisia and from Brittany, respectively. In the R. philippinarum species, results showed the occurrence of higher activity levels, values ranged from 0.26 ± 0.11 to 1.04 ± 0.38 μmol of paranitroanilide mg protein–1 min–1. None of the salinity regimes gave significant differences in LAP ctivity in R. decussatus from Tunisia. Conclusion has also been deduced from experiments carried out on R. decussatus and R. philippinarum from Brittany. Results reported here suggest that LAP ctivity seems to be not affected by salinity changes in populations investigated. The study provided some useful insights into response of the bivalves R. decussatus and R. philippinarum to salinity stress and offered a number of candidate hypothesis as potential explanations for moderate changes in LAP activity.
Acknowledgements
The authors thank all people who contributed to this work. We gratefully acknowledge Mr M. Nejib Medhioub for his assistance during experiments.
References
Akberali H.B. 1978. Behaviour of Scrobicularia plana (da Costa) in water of various salinities. J. Exp. Mar. Biol. Ecol. 33 (3): 237-249. 10.1016/0022-0981(78)90011-4Search in Google Scholar
Akberali H.B. & Davenport J. 1981. The responses of the bivalve Scrobicularia plana (da Costa) to gradual salinity changes. J. Exp. Mar. Biol. Ecol. 53 (2-3): 251-259. 10.1016/0022-0981(81)90024-1Search in Google Scholar
Bayne B.L. 1973. The responses of three species of bivalve mollusc to declining oxygen tension at reduced salinity. Comp. Biochem. Physiol. Part A: Physiology 45 (3): 793-806. 10.1016/0300-9629(73)90082-0Search in Google Scholar
Bayne B.L., Moore N.M & Koehn R.K. 1981. Lysosomes and the response by Mytilus edulis L. to an increase in salinity. Mar. Biol. Lett. 2 (4): 193-204.Search in Google Scholar
Ben Aoun Z., Farhat F., Chouba L. & Hadj-Ali M.S. 2007. Investigation on possible chemical pollution of the Boughrara lagoon, south of Tunisia, by chemical wastes.Bull. Inst. Nat. Sci. Tech. Mer de Salammbô 34: 119-127.Search in Google Scholar
Benrejeb-Jenhani A. & Romdhane M.S. 2002. Impact des perturbations anthropiques sur l’évolution du phytoplancton de la lagune de Boughrara, (TUNISIE). Bull. Inst. Nat. Sci. Tech. Mer de Salammbô 29: 65-75.Search in Google Scholar
Bishop S.H. 1976. Nitrogen metabolism and excretion: regulation of intracellular and extracellular amino acid concentrations, pp. 414—431. In: Wiley M. (ed.), Estuarine Processes, Vol. I. Uses, Stresses and Adaptations to the Estuary, Conference Paper, Meeting of the Estuarine Research Conference, Galve-ston, Texas, 1975, 541 pp. ISBN: 1-48-324853-410.1016/B978-0-12-751801-5.50042-3Search in Google Scholar
Breber P. 1985. On-growing of the carpet shell clam (Ruditapes decussatus) two years' experience in Venice lagoon. Aquacul-ture 44(1): 51-56. 10.1016/0044-8486(85)90041-9Search in Google Scholar
Brent L.L. & Somero G.N. 2011.Transcriptomic responses to salinity stress in invasive and native blue mussels (genus Mytilus). Mol. Ecol. 20(3): 517-529. 10.1111/j. 1365-294X.2010.04973.x.Search in Google Scholar
Buroker N. 1983. Population genetics of the American oyster Crassostrea virginica along the Atlantic coast and the Gulf of Mexico. Mar. Biol. 75 (1): 99-112. 10.1007/BF00392635Search in Google Scholar
Caruso G. & Zaccone R. 2000. Estimates of leucine aminopepti-dase activity in different marine and brackish environments. J. Appl. Microbiol. 89(6): 951-959. 10.1046/j.1365-2672.2000.01198.xSearch in Google Scholar
Deaton L.E. 2001 Hyperosmotic volume regulation in the gills of the ribbed mussel, Geukensia demissa: rapid accumulation of betaine and alanine J. Exp. Mar. Biol. Ecol. 260:185-197. 10.1016/S0022-0981(01)00237-4Search in Google Scholar
Denis F. 1995. Génétique biochimique et moléculaire de la palourde japonaise Ruditapes philippinarum. Doctorat de l’Université de Bretagne Ouest, 145 pp.Search in Google Scholar
De Zwaan A. & Wijsman T.C.M. 1976.Anaerobic metabolism in Bivalvia (Mollusca). Characteristics of anaerobic metabolism. Comp. Biochem. Physiol. Part B: Comp. Biochem. 54 (3): 313-324. 10.1016/0305-0491(76)90247-9Search in Google Scholar
Food and Agriculture Organization of the United Nations (FAO) 2013a. FAO Yearbook of Fishery Statistics: Summary, Tables. Fish Crustaceans, Mollusks, etc. Capture Production by groups of species. ftp://ftp.fao.org/fi/stat/summary/a1d. pdf.page 26.Search in Google Scholar
Food and Agriculture Organization of the United Nations (FAO) 2013b. FAO Yearbook of Fishery Statistics: Summary Tables. World aquaculture production by species groups ftp://ftp.fao.org/fi/stat/summary/b-1.pdf.page 53.Search in Google Scholar
Food and Agriculture Organization of the United Nations (FAO) 2013c. FAO Yearbook of Fishery Statistics: Summary Tables. World aquaculture production of fish, crustaceans, molluscs, etc., by principal species. ftp://ftp.fao.org/fi/stat/summary/ a-6.pdf.page 46.Search in Google Scholar
Food and Agriculture Organization of the United Nations (FAO) 2013d. FAO Yearbook of Fishery Statistics: Summary Tables. World aquaculture production of fish, crustaceans, molluscs by principal producers. ftp://ftp.fao.org/fi/stat/summary/a-4.pdf.page 44.Search in Google Scholar
Gardner J.P. & Kathiravetpillai G. 1997. Biochemical genetic variation at a leucine aminopeptidase (Lap) locus in blue (Mytilus galloprovincialis) and greenshell (Perna canalicu-lus) mussel population along a salinity gradient. Mar. Biol. 128(4): 619-625. 10.1007/s002270050128Search in Google Scholar
Gardner J.P.A. & Palmer N.L. 1998. Size dependant, spatial and temporal genetic variation at a leucine aminopeptidase (LAP) locus among blue mussel (Mytilus galloprovincialis). Mar. Biol. 132:275-281.10.1007/s002270050393Search in Google Scholar
Garthwaite R. 1986. The genetics of California populations of Geukensia demissa (Dillwin) (Mollusca): further evidence on the selective importance of leucine aminopeptidase variation in salinity acclimation. Biol. J. Linn. Soc. 28(4): 342—358. 10.1111/j. 1095-8312.1986.tb01763.xSearch in Google Scholar
Garthwaite R. 1989. Leucine aminopeptidase variation and fitness parameters in the estuarine bivalve Geunkensia demissa. Mar. Biol. 103(2): 183-192. 10.1007/BF00543346Search in Google Scholar
Gharbi A., Zitari-Chatti R., Van Wormhoudt A., Dhraief M.N., Denis F., Said K. & Chatti N. 2011. Allozyme variation and population genetic structure in the carpet shell clam Ruditapes decussatus across the Siculo-Tunisian Strait. Biochem. Genet. 49 (11-12):788-805. 10.1007/s10528-011-9450-8Search in Google Scholar
Gilles R. 1987. Volume regulation in cells of euryhaline invertebrates, pp. 205-247. 10.1016/S0070-2161(08)60372-X. In: Gilles R., Kleinzeller A. & Bolis L. (eds), Current Topics in Membranes and Transport Vol. 30, Cell Volume Control: Fundamental and Comparative Aspects in Animal Cells. ISBN: 0-12-153330-1Search in Google Scholar
Hamida L. 2004 Reproduction de la palourde Ruditapes decussatus, en milieu naturel (Sud Tunisie) et en milieu contrôlé (écloserie expérimentale): relation avec le systeme immuni-taire. These de doctorat de l’Université de Bretagne Occi-dentale, 120 pp.Search in Google Scholar
Harzallah A. 2003. Transport de polluants dans la lagune de Biz-erte simulé par un modele de circulation de l’eau. Bull. Inst. Nat. Sci. Tech. Mer de Salambôo 30:121-133.Search in Google Scholar
Hawkins A. J.S. & Day A. J. 1999. Metabolic interrelations underlying the physiological and evolutionary advantages of genetic diversity. Amer. Zool. 39:401-411.10.1093/icb/39.2.401Search in Google Scholar
Hilbish T.J., Deaton L.E. & Koehn R.K. 1982. Effect of an allozyme polymorphism on regulation of cell volume. Nature 298:688-689.10.1038/298688a0Search in Google Scholar
Huang H., Tanaka H., Hammock B.D. & Morisseau C. 2009. Novel and highly sensitive fluorescent assay for leucine aminopeptidases. Anal. Biochem. 391(1): 11-16. 10. 1016/j.ab.2009.05.004Search in Google Scholar
Kim W.S., Huh H.T., Huh S.H. & Lee T.W.2001. Effects of salinity on endogenous rhythm of the Manila clam, Ruditapes philippinarum (Bivalvia : Veneridae). Mar. Biol. 138(1): 157-162. 10.1007/s002270000430Search in Google Scholar
Koehn R.K. 1978. Physiology and biochemistry of enzyme variation: the interface of ecology and population genetics, pp. 51—72. In: Brussard P. (ed.), Ecological Genetics: The Interface, Springer Verlag, N.Y., 248 pp. ISBN: 978-1-4612-6332-6. 10.1007/978-1-4612-6330-2Search in Google Scholar
Koehn R.K. & Hilbish J. 1987. The adaptive importance of genetic variation. Amer. Sci. 75 (2): 134-141.Search in Google Scholar
Koehn R.K. & Immermann F. 1981. Biochemical studies of aminopeptidase polymorphism in Mytilus edulis. I. Dependence of enzyme activity on season, tissue, and genotype. Biochem. Genet. 19(11): 1115-1142. 10.1007/BF0048 4569Search in Google Scholar
Koehn R.K., Milkman R. & Mitton J.B. 1976. Population genetics of marine pelecypods. IV Selection, migration and genetic differentiation in the blue mussel Mytilus edulis. Evolution 30(1): 2-32. 10.2307/2407669Search in Google Scholar
Koehn R.K. & Mitton J.B. 1972. Population genetics of marine pelecypods. I. Ecological heterogeneity and evolutionary strategy at an enzyme locus. Am. Nat. 106 (947):47—56. 10/1086/282750Search in Google Scholar
Koehn R.K., Newell R.I.E. & Irnmermann F. 1980. Maintenance of an aminopeptidase allele frequency cline by natural selection. Proc. Natl. Acad. Sci. USA 77(9): 5385-5389. 10.1073/pnas.77.9.5385Search in Google Scholar
Koehn R.K. & Siebenaller J.F. 1981. Biochemical studies of arninopeptidase polymorphism in Mytilus edulis. II. Dependence of reaction rate on physical factors and enzyme concentration. Biochem. Genet. 19(11): 1143-1161. 10.1007/BF00484570Search in Google Scholar
Lowry O., Rosebrough N.J., Farr A.L. & Randell R.S. 1951. Protein measurements with Folin phenol reagent. J. Biol. Chem. 193(1): 265-275. PMID: 1490771310.1016/S0021-9258(19)52451-6Search in Google Scholar
Mangum C. & Towle D. 1977. Physiological adaptation to unstable environments. Amer. Scientist 65 (1): 67—75. PMID: 842933Search in Google Scholar
Michinina S.R. & Rebordinos L. 1997. Genetic differentiation in marine and estuarine populations of Crassostrea angulata. Mar. Ecol. Prog. Ser. 154:167-174.10.3354/meps154167Search in Google Scholar
Moore M.N., Koehn R.K. & Bayne B.L. 1980. Leucine aminopeptidase (aminopeptidase-1), N-acetyl-beta-hexosaminidase and lysosomes in the mussel, Mytilus edulis L., in response to salinity changes. J. Exp. Zool. 214(3): 239-249. 10. 1002/jez. 1402140302Search in Google Scholar
Moraga D. 1984. Polymorphisme enzymatique de populations na-turelles et expérimentales de la palourde européennes (Ruditapes decussatus). These de doctorat de l’Université de Bretagne Occidentale, 114 pp.Search in Google Scholar
National Research Council of the National Academies 2010. Ecosystem Concepts for Sustainable Bivalve Mariculture. National Academies Press, Washington DC, 190 pp. 10.17226/12802. ISBN: 978-0-309-38486-5Search in Google Scholar
Nirchio M., Pérez J. & Cequea H. 1991. Allozyme variation of Lap loci in Crassostrea rhizophorae in relation to temperature and/or salinity. Scientia Marina 55(4): 563—587.Search in Google Scholar
Pierce S.K. 1971. Volume regulation and valve movements by marine mussels. Comp. Biochem. Physiol. Part A: Physiology 39 (1): 103-117. 10.1016/0300-9629(71)90350-1Search in Google Scholar
Rose R.L. 1984. Genetic variation in the oyster, Crassostrea vir-ginica (Gmelin), in relation to environmental variation. Estuaries 7 (2): 128-132. 10.2307/1351766Search in Google Scholar
Schoffeniels E. 1976. Adaptations with respect to salinity. Biochem. Soc. Symp. 41:179-204. PMID: 788717Search in Google Scholar
Shurova N.M. 2001. Influence of Salinity on the Structure and the State of Bivalve Mytilus galloprovincialis populations. Russ. J. Mar. Biol. 27(3): 151-155. 10.1023/A: 1016713401 707Search in Google Scholar
Skalamera J.P., Renaud F., Raymond M. & De Meefts T. 1999. No evidence for genetic differentiation of the mussel Mytilus galloprovincialis between lagoons and the seaside. Mar. Ecol. Prog. Ser. 178:251-258. 10.3354/meps178251Search in Google Scholar
Somero G.N. & Bowlus R.D. 1983. Osmolyte and metabolic end products of mollusks: the design of compatible solute systems, pp. 77-100. In: Hochachka P.W. (ed.), The Mollusca. Environmental Biochemistry and Physiology Vol. 2, Academic Press, New York, 362 pp. ISBN: 0-12-751402-3Search in Google Scholar
Tomanek L. & Helmuth B. 2002. Physiological Ecology of Rocky Intertidal Organisms: A Synergy of Concepts. Integ. Comp. Biol. 42(4): 771-775. 10.1093/icb/42.4.771.Search in Google Scholar PubMed
Veiga M.P.T., Gutierre S.M.M., Castellano G.C. & Freire C.A. 2015. Tolerance of high and low salinity in the intertidal gastropod Stramonita brasiliensis (Muricidae): behaviour and maintenance of tissue water content. J. Mollus. Stud. 82(1): 154-160. 10.1093/mollus/eyv044Search in Google Scholar
Venier P., De Pittŕ C., Bernante F., Varotto L., De Nardi B., Bovo G., Roch P., Novoa B., Figueras A., Pallavicini A. & Lanfranchi G. 2009. MytiBase: a knowledge base of mussel (M. galloprovincialis) transcribed sequences. BMC Genomics 10: 72. 10.1186/1471-2164-10-72.Search in Google Scholar PubMed PubMed Central
Yancey P.H., Clark M.E., Hand S.C., Bowlus R.D. & Somero G.N. 1982. Living with water stress: evolution of osmolyte systems. Science 217 (4566):1214-1222. 10.1126/sci-ence.7112124Search in Google Scholar
Young J.P.W., Koehn R.K. & Arnheim N. 1979. Biochemical characterization of “Lap”, a polymorphic aminopeptidase from the blue mussel Mytilus edulis. Biochem. Genet. 17(3): 305-323. 10.1007/BF00498971Search in Google Scholar PubMed
Zhao X., Yu H., Kong L. & Li Q. 2012. Transcriptomic Responses to Salinity Stress in the Pacific Oyster Crassostrea gigas. PLoS One 7 (9): e46244. 10.1371/journal.pone.0046244Search in Google Scholar PubMed PubMed Central
Van Horn J. & Tolley S.G. 2009. Acute response of the estuarine crab Eurypanopeus depressus to salinity and desiccation stress. J. Crustacean Biol. 29 (4): 556-561. 10.1651/08-3123.1Search in Google Scholar
© 2016 Institute of Botany, Slovak Academy of Sciences
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Articles in the same Issue
- Cellular and Molecular Biology
- A broad host range food-grade cloning vector for lactic acid bacteria
- Cellular and Molecular Biology
- Antimicrobial and morphogenic effects of emodin produced by A spergillus awamori WAIR120
- Cellular and Molecular Biology
- Herbal augmentation enhances malachite green bio degradation efficacy of Saccharomyces cerevisiae
- Cellular and Molecular Biology
- Efflux pump inhibitory activity of flavonoids isolated from Alpinia calcarata against methicillin-resistant Staphylococcus aureus
- Cellular and Molecular Biology
- Status of metal pollution in rivers flowing through urban settlements at Pune and its effect on resident microflora
- Cellular and Molecular Biology
- Use of N, N′-diacetylchitobiose in decreasing toxic effects of indoor air pollution by preventing oxidative DNA damage
- Botany
- The relationship between macrophyte assemblages and environmental variables in drainage and irrigation canals in Slovakia
- Botany
- Effects of ZnCl2 on ROS generation, plasma membrane properties, and changes in protein expression in grapevine root explants
- Botany
- Molecular characterization and alternative splicing of a MYB transcription factor gene in tumourous stem mustard and its response to abiotic stresses
- Zoology
- First report of Gussevia asota (Monogenea: Dactylogyridae), destructive parasite of A stronotus ocellatus (Perciformes: Cichlidae) in Europe
- Zoology
- Response of the carpet shell clam (Ruditapes decussatus) and the Manila clam (Ruditapes philippinarum) to salinity stress
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- Biodiversity of zooplankton (Rotifera and crustacea) in water soldier (Stratiotes aloides) habitats
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- Testing for longitudinal zonation of macroinvertebrate fauna along a small upland headwater stream in two seasons
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- Aphids (Hemiptera: Aphididae) of different plant communities in an urban environment
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- Cellular and Molecular Biology
- Ependymal tables designated for differentiation of the ependyma based on the adjacent periventricular structures