Skip to main content
SpringerLink
Log in

Changes in composition of digestive gland and mantle muscle of the cuttlefish Sepia officinalis during starvation

  • Published:
Marine Biology Aims and scope Submit manuscript

Abstract

Changes in the biochemical composition of the digestive gland and in the proteins of the mantle muscle of Sepia officinalis L, collected in September 1989 from the Ria de Vigo (northwest Spain), were measured during periods of 2, 4, 10 and >53 d starvation. The digestive gland lost weight faster than the rest of the body throughout the whole period of starvation. In the digestive gland, carbohydrate and protein contents did not change during starvation; however, lipid levels decreased significantly after 53 d. Phospholipid content increased during longterm starvation. The content of free fatty acids rose after 16 d. Sterols, diacylglycerylethers, triacylglycerols and carotenoids contents did not change significantly. Of the total fatty acids, 18:0, 20:2n6, 20:4n6 and the monounsaturated moieties were preferentially consumed; others, such as 22:5n3, 22:6n3 and 16:4n1, were selectively retained. In the mantle muscle, water content increased and total protein content decreased. The myofibrillar proteins decreased after 53 d starvation, whereas the sarcoplasmic fraction did not change and the stromatic proteins increased. No changes were observed in the electrophoretic patterns of sarcoplasmic and myofibrillar proteins. The digestive gland of S. officinalis does not seem to be an important reserve organ during long-term starvation, but does seem to be important during shortterm starvation.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

Literature cited

  • Allen, W. V. (1976). Biochemical aspects of lipid storage and utilization in animals. Am. Zool. 16: 631–647

    Google Scholar 

  • Ballantyne, J. S., Hochachka, P. W., Mommser, T. P. (1981). Studies on the metabolism of the migratory squid, Loligo opalescens, enzymes of tissues and heart mitochondria. Mar. Biol. Lett. 2: 75–85

    Google Scholar 

  • Beardall, C. H., Johnston, I. A. (1983). Muscle atrophy during starvation in a marine teleost. Eur. J. Cell Biol. 29: 209–217

    Google Scholar 

  • Black, D., Love, R. M. (1986). The sequential mobilisation and restoration of energy reserves in tissues of Atlantic cod during starvation and refeeding. J. comp. Physiol. (Sect. B) 156: 469–479

    Google Scholar 

  • Blanchier, B., Boucaud-Camou, E. (1982). Contenu lipidique de la glande digestive de Sepia officinalis L. a maturité sexuelle. Malacologia 22: 691–696

    Google Scholar 

  • Blanchier, B., Boucaud-Camou, E. (1984). Lipids in the digestive gland and the gonad of immature and mature Sepia officinalis (Mollusca: Cephalopoda). Mar. Biol. 80: 39–43

    Google Scholar 

  • Boucaud-Camou, E., Boucher-Rodoni, R. (1983). Feeding and digestion in cephalopods. In: Salenddin, A. S. M., Wilbur, K. M. (eds.) The Mollusca. Vol. 5. Academic Press, London, p. 149–188

    Google Scholar 

  • Boucaud-Camou, E., Yim, M. (1980). Fine structure and function of the digestive cell of Sepia officinalis (Mollusca: Cephalopoda). J. Zool., Lond. 191: 89–105

    Google Scholar 

  • Boucher-Rodoni, R. (1982a). La glande digestive des céphalopodes, organe de synthése et de sécretion d'enzymes digestives. Cah. Biol. mar. 23: 299–318

    Google Scholar 

  • Boucher-Rodoni, R. (1982b). Etude cytologique de la glande digestive de deux céphalopodes Eledone cirrosa et Sepia officinalis. Cah. Biol. mar. 23: 393–413

    Google Scholar 

  • Boucher-Rodoni, R. (1989). Consommation d'oxygéne et excrétion ammonicale de Nautilus macrophalus. C. r. hebd. Séanc. Acad. Sci., Paris 309 (Sér. III): 173–179

    Google Scholar 

  • Boucher-Rodoni, R., Boucaud-Camou, E., Mangold, K. (1987). Feeding and digestion. In: Boyle, P. R. (ed.) Cephalopods life cycles. Vol. 2. Academic Press, London, p. 85–108

    Google Scholar 

  • Boucher-Rodoni, R., Mangold, K. (1988). Comparative aspects of ammonia excretion in cephalopods. Malacologia 29: 145–151

    Google Scholar 

  • Christie, W. W. (1989). Gas chromatography and lipids: a practical guide. The Oily Press, Ayr, Scotland

    Google Scholar 

  • Chu Fulin, E. (1984). Polyunsaturated fatty acids and neutral lipids in developing larvae of the oyster, Crassostrea virginica. Lipids 19: 815–820

    Google Scholar 

  • Clarke, A. (1977). Lipids class and fatty acids composition of Chorismus antarcticus (Pfetter) (Crustacea: Decapoda) at South Georgia. J. exp. mar. Biol. Ecol 28: 279–314

    Google Scholar 

  • Clarke, A., Rodhouse, P. G., Holmes, L. J., Pascoe, P. L. (1989). Growth rate and nucleic acid ratio in cultured cuttlefish Sepia officinalis (Mollusca: Cephalopoda). J. exp. mar. Biol. Ecol. 133: 229–240

    Google Scholar 

  • Cuzon, G., Cahu, J., Aldrin, J. F., Messager, J. L., Stéphan, G., Mével, M. (1980). Starvation effect on metabolism of Penaus japonicus. Proc. Wld Maricult. Soc. 11: 410–423

    Google Scholar 

  • Dave, G., Johansson-Sjöbeckm M.-L., Larsson Å., Lewander, K., Lidman, U. (1976). Metabolic and hematological effects of starvation in the European eel, Anguilla anguilla L. III Fatty acid composition. Comp. Biochem. Physiol. 53 (B): 509–515

    Google Scholar 

  • Davies, B. H. (1976). Carotenoids. In: Goodwin, T. W. (ed). Chemistry and biochemistry of plant pigments. Vol 2. Academic Press, London, p. 38–165

    Google Scholar 

  • Filliben, J. J. (1975). The probability plot correlation coefficient test for normality. Technometrics 17: 111–117

    Google Scholar 

  • Fisher, L. R., Kon, S. K., Thompson S. Y. (1956). Vitamin A and carotenoids in certain invertebrates. V. Mollusca: Cephalopoda. J. mar. biol. Ass. U.K. 35: 63–80

    Google Scholar 

  • Fraser, A. J. (1989). Triacylglycerol content as a condition index for fish, bivalve, and crustacean larvae. Can. J. Fish. aquat. Sciences 49: 1868–1873

    Google Scholar 

  • Gas, N. (1972). Structural alterations in the white muscle of carp (Cyprinus carpio L.) during prolonged starvation. C. r. hebd. Séanc. Acad. Sci., Paris 275 (Sér. D): 1403–1406

    Google Scholar 

  • Gehron, M. J., White, D. C. (1982). Quantitative determination of the nutritional status of detrital microbiota and the grazing fauna by triglyceride glycerol analysis. J. exp. mar. Biol. Ecol. 64: 145–158

    Google Scholar 

  • Hames, D. B. (1981). An introduction to polyacrylamide gel electrophoresis. In: Hames, B. D., Rickwod, D. (eds.) Gel electrophoresis of proteins. A practical approach. IRL Press, Oxford, Washington, p. 1–86

    Google Scholar 

  • Hammond, E. W. (1986). Packed column gas-chromatography. In: Hamilton, R. J., Rossell, J. B. (eds.) Analysis of oils and fats. Elsevier Applied Science, Barking, p. 113–136

    Google Scholar 

  • Hashimoto, K., Watabe, S., Kono, M., Shiro, K. (1979). Muscle protein composition of sardine and mackerel. Bull. Jap. Soc. scient. Fish. 45: 1435–1441

    Google Scholar 

  • Hayashi, K., Takagi, T. (1977). Lipid metabolism in fish. II. Changes of lipids and fatty acids in the liver of puffer, Fugu vermiculare porphyreum, during starvation. Bull. Fac. Fish. Hokkaido Univ. 28: 193–201

    Google Scholar 

  • Herbes, S. E., Allen, C. P. (1983). Lipid quantification of freshwater invertebrates: method modification for microquantitation. Can. J. Fish. aquat. Sciences 40: 1315–1317

    Google Scholar 

  • Huang, T. C., Chen, C. P., Wefler, V., Raftery, A. (1961). A stable reagent for the Libermann-Buchard reaction. Application to rapid serum cholesterol determination. Analyt. Chem. 33: 1405–1407

    Google Scholar 

  • Jezierska, B., Hazel, J. R., Gerking, S. D. (1982). Lipid mobilization during starvation in the rainbow trout, Salmo gairdneri Richardson, with attention to fatty acids. J. Fish Biol. 21: 681–692

    Google Scholar 

  • Johansen, K., Brix, O., Kornerup, S., Lykkeboe, G. (1982). Factors affecting O2-uptake in the cuttlefish Sepia officinalis. J. mar biol. Ass. U.K. 62: 187–191

    Google Scholar 

  • Johnston, I. A. (1981). Quantitative analysis of muscle breakdown during starvation in the marine flatfish Pleuronectes platessa. Cell Tissue Res. 214: 369–386

    Google Scholar 

  • Johnston, I. A., Goldspink, G. (1973). Some effects of prolonged starvation on the metabolism of the red and white myotomal muscles of the plaice Pleuronectes platessa. Mar. Biol. 19: 348–353

    Google Scholar 

  • Joseph, J. (1982). Lipid composition of marine and estuarine invertebrates. Part II: Mollusca. Prog. Lipid Res. 21: 109–153

    Google Scholar 

  • Kanazawa, A., Teshima, S., Kazuo, O. (1979). Relationship between essential fatty acid requirements of aquatic animals and the capacity for bioconversion of linolenic acid to highly unsaturated fatty acids. Comp. Biochem. Physiol. 63 B: 295–298

    Google Scholar 

  • Kreuzer, R. (1984). Cephalopods: handling, processing and products. F.A.O. Fish. tech. Pap. 254: 1–108

    Google Scholar 

  • Laemmli, U. K. (1970). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature, Lond. 227: 680–685

    Google Scholar 

  • Love, R. M. (1970). The chemical biology of fishes. Vol 1. Academic Press, New York and London

    Google Scholar 

  • Love, R. M. (1980). The chemical biology of fishes. Vol 2. Academic Press, New York and London

    Google Scholar 

  • Lowry, O. H., Rosebrough, N. J., Farr, A. L., Randall, R. J. (1951). Protein measurement with the Folin phenol reagent. J. biol. Chem. 193: 265–275

    Google Scholar 

  • Lowry, R. R., Tinsley, I. J. (1976). Rapid colorimetric determination of free fatty acids. J. Am. Oil Chem. Soc. 53: 470–472

    Google Scholar 

  • Mangold, K. (1983). Food, feeding and growth in cephalopods. Mem. natn. Mus. Vict. 44: 81–83

    Google Scholar 

  • Mangold, K., Bidder, A. M. (1989). L'appareil digestif et la digestion. In: Traité de zoologie. Anatomie systématique, biologie: céphalopodes. Tomo V. Fascicule 4. Masson, Paris, p. 321–373

    Google Scholar 

  • Mather, J. A. (1986). A female-dominated feeding hierarchy in juvenile Sepia officinalis in the laboratory. Mar. Behav. Physiol. 12: 223–244

    Google Scholar 

  • Millward, D. J. (1970). Protein turnover in skeletal muscle. II. The effect of starvation and a protein free diet on the synthesis and catabolism of skeletal muscle proteins in comparison to liver. Clin. Sci. 39: 591–603

    Google Scholar 

  • Mommsen, T. P., Hochachka, P. W. (1981). Respiratory and enzymatic properties of squid heart mitochondria. Eur. J. Biochem. 120: 345–350

    Google Scholar 

  • Nakamura, K., Handa, S. (1984). Coomassie brilliant blue staining of lipids on thin-layer plates. Analyt. Biochem. 142: 406–410

    Google Scholar 

  • O'Dor, R. K., Mangold, K., Boucher-Rodoni, R., Wells, M. J., Wells, J. (1984). Nutrient absorption, storage and remobilization in Octopus vulgaris. Mar. behav. Physiol. 11: 239–258

    Google Scholar 

  • O'Dor, R. K., Weber, D. M. (1986). The constraints on cephalopods: why squid aren't fish. Can. J. Zool. 64: 1591–1605

    Google Scholar 

  • O'Dor, R. K., Wells, M. J. (1987). Energy and nutrient flow. In: Boyle, P. R. (ed.) Cephalopod life cycles. Vol 2. Academic Press, London, p. 109–133

    Google Scholar 

  • Packard, A. (1972). Cephalopods and fish: limits of convergence. Biol. Rev. 47: 241–307

    Google Scholar 

  • Pollero, R. J., Iribarne, O. O. (1988). Biochemical changes during the reproductive cycle of the small Patagonian octopus, Octopus tehuelchus, D'Orb. Comp. Biochem. Physiol. 90 (B): 317–320

    Google Scholar 

  • Raheja, R. K., Knaur, C., Singh, A., Bathia, I. S. (1973). New colorimetric method for the quantitative estimation of phospholipids without acid digestion. J. Lipid Res. 14: 695–697

    Google Scholar 

  • Reinard, T., Jacobsen, H.-J. (1989). An inexpensive small volume equilibrium dialysis system for protein-ligand binding assays. Analyt. Biochem. 176: 157–160

    Google Scholar 

  • Sargent, J. R. (1975). The structure, metabolism and function of lipids in marine organisms. In: Malins, D. C., Sargent, J. R. (eds.) Biochemical and biophysical perspectives in marine biology. Vol 2. Academic Press, New York and London, p. 149–212

    Google Scholar 

  • Sargent, J. R., Whittle, K. J. (1981). Lipids and hydrocarbons in the marine food web. In: Longhurst, A. R. (ed.) Analysis of marine ecosystems. Academic Press, London, p. 491–533

    Google Scholar 

  • Satho, S., Takeuchi, T., Watanabe, T. (1984). Effects of starvation and environmental temperature on proximate and fatty acid compositions of Tilapia nilotica. Bull. Jap. Soc. scient. Fish. 50: 79–84

    Google Scholar 

  • Segawa, S., Hanlon, R. T. (1988). Oxygen consumption and ammonia excretion rates in Octopus maya, Loligo forbesi and Lolliguncula brevis (Mollusca: Cephalopoda). Mar. Behav. Physiol. 13: 389–400

    Google Scholar 

  • Siegel, S., Castellan, N. J. (1988). Nonparametric statistics for the behavioral sciences. McGraw-Hill Book Co., New York

    Google Scholar 

  • Sikorski, Z. E., Kolodzieiska, I. (1986). The composition and properties of squid meat. Fd Chem. 20: 213–224

    Google Scholar 

  • Sokal, R. R., Rohlf, F. J. (1981). Biometry. The principles and practice of statistics in biological research. 2nd ed. W.H. Freeman & Co., New York.

    Google Scholar 

  • Steel, G. D., Torrie, J. H. (1985). Bioestadística. McGraw-Hill, Bogotá

    Google Scholar 

  • Storey, K. B., Storey, J. B. (1983). Carbohydrate metabolism in cephalopod molluscs. In: Hochachka, P. W. (ed) The Mollusca. Vol. 1. Academic Press, New York and London, p. 91–136

    Google Scholar 

  • Strancari, M. T., Lozano, F. (1987) Determinación de los contenidos en humedad, grasos y cenizas, en especies de sepiáridos (Cephalopoda: Sepioidea) del Banco Sahariano. Alimentaria 182: 57–62

    Google Scholar 

  • Strickland, J. D. H., Parsons, T. R. (1968). A practical handbook of seawater analysis. Bull. Fish. Res. Bd Can. 167: 1–311

    Google Scholar 

  • Suryanarayanan, H., Alexander, K. M. (1971). Fuel reserves of molluscan muscle. Comp. Biochem. Physiol. 40 (A):55–60

    Google Scholar 

  • Tait, R. W. (1986) Aspects physiologiques de la sénescence post-reproductive chez Octopus vulgaris. Thése de Doctorat. L'Université Paris VI

  • Takahashi, T. S. (1960). Studies on the utilization of cuttlefish, Ommastrephes sloani pacificus. III. The seasonal variations in the gravimetric constitution and the chemical composition of the various parts of the body. Bull. Jap. Soc. scient. Fish. 26: 95–98

    Google Scholar 

  • Takeuchi, T., Watanabe, T. (1982). The effects of starvation and environmental temperature on proximate and fatty acid composition of carp and rainbow trout. Bull. Jap. Soc. scient. Fish. 48: 1307–1316

    Google Scholar 

  • Wells, M. (1990). The dilemma of the jet set. New Scient. 125: 44–49

    Google Scholar 

  • Woo, N., Murat, Y. S. (1981). Studies on the biology of the red sea bream Chrysophrys major. III. Metabolic response to starvation in different salinities. Mar. Biol. 61: 255–260

    Google Scholar 

Download references

Author information

Author notes

  1. B. G. Castro

    Present address: Marine Biomedical Institute, University of Texas Medical Branch at Galveston, 77550-2772, Galveston, Texas, USA

Authors and Affiliations

  1. Instituto de Investigaciones Marinas de Vigo (CSIC), C/Eduardo Cabello 6, E-36208, Vigo (Pontevedra), Spain

    B. G. Castro, J. L. Garrido & C. G. Sotelo

Authors
  1. B. G. Castro
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. J. L. Garrido
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. C. G. Sotelo
    View author publications

    You can also search for this author in PubMed Google Scholar

Additional information

Communicated by J. M. Pérès, Marseille

Rights and permissions

Reprints and permissions

About this article

Cite this article

Castro, B.G., Garrido, J.L. & Sotelo, C.G. Changes in composition of digestive gland and mantle muscle of the cuttlefish Sepia officinalis during starvation. Marine Biology 114, 11–20 (1992). https://doi.org/10.1007/BF00350851

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00350851

Keywords

Search

Navigation