Abstract
The present study is a comprehensive comparison of the biochemical composition (protein, lipid, glycogen and cholesterol contents, and amino acid and fatty acid profiles) of 14 species of cephalopods with different life strategies (benthic, nektobenthic, benthopelagic and pelagic) in distinct habitats (neritic, demersal, oceanic and deep sea), with special emphasis placed on a male Architeuthis sp. The giant squid showed a significantly lower protein and total amino acid content in the gonad and digestive gland. The major essential amino acids were leucine, lysine and arginine. The major non-essential amino acids were glutamic acid, aspartic acid and proline. The benthopelagic cirrate octopus Opisthoteuthis sp. showed a lower content of these nitrogen compounds in the muscle. In respect to lipid and fatty acid contents, the giant squid showed the highest values in the gonad and digestive gland and the lowest in the muscle. Most of saturated fatty acid content was presented as 16:0; monounsaturated fatty acid content, as 18:1 and 20:1; and polyunsaturated fatty acid content, as 20:4n-6, 20:5n-3 and 22:6n-3. The highest cholesterol content in the gonad was detected in Opisthoteuthis sp. and Architeuthis sp.; in the digestive gland. in Todarodes sagittatus; and in the muscle, in Sepia elegans. The highest glycogen value in the gonad was detected in Octopus vulgaris; in the digestive gland and muscle, the highest values were attained in Opisthoteuthis sp. The relationships between life strategies and biochemical composition were investigated and principal component analysis (PCA) was performed. The different cephalopod life strategies could be well separated on the basis of the first two principal components. The nektobenthic and pelagic strategies were clearly separated from the benthic, suggesting that these groups of species are characterized by lower lipid content and higher protein content in the gonad. A rather similar life-strategy distinction was obtained for the digestive gland. The benthopelagic strategy was also well separated from benthic and pelagic strategies and from Architeuthis sp. In the muscle, the results indicated lower nitrogen and carbon compound contents in Architeuthis sp. and Opisthoteuthis sp. The environmental conditions that possibly explain the Architeuthis sp. stranding, the relationships between biochemical compositions and the life strategies of the different cephalopod species studied are discussed.
Similar content being viewed by others
References
Bidder AM (1970) Some problems of cephalopod locomotion. In: Proceedings of the Symposium Mollusca, vol 3.Marine Biological Association of India, Madras, pp 1029–1052
Bligh EG, Dyer WJ (1959) A rapid method of total lipid extraction and purification. Can J Biochem Physiol 37:911–917
Boucher-Rodoni R, Boucaud-Camou E, Mangold K (1987) Feeding and digestion. In: Boyle PR (ed) Cephalopod life cycles, vol 2: comparative reviews. Academic, London, pp 85–108
Brix O (1983) Giant squid may die when exposed to warm water currents. Nature 303:422–423
Childress JJ (1995) Are there physiological and biochemical adaptations of metabolism in deep-sea animals? Trends Ecol Evol 10:30–36
Childress JJ, Mickel TJ (1985) Metabolic rates of animals from the hydrothermal vents and other deep-sea habitats. Bull Biol Soc Wash 6:249–260
Childress JJ, Nygaard MH (1974) The chemical composition and relative buoyancy of midwater crustaceans as a function of depth off Southern California. Mar Biol 27:225–238
Childress JJ, Price MH, Favuzzi JA, Cowles DL (1990) Chemical composition of midwater fishes as a function of depth occurrence off the Hawaiian Islands: food availability as a selective factor. Mar Biol 105:235–246
Clarke A, Rodhouse PG, Gore DJ (1994) Biochemical composition in relation to the energetics of growth and sexual maturation in the ommastrephid squid Illex argentinus. Philos Trans R Soc Lond B 344:201–212
Clarke MR (1966) A review of the systematics and ecology of the oceanic squids. Adv Mar Biol 4:91–300
Clarke MR, Merret NR (1972) The significance of squid, whale and other remains from the stomachs of bottom-living deep-sea fish. J Mar Biol Assoc UK 52:599–603
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
Company JB, Sardà F (1998) Metabolic rates and energy content of deep-sea benthic decapod crustaceans in the western Mediterranean Sea. Deep-Sea Res I 45:1861–1880
Denton EJ, Gilpin-Brown JB (1973) Floatation mechanisms in modern and fossil cephalopods. Adv Mar Biol 11:197–268
Fiúza AFG (1983) Upwelling patterns off Portugal. In: Suess E, Thied J (eds) Coastal upwelling, its sediment record, part A: responses of the sedimentary regime to present coastal upwelling. Plenum, New York, pp 85–98
Gäde G (1980) Biological role of octopine formation in marine molluscs. Mar Biol Lett 1:121–135
Hayashi K, Kishimura H, Sakurai Y (1990) Level and composition of diacyl glyceryl ethers in different tissues and stomach contents of giant squid Moroteuthis robusta. Nippon Suisan Gakkaishi 56:1635–1639
Hochachka PW, Fields JHA (1982) Arginine, glutamate and proline as substrates for oxidation and for glycogenesis in cephalopod tissues. Pac Sci 36:325–335
Ikeda T (1988) Metabolism and chemical composition of crustaceans from the Antarctic mesopelagic zone. Deep-Sea Res 35:1991–2002
Kanazawa A (2001) Sterols in marine invertebrates. Fish Sci (Tokyo) 67:997–1007
Landman NH, Cochran JK, Cerrato R, Mak J, Roper CFE, Lu CC (2004) Habitat and age of the giant squid (Architeuthis sanctipauli) inferred from isotopic analyses. Mar Biol 144:685–691
Lee PG (1994) Nutrition of cephalopods: fueling the system. Mar Freshw Behav Physiol 25:35–51
Lepage G, Roy CC (1986) Direct transesterification of all classes of lipids in one-step reaction. J Lipid Res 27:114–119
Lipinski M (1979) Universal maturity scale for the commercially important squids. The results of maturity classification of the Illex illecebrosus population for the years 1973–77. Research document 79/II/38, serial no. 5364, International Commission for the Northwest Atlantic Fisheries (ICNAF), Dartmouth, Canada
Lordan C, Collins MA, Peralez-Raya C (1998) Observations on morphology, age and diet of three Architeuthis caught off the West coast of Ireland in 1995. J Mar Biol Assoc UK 78:903–917
Lowry OH, Rosenburgh NJ, Farr AL, Randall RJ (1951) Protein measurement with Folin phenol reagent. J Biol Chem 193:265–275
Mangold-Wirz K (1963) Biologie des céphalopods benthiques et nectoniques de la Mer Catalane. Vie Millieu 13[Suppl]:1–285
Moita MT (2001) Estrutura, variabilidade e dinâmica do fitoplâncton na costa de Portugal continental. PhD dissertation, University of Lisbon, Lisbon
Mommsen TP, Hochachka PW (1981) Respiratory and enzymatic properties of squid heart mitochondria. Eur J Biochem 120:345–350
Naemmi ED, Ahmad N, Al-sharrah TK, Behbahani M (1995) Rapid and simple method for determination of cholesterol in processed food. AOAC Int J 78:1522–1525
Navarro JC, Villanueva R (2000) Lipid and fatty acid composition of early stages of cephalopods: an approach to their lipid requirements. Aquaculture 183:161–177
Navarro JC, Villanueva R (2003) The fatty acid composition of Octopus vulgaris paralarvae reared with live and inert food: deviation from their natural fatty acid profile. Aquaculture 219:613–631
Nesis KN (2002) Life style strategies of recent cephalopods: a review. Bull Mar Sci 71:561–579
O’Dor RK (1988) The energetic limits on squid distributions. Malacologia 29:113–119
O’Dor RK (2002) Telemetered cephalopod energetics: swimming, soaring and blimping. Integr Comp Biol 42:1065–1070
O’Dor RK, Shadwick RE (1989) Squid, the olympic cephalopods. J Cephalopod Biol 1:33–54
O’Dor RK, Mangold K, Boucher-Rodoni R, Wells MJ, Wells J (1984) Nutrient absorption, storage and remobilisation in Octopus vulgaris. Mar Behav Physiol 11:239–258
Oehlenschläger J (2000) Cholesterol content in edible part of marine fatty pelagic fish species and other seafood. In: Georgakis SA (ed), Proceedings of 29th WEFTA meeting. Greek Society of Food Hygienists and Technologists, Thessaloniki, pp 107–115
Phillips KL, Jackson GD, Nichols PD (2001) Predation on myctophids by the squid Moroteuthis ingens around Macquarie and Heard Islands: stomach contents and fatty acid analyses. Mar Ecol Prog Ser 215:179–189
Phillips KL, Nichols PD, Jackson GD (2002) Lipid and fatty acid composition of the mantle and digestive gland of four southern ocean squid species: implications for food-web studies. Antarct Sci 14:212–220
Quetglas A, Alemany F, Carbonell A, Merella P, Sánchez P (1998) Biology and fishery of Octopus vulgaris Cuvier, 1797, caught by trawlers in Mallorca (Balearic Sea, western Mediterranean). Fish Res (Amst) 36:237–249
Robison BH (1989) Depth of occurrence and partial chemical composition of a giant squid, Architeuthis, off Southern California. Veliger 32:39–42
Robson GC (1933) On Architeuthis clarkei, a new species of giant squid, with observations on the genus. Proc Zool Soc Lond 3:681–697
Rosa R, Nunes ML (2003) Biochemical composition of deep-sea decapod crustaceans with two different benthic life strategies in the Portuguese south coast. Deep-Sea Res I 50:119–130
Rosa R, Nunes ML, Sousa Reis C (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
Seibel BA, Childress JJ (2000) Metabolism of benthic octopods (Cephalopoda) as a function of habitat depth and oxygen concentration. Deep-Sea Res I 47:1247–1260
Seibel BA, Carlini DB (2001) Metabolism of pelagic cephalopods as a function of habitat depth: a reanalysis using phylogenetically independent contrasts. Biol Bull (Woods Hole) 201:1–5
Seibel BA, Thuesen EV, Childress JJ, Gorodezky LA (1997) Decline in pelagic cephalopod metabolism with habitat depth reflects differences in locomotory efficiency. Biol Bull (Woods Hole) 192:262–278
Seibel BA, Thuesen EV, Childress JJ (2000) Light-limitation on predator–prey interactions: consequences for metabolism and locomotion of deep-sea cephalopods. Biol Bull (Woods Hole) 198:284–298
Semmens JM (2002) Changes in the digestive gland of the loliginid squid Sepioteuthis lessoniana (Lesson, 1830) associated with feeding. J Exp Mar Biol Ecol 274:19–39
Somero GN (1990) Life at low volume change: hydrostatic pressure as a selective factor in the aquatic environment. Am Zool 30:123–135
Somero GN (1992) Biochemical ecology of deep-sea animals. Experientia 48:537–543
Storey KB, Storey JM (1978) Energy metabolism in the mantle muscle of the squid, Loligo pealeii. J Comp Physiol 123:169–175
Storey KB, Storey JM (1983) Carbohydrate metabolism in cephalopod molluscs. In: Hochachka PW (ed) The Mollusca, vol 1. Metabolic biochemistry and molecular biomechanics. Academic, New York, pp 91–136
Torres JJ, Somero GN (1988) Metabolism, enzymatic activities and cold adaptation in Antarctic mesopelagic fishes. Mar Biol 98:169–180
Viles P, Silverman J (1949) Determination of starch and cellulose with anthrone. Anal Chem 21:950–953
Villanueva R (1992) Continuous spawning in the cirrate octopods Opisthoteuthis sp. and O. vossi: features of sexual maturation defining a reproductive strategy in cephalopods. Mar Biol 114:265–275
Vogel S (1994) Life in moving fluids: the physical biology of flow. Princeton University Press, Princeton, N.J., USA
Voight JR, Portner HO, O’Dor RK (1994) A review of ammonia-mediated buoyancy in squids (Cephalopoda: Teuthoidea). Mar Freshw Behav Physiol 25:193–203
Voss GL (1967) The biology and bathymetric distribution of deep-sea cephalopods. Stud Trop Oceanogr 5:511–535
Webber DM, Aitken JP, O’ Dor RK (2000) Costs of locomation and vertic dynamics of cephalopods and fish. Physiol Biochem Zool 73:651–662
Zar JH (1996) Biostatistical analysis. Prentice Hall, Upper Saddle River, N.J., USA
Acknowledgements
The Portuguese Foundation for Science and Technology (FCT) supported this study through a doctoral grant to the first author. We are grateful to the crews and scientists aboard the research vessels “Noruega” and “Capricórnio”. The technical assistance of P. Conceição was especially appreciated.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by S.A. Poulet, Roscoff
Rights and permissions
About this article
Cite this article
Rosa, R., Pereira, J. & Nunes, M.L. Biochemical composition of cephalopods with different life strategies, with special reference to a giant squid, Architeuthis sp.. Marine Biology 146, 739–751 (2005). https://doi.org/10.1007/s00227-004-1477-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00227-004-1477-5