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Evidence that lipid can be digested by the dumpling squid Euprymna tasmanica, but is not stored in the digestive gland

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Abstract

The aims of this study were to assess quantitatively the enzymatic ability of squid to digest lipids and the ability of the digestive gland to accumulate lipid classes associated with storage. This was achieved through two manipulative experiments using the dumpling squid, Euprymna tasmanica. Firstly, we measured lipase activity and determined the presence and location of lipid vacuoles within the digestive gland; secondly we identified and quantified lipid classes in the digestive gland. Given the levels of lipase activity, we provided evidence for the first time that a squid species is capable of digesting lipid at levels comparable to invertebrates known to use dietary lipid. A poor relationship between feeding activity and lipase secretion suggests that enzyme production is continuous. The second experiment found no evidence that lipid was stored in the digestive gland; most of the lipid present in the gland was either structural or a dietary by-product. The implication of these findings is that for this species lipid is most probably being immediately digested and used for growth and reproduction rather than being stored in the digestive gland. We consider that the role and storage of lipid is likely to vary among different cephalopod species, but not predictably as function of their lifestyle. Therefore, potential locations for lipid storage, other than the digestive gland, need to be considered and using changes in the relative size of the digestive gland as a measure of condition needs to be interpreted with care.

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References

  • 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

    Article  CAS  Google Scholar 

  • Bligh EG, Dyer WJ (1959) A rapid method of total lipid extraction and purification. J Biochem Physiol 37:911–917

    CAS  Google Scholar 

  • Boucaud-Camou E, Boucher-Rodoni R (1983) Feeding and digestion in cephalopods. In: Boyle PR (eds) The mollusca. Academic, New York, pp 149–187

    Chapter  Google Scholar 

  • Boyle PR, Pierce GJ, Hastie LC (1995) Flexible reproductive strategies in the squid Loligo forbesi. Mar Biol 121:501–508

    Article  Google Scholar 

  • Bradford MM (1977) A rapid and sensitive method for the quantitation of microgram quantities of proteins utilising the principle of protein-dye binding. Anal Biochem 72:248–254

    Article  Google Scholar 

  • Castro BG, Garrido JL, Sotelo CG (1992) Changes in composition of digestive gland and mantle muscle of the cuttlefish Sepia officinalis during starvation. Mar Biol 114:11–20

    CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • Eyster LS, Van Camp LM (2003) Extracellular lipid droplets in Idiosepius notoides, the southern pygmy squid. Biol Bull 205:47–53

    Article  CAS  Google Scholar 

  • Fox-Smith T (2002) Protein-nitrogen flux in the southern dumpling squid Euprymna tasmanica. BSc (Hons). School of Aquaculture, Australia

  • Gjellesvik DR, Lombardo D, Walther BT (1992) Pancreatic bile salt dependent lipase from cod (Gadus morhua): purification and properties. Biochim Biophys Acta 1124:123–134

    Article  CAS  Google Scholar 

  • Hammer HS, Bishop C, Watts S (2000) Activities of three digestive enzymes during development in the crayfish Procambarus clarkii (Decapoda). J Crust Biol 20:614–620

    Article  Google Scholar 

  • Hayes JP, Shonkwiler JS (2001) Morphometric indicators of body condition: worthwhile or wish thinking? In: Speakman JR (ed) Body composition analysis of animals: a handbook of non-destructive methods. Cambridge University Press, Cambridge, pp 8–38

    Chapter  Google Scholar 

  • Jackson GD, Mladenov PV (1994) Terminal spawning in the deepwater squid Moroteuthis ingens (Cephalopoda: Onychoteuthidae). J Zool Lond 234:189–201

    Article  Google Scholar 

  • Jackson GD, Semmens JM, Phillips KL, Jackson CH (2004) Reproduction in the deepwater squid Moroteuthis ingens, what does it cost? Mar Biol 145:905–916

    Article  Google Scholar 

  • Johnston DJ (2003) Ontogenetic changes in digestive enzymology of the spiny lobster, Jasus edwardsii Hutton (Decapoda, Palinuridae). Mar Biol 143:1071–1082

    Article  Google Scholar 

  • Johnston DJ, Freeman J (2006) Dietary preference and digestive enzyme activities as indicators of trophic resource utilization by six species of crab. Biol Bull (in press)

  • Johnston DJ, Yellowlees D (1998) Relationship between dietary preferences and digestive enzyme complement of the slipper lobster Thenus orientalis (Decapoda: Scyllaridae). J Crust Biol 18:126–135

    Article  Google Scholar 

  • Johnston DJ, Hermans JM, Yellowlees D (1995) Isolation and characterisation of a trypsin from the slipper lobster Thenus orientalis. Lund Archiv Biochem Biophys 324:35–40

    Article  CAS  Google Scholar 

  • Johnston D, Moltschaniwskyj N, Wells J (2006) Development of the radula and digestive system of juvenile blacklip abalone (Haliotis rubra): potential factors responsible for variable weaning success on artificial diets. Aquaculture (in press)

  • Kunitz M (1947) Crysalline soybean trypsin inhibitor: II. General properties. J Gen Physiol 30:291–310

    Article  CAS  Google Scholar 

  • Lee PG, Blake NJ, Rodrick GE (1980) A quantitative analysis of digestive enzymes for the freshwater prawn Macrobrachium rosenbergii. Proc World Maricult Soc 11:392–402

    Article  CAS  Google Scholar 

  • Lee PG, Smith LL, Lawrence AL (1984) Digestive proteases of Penaeus vannamei Boone: relationship between enzyme activity, size and diet. Aquaculture 42:225–239

    Article  CAS  Google Scholar 

  • Lehninger AL (1987) Lipids and membranes. In: Lehninger AL (ed) Principles of biochemistry. Worth Publishers, New York, pp 303–329

    Google Scholar 

  • Moltschaniwskyj NA (1995) Changes in shape associated with growth in the loliginid squid Photololigo sp.: a morphometric approach. Can J Zool 73:1335–1343

    Article  Google Scholar 

  • Moltschaniwskyj NA, Semmens JM (2000) Limited use of stored energy reserves for reproduction by the tropical loliginid squid Photololigo sp. J Zool Lond 251:307–313

    Article  Google Scholar 

  • Mommensen TP, Hochachka PW (1981) Respiratory and enzymatic properties of squid heart mitochondria. Eur J Biochem 120:345–350

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Pecl G (2001) Flexible reproductive strategies in tropical and temperate Sepioteuthis squids. Mar Biol 138:93–101

    Article  Google Scholar 

  • Phillips KL, Nichols PD, Jackson GD (2003) Size-related dietary changes observed in the squid Moroteuthis ingens at the Falkland Islands: stomach contents and fatty-acid analyses. Polar Biol 26:474–485

    Google Scholar 

  • Rodriguez A, Le Vay L, Mourente G, Jones DA (1994) Biochemical composition and digestive enzyme activity in larvae and postlarvae of Penaeus japonicus during herbivorous and carnivorous feeding. Mar Biol 118:45–51

    Article  CAS  Google Scholar 

  • Rosa R, Costa PR, Pereira J, Nunes ML (2004a) Biochemical dynamics of spermatogenesis and oogenesis in Eledone cirrhosa and Eledone moschata (Cephalopoda: Octopoda). Comp Biochem Physiol B 139:299–310

    Article  CAS  Google Scholar 

  • Rosa R, Costa PR, Nunes ML (2004b) Effect of sexual maturation on the tissue biochemical composition of Octopus vulgaris and O. defilippi (Mollusca: Cephalopoda). Mar Biol 145:563–574

    Article  CAS  Google Scholar 

  • Rosa R, Pereira J, Nunes ML (2005a) Biochemical composition of cephalopods with different life strategies, with special reference to a giant squid, Architeuthis sp. Mar Biol 146:739–751

    Article  CAS  Google Scholar 

  • Rosa R, Costa PR, Bandarra N, Nunes ML (2005b) Changes in biochemical composition and energy reserves associated with sexual maturation in the ommastrephid squids Illex coindetii and Todaropsis eblanae. Biol Bull 208:100–113

    Article  CAS  Google Scholar 

  • Semmens JM (1998) An examination of the role of the digestive gland of two loliginid squids, with respect to lipid: storage or excretion? Proc R Soc Lond B 265:1685–1690

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • Semmens JM, Moltschaniwskyj NA, Alexander CG (1995) Effect of feeding on the structure and function of the digestive gland of the tropical sepioid Idiosepius pygmaeus. J Mar Biol Assoc UK 75:885–897

    Article  Google Scholar 

  • Swift K, Johnston DJ, Moltschaniwskyj N (2005) The digestive gland of the southern dumpling squid (Euprymna tasmanica): structure and function. J Exp Mar Biol Ecol 315:177–186

    Article  Google Scholar 

  • Tocher DR (2003) Metabolism and functions of lipids and fatty acids in teleost fish. Rev Fish Sci 11:107–184

    Article  CAS  Google Scholar 

  • Walter HE (1984) Proteinases: methods with hemoglobin, casein and azocoll as substrates. In: Bergmeyer HU (ed) Methods of enzymatic analysis. Verlag Chemie, Weinheim, pp 270–277

    Google Scholar 

  • Wigglesworth JM, Griffith DRW (1994) Carbohydrate digestion in Penaeus monodon. Mar Biol 120:571–578

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This project was funded by the University Internal Research Grant Scheme. We thank D. Sinn and T. Fox-Smith for assistance in collection of animals, and K. Swift for assistance in the experiments. Collection, handling and killing procedures cleared by University of Tasmania Animal Ethics Committee, Permit #A0006998.

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Correspondence to Natalie Moltschaniwskyj.

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Communicated by M.S. Johnson, Crawley

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Moltschaniwskyj, N., Johnston, D. Evidence that lipid can be digested by the dumpling squid Euprymna tasmanica, but is not stored in the digestive gland. Mar Biol 149, 565–572 (2006). https://doi.org/10.1007/s00227-006-0246-z

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  • DOI: https://doi.org/10.1007/s00227-006-0246-z

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