Digestive enzyme ratios are good indicators of hatchling yolk reserve and digestive gland maturation in early life stages of cuttlefish Sepia officinalis L.: application of these new tools in ecology and aquaculture

Abstract

In Sepia officinalis (Linnaeus, 1758), the digestive gland matures during the first month post-hatching, while a shift from intracellular acid to extracellular alkaline digestion occurs. The purpose of this study was to investigate the possibility of using enzymatic ratios for the description of digestive system maturation in early life stages of S. officinalis. Second, it is intended to apply these new tools as eco-physiological indicators for understanding the impact of cuttlefish eggs’ life history from different spawning sites of the English Channel on digestive performance of juveniles. An experimental rearing was performed over 35 days after hatching (DAH) on juveniles from wild collected eggs in 2010 and 2011. Four digestive enzyme activities and their ratios [i.e., trypsin, cathepsin, acid (ACP), and alkaline (ALP) phosphatase, ALP/ACP, and trypsin/cathepsin] were studied along with histological features (e.g., internal yolk surface and digestive gland development). The two enzyme ratios were good indicators of digestive system maturation allowing the study of the digestive gland’s development. They were highly correlated to juveniles’ weight increase and histological features of the gland in early DAH. These ratios described more accurately the shift occurring between the intracellular acid and the extracellular alkaline modes of digestion in S. officinalis and were more specific than separated enzyme activities. Their application as eco-physiological tools revealed that enzyme ratios reflected yolk content and digestive gland development in new hatching juveniles. Finally, ALP/ACP ratio was shown to be a powerful tool to describe growth performance of S. officinalis which is useful for aquaculture optimization.

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Acknowledgements

This work was supported by European funding as part of the CRESH (Cephalopods Recruitment from English Channel Spawning Habitats) INTERREG IV-A project and by the regional funding of Basse-Normandie. This work was achieved in the CREC marine research station (for the rearing) and in BOREA laboratory (for biochemical and histological analysis). We would like to thank Mrs. Béatrice Adeline for her precious help in achieving the histological sections and Mrs. Laura Varin for her great job, during her internship, in processing histological slides for digestive vesicles counting, which is a very long and time-consuming work. We are grateful to Mrs. Céline Quint from the international language service of the University of Caen “Le Carré international” for professional English editing of the manuscript. Finally, we are thankful to reviewers for their comments and suggestions which highly improved the manuscript.

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Safi, G., Martinez, A.S., Le Pabic, C. et al. Digestive enzyme ratios are good indicators of hatchling yolk reserve and digestive gland maturation in early life stages of cuttlefish Sepia officinalis L.: application of these new tools in ecology and aquaculture. J Comp Physiol B 188, 57–76 (2018). https://doi.org/10.1007/s00360-017-1115-4

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Keywords

  • Sepia officinalis
  • Early life stages
  • Enzyme ratio
  • Indicator
  • Digestive gland
  • Cathepsin
  • Phosphatase
  • Trypsin