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Maturation of the digestive system of Downs herring larvae (Clupea harengus, Linnaeus, 1758): identification of critical periods through ontogeny

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Abstract

Digestive system functionality is a key process linked to larval recruitment and survival. However, little is known about organ development and enzyme maturation of the digestive system of North Sea Atlantic herring (Clupea harengus). In this study, herring larvae were reared at 13 °C from hatching to 69 day post hatch, covering four developmental stages: (1) yolk sac (8–9 mm), (2) pre-flexion (9–14 mm), (3) flexion (12–18 mm) and (4) post-flexion stages (15–30 mm). Combined histological (semi-quantitative scoring) and enzyme analyses (pancreatic and intestinal) showed that developmental stages are strongly linked to physiological changes. The larvae lack a functional stomach and use the intestine as the primary site of digestion which is mainly supported by pancreatic enzyme activity. The intestine acquired adult enzymatic digestive features with a functional brush border at the end of the flexion stage and pyloric ceca started to develop during the post-flexion stage. The transition from pre-flexion to flexion stage and the end of the post-flexion stage are energetically taxing periods as indicated by a reduced number and size of liver vacuoles. Based on these findings, we consider these moments as critical periods, where herring larvae could be dramatically affected by suboptimal feeding conditions in the field. This implies that pre-flexion stage larvae with low or no liver reserves may not be able to proceed to the next developmental stage. Hence, the level of energy storage in first-feeding larvae needs to be examined for its use as a field indicator of survival and development.

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Acknowledgment

Funding for this study was provided by the AWI–MARUM–IFREMER (AMI) Partnership Programme awarded to the “CoCktAIL” (Climate ChAnge effects on fIsh Larvae) project (2018–2022). The PhD Grant for L. Joly is supported by IFREMER and AWI. Additional support was provided by the French government and the region Hauts-de-France in the framework of the project CPER MARCO 2014–2020. The authors thank Prof. Philippe Koubbi for his valuable guidance regarding histological analysis as well as Clara Ortu, Marie-Anais Leprêtre, and IFREMER technicians and researchers (Margaux Denamiel, Fabien Lebon, Coline Lazard, Stéphane Karasiewicz, David Mazurais, Arianna Servili) for their valuable help in the laboratory for the fertilization procedure. Logistical aid was also provided by the Nausicaä Centre National de la Mer and in particular by Stéphane Hénard. Finally, this work would have not been possible without the implication of local fishermen (CME, From Nord) in Boulogne sur Mer willing to support science and research on highly important local fish species.

Funding

Funding for this study was provided by the AWI–MARUM–IFREMER (AMI) Partnership Program awarded to the “CoCktAIL” (Climate ChAnge effects on fIsh Larvae) project (2018–2022). The PhD Grant for L. Joly is supported by IFREMER and AWI. Additional support was provided by the French government and the region Hauts-de-France in the framework of the project CPER MARCO 2014–2020. CLM was supported by the Bundesministerium für Bildung und Forschung (BMBF grant no. 01LN1702A). MB was supported by the German Science Foundation (DFG), with the Priority Programme Dynatrait, and the BMBF FONA-Project Bioweb.

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Authors and Affiliations

  1. English Channel and North Sea Research Unit, Ifremer, Boulogne-sur-Mer, France

    Léa J. Joly, Christophe Loots, Valérie Lefebvre & Carolina Giraldo

  2. Alfred-Wegener-Institut Helmholtz-Zentrum für Polar-und Meeresforschung Biologische Anstalt Helgoland, Helgoland, Germany

    Léa J. Joly, Cédric L. Meunier & Maarten Boersma

  3. FB2, University of Bremen, Bremen, Germany

    Maarten Boersma

  4. Ifremer, Univ Brest, CNRS, IRD, LEMAR, 29280, Plouzané, France

    Sophie Collet & José-Luis Zambonino-Infante

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  1. Léa J. Joly
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  3. Cédric L. Meunier
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  4. Maarten Boersma
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Contributions

Conceptualization: LJJ, CG, JLZ, CLM. Methodology: LJJ, JLZ, CL, SC, VL. Formal analysis and investigation: LJJ, JLZI, CLM, CL, CG. Writing–original draft preparation: LJJ.

Writing–review and editing: CG, CLM, JLZI, CL, MB. Funding acquisition: CG, CLM, MB. Resources: CG, CL, JLZI. Supervision: CG, CLM, JLZI, CL.

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Correspondence to Carolina Giraldo.

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The authors have no conflicts of interest to declare that are relevant to the content of this article.

Ethics approval

Fish experiments were conducted at the Ifremer-Centre de Bretagne facilities (agreement number: B29-212–05) following French national regulations and authorized by the Regional Ethics Committee (authorization number 16513–2018082709221792).

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Joly, L.J., Loots, C., Meunier, C.L. et al. Maturation of the digestive system of Downs herring larvae (Clupea harengus, Linnaeus, 1758): identification of critical periods through ontogeny. Mar Biol 168, 82 (2021). https://doi.org/10.1007/s00227-021-03894-z

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