Elsevier

Aquaculture

Volume 309, Issues 1–4, 22 November 2010, Pages 38-48
Aquaculture

A case report on the distended gut syndrome (DGS) in cultured larvae of Atlantic cod (Gadus morhua)

https://doi.org/10.1016/j.aquaculture.2010.09.006Get rights and content

Abstract

Production of juvenile Atlantic cod (Gadus morhua) in Norway has made progress during the past few years; however, high mortality in the larval stage is still one of the bottlenecks in commercial mass production. “Distended gut syndrome (DGS)” is often seen before and during phases of high mortality in the larval stage. The syndrome, which may affect various larval stages, is characterized by low activity and reduced appetite. The gut lumen becomes opaque, distended and filled with fluid. This study reports an outbreak of DGS in a commercial cod hatchery and employed histology and transcriptomics to characterize differences between DGS-affected larvae and well-performing larvae.

During commercial larval production in autumn 2008, samples were collected regularly from two of the rearing tanks, enabling us to follow a typical outbreak of DGS. During the outbreak of DGS, larvae were sampled from the water surface (floating larvae, with typical DGS symptoms) and from the water column (swimming larvae, apparently unaffected, as an internal control), and they were compared with well-performing larvae from spring 2008 (as an external control).

Histological sections showed extraordinarily many exfoliated epithelial cells in the gut of DGS larvae. There was also hydropic degeneration of hepatocytes in the liver of most of the larvae (from both DGS and internal control). Microarray analysis revealed several genes which were differentially regulated in DGS larvae. A literature search for genes with large differences in expression revealed that the genes which are related to redox balance and inflammation response were affected. The data indicate that oxidative stress is one of the underlying mechanisms of DGS and that the primary problems occur in the liver while secondary effects develop in the gut.

Introduction

Aquaculture of Atlantic cod (Gadus morhua) is still a young, immature, and cost-intensive industry. In the course of the past two years, there has been a dramatic setback in commercial production, due to a coincidence of the world-wide financial crisis and a simultaneous increase in the North-east Arctic cod population. Biologically, however, the industry has gradually succeeded in escalating its production of juveniles. One of the main remaining problems in fry production is high mortality during the larval stage especially at first-feeding and weaning, resulting in unpredictable production and economic results (Mikkelsen et al., 2004, Samuelsen and Bergh, 2004, Bergh et al., 2005).

Symptoms often seen prior to larval mortality include low larval activity combined with reduced appetite. As a result, the growth rates and condition factor of the larvae are reduced, and are followed by a peak in mortality one to two weeks later. Based on the visible symptoms where the gut lumen becomes opaque, distended and filled with fluid (Fig. 1), we have termed this condition “distended gut syndrome (DGS)”. Symptoms similar to DGS have been described in a range of other fish species cultured in intensive systems all over the world, including Japanese flounder (Paralichthys olivaceus) (Muroga et al., 1990, Kim et al., 2004, Mizuki et al., 2006), sea bass (Dicentrarchus labrax) and sea bream (Sparus aurata) (Grisez et al., 1997, Savas et al., 2005), summer flounder (Paralichthys dentatus) (Eddy and Jones, 2002, Gauger et al., 2006), turbot (Colistium nudipinnis) and brill (C. guntheri) (Diggles et al., 2000). Most research on larvae affected by DGS-like symptoms has focused on describing the microflora, but the underlying primary biological mechanisms involved are still not understood. In order to rectify the conditions which enable larvae to develop DGS and to maximize and realize the full growth and survival potential of cod fry production, further detailed biological understanding is essential.

The present study describes larvae from a batch of cod fry produced in autumn 2008 at a Norwegian commercial cod hatchery, where typical DGS characteristics were observed. Initially some larvae started to float on the surface with an empty and distended fluid-filled gut. The larvae were passive and appeared lethargic and moribund. The remaining larvae were still actively swimming and their gut was full of food. In contrast to classical acute Vibrio infection (e.g. Listonella anguillarum), the clinical patterns in this batch developed slowly and the daily mortality was low, culminating in one or more peaks.

Using these samples, the present study focused on histological and morphological changes of digestive organs in the larval cod with typical DGS symptoms compared with well-performing larvae. In order to describe the underlying biological mechanisms and processes affected by DGS, the larval material was examined by means of microarray analysis.

Section snippets

Larval rearing condition

During commercial larval production in 2008 at SagaFjord Sea Farm AS, a cod hatchery on the western coast of Norway, samples were collected regularly from two of the rearing tanks, enabling us to follow a typical outbreak of DGS. The larvae originated from eggs that had spawned naturally in mid-October 2008, from broodstock previously adapted and kept in the hatchery for two years. Rearing conditions were similar to those of spring 2008 (Kamisaka and Rønnestad, in press). Newly hatched larvae

Growth

Cod in aquaculture are fed rotifers during most of the larval stage, and there was a problem in autumn 2008 to produce sufficient numbers of rotifers of satisfactory quality for larval feeding. The rotifers were passive and seemed to have problems in taking enrichment (personal observation). No alternative feed was available at the larval stage. The cod larvae became passive and did not grow well, and some of them began to float on the surface from around 17 dph in almost all the rearing tanks.

Discussion

Many of the symptoms associated with DGS indicate that it may be related to infectious agents like viruses or bacteria and that the pathophysiological basis of DGS involves disturbed enteral water and electrolyte balance caused by toxins. Bacterial infections are still responsible for major problems in marine larval production (Hansen and Olafsen, 1999, Ringø and Birkbeck, 1999, Muroga, 2001, Olafsen, 2001, Toranzo et al., 2005, Bricknell et al., 2006, Samuelsen et al., 2006, Sandlund et al.,

Conclusions

DGS larvae with a distended and fluid-filled gut lacking solid content displayed exfoliated epithelial cells (probably apoptosis) in the gut lumen and numerous small holes between microvilli in the brush border membrane. However, the livers of DGS larvae and also younger or active larvae showed degeneration of hepatocytes (probably necrosis) even though they had full gut content. These results suggest that Atlantic cod larvae which develop DGS suffer the primary problem in the liver and become

Acknowledgements

We thank N. Ellingsen, T. Cieplinska and S. Mæhle for technical assistance in the lab, E. S. Erichsen for expert help with the SEM observations, and Professor G. K. Totland and Dr. H. Hellberg for their comments on the histological observations. Thanks are also due to Dr. S. Applebaum, Dr. C. Jolly, and S. Garg for technical assistance during sampling and molecular analysis. This study was supported by the Research Council of Norway project grant #187281.

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