Stress Signalling by Gills and Skin of Aquatic finfishes in Aquaculture

By: Soibam Khogen Singh *

Introduction

The stress response is essentially similar in all vertebrates and involves physiological and behavioural responses directed at restoring the disturbance of, or protecting, the physiological equilibrium of an organism. The factors threatening or disturbing this equilibrium are called stressors, and the condition of the animal is defined as stress.

The stress response is essentially adaptive and promoting survival under demanding conditions, in particular when stressor exposure is avoidable or limited in duration. Under chronic, unavoidable stressor exposure, the stress response can become maladaptive.

Consequences are loss of appetite and reduced growth or weight loss, as well as reduced reproduction and, as a result of immune suppression, reduced disease resistance.

In aquaculture, fish often can not escape a stressor, whereas stressors are common because of e.g. high fish density and management practices. Chronic stress is therefore an intrinsic problem in aquaculture, resulting in low food conversion, diseases and mortalities.

Stress response indicators

The current model of the stress response is based on the dominant roles of catecholamines and glucocorticoids. These hormones are the primary messengers of the two major routes through which the brain coordinates the stress response. In fish these are the brain-sympathetic-chromaffin (bsc-)axis, producing catecholamines, and the hypothalamic-pituitary-interrenal (hpi-)axis, with cortisol as end product.

Persistently or frequently high catecholamine levels during chronic stress are responsible for damage to the cadiovascular system, whereas the deleterious effects of prolonged stress on growth, reproduction and disease resistance are due to prolonged elevated cortisol levels.

Fish are relatively sensitive to stressors when compared to terrestrial vertebrates and one of the main reasons for this is the presence of gills, very delicate and extensive structures with epithelial layers forming a barrier of only a few micrometers between the blood and the ambient water.

Another reason is the structure of the skin, which is very thin, compared to that of terrestrial vertebrates, and only covered by a mucus layer instead of well protected by keratinised layers and structures such as feathers and hairs.

The advantage of the fish skin, with its complicated structure and many different cell types, is its role as an important interface between the fish and its environment, with many sensory cells and organs, with exquisite sensitivity for the detection of water movements, chemicals and signals from other fish, prey animals, or predators. However, the skin is easily damaged mechanically, and through infection, leading to epithelial ulcers which arise rapidly.

Acute stress, as well as chronic stress, is usually associated with marked structural changes of the skin and gills and structural damage to the gills. The latter effect is mainly due to the high blood pressure and increased blood circulation as a result of the stimulated heart rate and ventilatory movements induced by high adrenalin levels.

This may even lead to disruption of the vascularisation of the gills and swelling of the lamellae (epithelial lifting). It may also lead to increased permeability of the branchial and, most likely, the skin epithelia to water and ions which causes severe disturbance of the hydromineral balance, a typical phenomenon of stressed fish. Skin and gills are also primary targets for infectious agents, from viruses to crustacean ectoparasites.

As part of the stress response, skin and gills show many structural changes at the cellular level that can be interpreted as compensatory adjustments. These include rapid replacement of damaged cells and in general a higher turnover of many of the epithelial cell types, as is reflected by high rates of cell death by apoptosis and of mitotic activity.

High proliferation and turnover rates are not only observed for the normal epithelial cells but also in many specialised cell types such as the chloride cells of the gills, which are responsible for ion exchange with the water.

Mitigation of Stress

To reduce the impact of stressors and to facilitate the compensatory adjustments of fish in aquaculture, several food supplements have been advocated. Substances derived from bacteria, algae and fungi, or lyophilised preparations of these organisms, have been introduced to activate the innate defence mechanisms, resulting in stimulated production of antimicrobial molecules or activation of the phagocytotic cells of the immune system.

Also nucleotides as a diet supplement have been shown to stimulate the immune system and to counteract the suppressive effects of stressors. Our studies on arachidonic acid as a food additive have resulted in a significant reduction of the mortality of larval seabream during and after salinity changes, whereas in larval as well as adult seabream the cortisol response to stressors could be reduced.

Addition of L-carnitine has been advocated as a growth promotor and as a factor in providing protection against toxic levels of ammonia and xenobiotics, and alleviation of stress related to water temperature extremes. Another approach concerns the selection of strains of fish with a low cortisol response. In this field only few successes have been reported.

Conclusion

In general, food supplements are promising. But they are expensive and their cost-effectiveness is not always evident. The selection and propagation of stress-resistant strains is still in its infancy.

Preventive measures, such as creating optimal conditions with respect to holding facilities and water quality, the use of well-balanced food, and the strict limitation of stressful management procedures such as grading, transfer and vaccination, are still most effective, in particular for the young life stages with their insufficiently developed innate defense systems.