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Intestinal barrier function of Atlantic salmon (Salmo salar L.) post smolts is reduced by common sea cage environments and suggested as a possible physiological welfare indicator.

Sundh H, Kvamme BO, Fridell F, Olsen RE, Ellis T, Taranger GL, Sundell K - BMC Physiol. (2010)

Bottom Line: The intestinal barrier function, measured as electrical resistance (TER) and permeability of mannitol at the end of the experiment, were reduced at 50% DO, in both proximal and distal intestine.The intestinal barrier function was clearly disturbed in the 50% DO group; TER was reduced in both intestinal regions concomitant with increased paracellular permeability in the distal region.The intestinal barrier function was significantly affected by prolonged hypoxic stress even when no primary stress response was observed.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Zoology/Zoophysiology, University of Gothenburg, Sweden. henrik.sundh@zool.gu.se

ABSTRACT

Background: Fish farmed under high intensity aquaculture conditions are subjected to unnatural environments that may cause stress. Therefore awareness of how to maintain good health and welfare of farmed fish is important. For Atlantic salmon held in sea cages, water flow, dissolved oxygen (DO) levels and temperature will fluctuate over time and the fish can at times be exposed to detrimentally low DO levels and high temperatures. This experimental study investigates primary and secondary stress responses of Atlantic salmon post smolts to long-term exposure to reduced and fluctuating DO levels and high water temperatures, mimicking situations in the sea cages. Plasma cortisol levels and cortisol release to the water were assessed as indicators of the primary stress response and intestinal barrier integrity and physiological functions as indicators of secondary responses to changes in environmental conditions.

Results: Plasma cortisol levels were elevated in fish exposed to low (50% and 60% saturation) DO levels and low temperature (9°C), at days 9, 29 and 48. The intestinal barrier function, measured as electrical resistance (TER) and permeability of mannitol at the end of the experiment, were reduced at 50% DO, in both proximal and distal intestine. When low DO levels were combined with high temperature (16°C), plasma cortisol levels were elevated in the cyclic 1:5 h at 85%:50% DO group and fixed 50% DO group compared to the control (85% DO) group at day 10 but not at later time points. The intestinal barrier function was clearly disturbed in the 50% DO group; TER was reduced in both intestinal regions concomitant with increased paracellular permeability in the distal region.

Conclusions: This study reveals that adverse environmental conditions (low water flow, low DO levels at low and high temperature), that can occur in sea cages, elicits primary and secondary stress responses in Atlantic salmon post smolts. The intestinal barrier function was significantly affected by prolonged hypoxic stress even when no primary stress response was observed. This suggests that intestinal barrier function is a good experimental marker for evaluation of chronic stress and that it can be a valuable tool to study the impact of various husbandry conditions on health and welfare of farmed Atlantic salmon.

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Plasma cortisol and cortisol release rate after long term hypoxia (Experiment 1). This experiment aimed at mimicking an overall situation often found in sea cages when water flow decreases and DO levels are reduced to levels as low as around 50%. Decreased water exchange rate may also cause increased concentrations of toxic metabolites. Four experimental oxygen regimes in triplicate tanks were created, fixed oxygen levels at 50%, 60%, 70% and 80%, automatically regulated by adjusting inflow (range 41-137 L min-1) in response to oxygen consumption of the fish. Blood was sampled for plasma cortisol measurements from all treatment groups at days 9, 29 and 48 and from the 80% and 50% DO between days 41-43. Non-invasive measurement of cortisol status of the fish was conducted by measuring the cortisol release rate into the water. Plasma cortisol levels were analysed using a general linear model with sampling occasion and DO treatment levels (with tank nested within treatment) as factors. DO levels had an effect on plasma cortisol levels (A) (p < 0.001) but were not affected by time (p = 0.607) and no interaction could be observed (p = 0.128). Further, SNK post hoc test grouped the 50% and 60% DO groups in one subset and the 70% and 80% DO groups in one subset at day 9, 29 and 48. No differences could be observed in plasma cortisol between 80% and 50% DO levels in fish sampled for intestinal barrier function between days 41-43. No major differences could be observed in the cortisol release rate between treatment groups (B). All data are expressed as means ± SEM and p < 0.05. The overall effect of treatment is indicated by ◊.
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Figure 1: Plasma cortisol and cortisol release rate after long term hypoxia (Experiment 1). This experiment aimed at mimicking an overall situation often found in sea cages when water flow decreases and DO levels are reduced to levels as low as around 50%. Decreased water exchange rate may also cause increased concentrations of toxic metabolites. Four experimental oxygen regimes in triplicate tanks were created, fixed oxygen levels at 50%, 60%, 70% and 80%, automatically regulated by adjusting inflow (range 41-137 L min-1) in response to oxygen consumption of the fish. Blood was sampled for plasma cortisol measurements from all treatment groups at days 9, 29 and 48 and from the 80% and 50% DO between days 41-43. Non-invasive measurement of cortisol status of the fish was conducted by measuring the cortisol release rate into the water. Plasma cortisol levels were analysed using a general linear model with sampling occasion and DO treatment levels (with tank nested within treatment) as factors. DO levels had an effect on plasma cortisol levels (A) (p < 0.001) but were not affected by time (p = 0.607) and no interaction could be observed (p = 0.128). Further, SNK post hoc test grouped the 50% and 60% DO groups in one subset and the 70% and 80% DO groups in one subset at day 9, 29 and 48. No differences could be observed in plasma cortisol between 80% and 50% DO levels in fish sampled for intestinal barrier function between days 41-43. No major differences could be observed in the cortisol release rate between treatment groups (B). All data are expressed as means ± SEM and p < 0.05. The overall effect of treatment is indicated by ◊.

Mentions: DO levels had an effect on plasma cortisol levels (p < 0.001) but were not affected by time (p = 0.607) and no interaction could be observed (p = 0.128) (Figure 1A). Further post hoc (SNK) analysis of DO treatment levels revealed two subsets of the four oxygen treatments, with 80% and 70% DO in one subset showing lower plasma cortisol values compared to the other subset, containing 60% and 50% DO (p < 0.05). Plasma cortisol levels were also analysed in blood collected from the fish sampled for Ussing chamber experiments, but only in the two extreme treatments at day 41-43, and revealed no differences between these groups.


Intestinal barrier function of Atlantic salmon (Salmo salar L.) post smolts is reduced by common sea cage environments and suggested as a possible physiological welfare indicator.

Sundh H, Kvamme BO, Fridell F, Olsen RE, Ellis T, Taranger GL, Sundell K - BMC Physiol. (2010)

Plasma cortisol and cortisol release rate after long term hypoxia (Experiment 1). This experiment aimed at mimicking an overall situation often found in sea cages when water flow decreases and DO levels are reduced to levels as low as around 50%. Decreased water exchange rate may also cause increased concentrations of toxic metabolites. Four experimental oxygen regimes in triplicate tanks were created, fixed oxygen levels at 50%, 60%, 70% and 80%, automatically regulated by adjusting inflow (range 41-137 L min-1) in response to oxygen consumption of the fish. Blood was sampled for plasma cortisol measurements from all treatment groups at days 9, 29 and 48 and from the 80% and 50% DO between days 41-43. Non-invasive measurement of cortisol status of the fish was conducted by measuring the cortisol release rate into the water. Plasma cortisol levels were analysed using a general linear model with sampling occasion and DO treatment levels (with tank nested within treatment) as factors. DO levels had an effect on plasma cortisol levels (A) (p < 0.001) but were not affected by time (p = 0.607) and no interaction could be observed (p = 0.128). Further, SNK post hoc test grouped the 50% and 60% DO groups in one subset and the 70% and 80% DO groups in one subset at day 9, 29 and 48. No differences could be observed in plasma cortisol between 80% and 50% DO levels in fish sampled for intestinal barrier function between days 41-43. No major differences could be observed in the cortisol release rate between treatment groups (B). All data are expressed as means ± SEM and p < 0.05. The overall effect of treatment is indicated by ◊.
© Copyright Policy - open-access
Related In: Results  -  Collection

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Figure 1: Plasma cortisol and cortisol release rate after long term hypoxia (Experiment 1). This experiment aimed at mimicking an overall situation often found in sea cages when water flow decreases and DO levels are reduced to levels as low as around 50%. Decreased water exchange rate may also cause increased concentrations of toxic metabolites. Four experimental oxygen regimes in triplicate tanks were created, fixed oxygen levels at 50%, 60%, 70% and 80%, automatically regulated by adjusting inflow (range 41-137 L min-1) in response to oxygen consumption of the fish. Blood was sampled for plasma cortisol measurements from all treatment groups at days 9, 29 and 48 and from the 80% and 50% DO between days 41-43. Non-invasive measurement of cortisol status of the fish was conducted by measuring the cortisol release rate into the water. Plasma cortisol levels were analysed using a general linear model with sampling occasion and DO treatment levels (with tank nested within treatment) as factors. DO levels had an effect on plasma cortisol levels (A) (p < 0.001) but were not affected by time (p = 0.607) and no interaction could be observed (p = 0.128). Further, SNK post hoc test grouped the 50% and 60% DO groups in one subset and the 70% and 80% DO groups in one subset at day 9, 29 and 48. No differences could be observed in plasma cortisol between 80% and 50% DO levels in fish sampled for intestinal barrier function between days 41-43. No major differences could be observed in the cortisol release rate between treatment groups (B). All data are expressed as means ± SEM and p < 0.05. The overall effect of treatment is indicated by ◊.
Mentions: DO levels had an effect on plasma cortisol levels (p < 0.001) but were not affected by time (p = 0.607) and no interaction could be observed (p = 0.128) (Figure 1A). Further post hoc (SNK) analysis of DO treatment levels revealed two subsets of the four oxygen treatments, with 80% and 70% DO in one subset showing lower plasma cortisol values compared to the other subset, containing 60% and 50% DO (p < 0.05). Plasma cortisol levels were also analysed in blood collected from the fish sampled for Ussing chamber experiments, but only in the two extreme treatments at day 41-43, and revealed no differences between these groups.

Bottom Line: The intestinal barrier function, measured as electrical resistance (TER) and permeability of mannitol at the end of the experiment, were reduced at 50% DO, in both proximal and distal intestine.The intestinal barrier function was clearly disturbed in the 50% DO group; TER was reduced in both intestinal regions concomitant with increased paracellular permeability in the distal region.The intestinal barrier function was significantly affected by prolonged hypoxic stress even when no primary stress response was observed.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Zoology/Zoophysiology, University of Gothenburg, Sweden. henrik.sundh@zool.gu.se

ABSTRACT

Background: Fish farmed under high intensity aquaculture conditions are subjected to unnatural environments that may cause stress. Therefore awareness of how to maintain good health and welfare of farmed fish is important. For Atlantic salmon held in sea cages, water flow, dissolved oxygen (DO) levels and temperature will fluctuate over time and the fish can at times be exposed to detrimentally low DO levels and high temperatures. This experimental study investigates primary and secondary stress responses of Atlantic salmon post smolts to long-term exposure to reduced and fluctuating DO levels and high water temperatures, mimicking situations in the sea cages. Plasma cortisol levels and cortisol release to the water were assessed as indicators of the primary stress response and intestinal barrier integrity and physiological functions as indicators of secondary responses to changes in environmental conditions.

Results: Plasma cortisol levels were elevated in fish exposed to low (50% and 60% saturation) DO levels and low temperature (9°C), at days 9, 29 and 48. The intestinal barrier function, measured as electrical resistance (TER) and permeability of mannitol at the end of the experiment, were reduced at 50% DO, in both proximal and distal intestine. When low DO levels were combined with high temperature (16°C), plasma cortisol levels were elevated in the cyclic 1:5 h at 85%:50% DO group and fixed 50% DO group compared to the control (85% DO) group at day 10 but not at later time points. The intestinal barrier function was clearly disturbed in the 50% DO group; TER was reduced in both intestinal regions concomitant with increased paracellular permeability in the distal region.

Conclusions: This study reveals that adverse environmental conditions (low water flow, low DO levels at low and high temperature), that can occur in sea cages, elicits primary and secondary stress responses in Atlantic salmon post smolts. The intestinal barrier function was significantly affected by prolonged hypoxic stress even when no primary stress response was observed. This suggests that intestinal barrier function is a good experimental marker for evaluation of chronic stress and that it can be a valuable tool to study the impact of various husbandry conditions on health and welfare of farmed Atlantic salmon.

Show MeSH
Related in: MedlinePlus