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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 fixed and cyclic, low DO levels at high temperature (Experiment 2). This experiment aimed at mimicking DO levels measured in sea cages in fjords sheltered from waves, wind and strong currents. In these situations, cyclic drops in DO levels are frequently observed during slack water at tidal reverse and further decreased DO levels are observed during high temperatures. Four oxygen treatment regimes were initiated: fixed 50% or 85% DO levels, or 50% or 85% DO levels in two different 6 hour cycles (4:2 h at 85:50%; 1:5 h at 85:50%) at 16°C. Blood was sampled for plasma cortisol measurements from all treatment groups day 10 and 29, and from the fixed 85% and 50% DO groups between days 36-38. Cortisol levels in plasma at different time points after start of Experiment 2, assessing the impact of cyclic and fixed DO levels. Plasma cortisol samples below the limit of detection was removed and indicated in each bar (A). DO levels were not affected by sampling occasion (p = 0.572) but slightly influenced by DO treatment levels (p = 0.088). An interaction was observed (p = 0.029) and Bonferroni corrected pair-wise comparison of plasma cortisol levels revealed elevated cortisol levels in the 1:5 h at 85:50% DO group and 50% DO group compared to the 85% DO group (p = 0.002 and p = 0.012 respectively) at the first sampling after 10 days. Thereafter no differences could be observed. Overall, the cortisol release rate (B) reflected the plasma cortisol levels as there was a tendency toward lower cortisol release rate in the 85% DO group (p = 0.1). Further, plasma cortisol levels on day 29 appeared to be reflected in the cortisol release rate on day 28. All data are expressed as means ± SEM and p < 0.05 was regarded as significant and indicated as *, p < 0.01 as ** and p < 0.001 indicated as ***.
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Figure 2: Plasma cortisol and cortisol release rate after fixed and cyclic, low DO levels at high temperature (Experiment 2). This experiment aimed at mimicking DO levels measured in sea cages in fjords sheltered from waves, wind and strong currents. In these situations, cyclic drops in DO levels are frequently observed during slack water at tidal reverse and further decreased DO levels are observed during high temperatures. Four oxygen treatment regimes were initiated: fixed 50% or 85% DO levels, or 50% or 85% DO levels in two different 6 hour cycles (4:2 h at 85:50%; 1:5 h at 85:50%) at 16°C. Blood was sampled for plasma cortisol measurements from all treatment groups day 10 and 29, and from the fixed 85% and 50% DO groups between days 36-38. Cortisol levels in plasma at different time points after start of Experiment 2, assessing the impact of cyclic and fixed DO levels. Plasma cortisol samples below the limit of detection was removed and indicated in each bar (A). DO levels were not affected by sampling occasion (p = 0.572) but slightly influenced by DO treatment levels (p = 0.088). An interaction was observed (p = 0.029) and Bonferroni corrected pair-wise comparison of plasma cortisol levels revealed elevated cortisol levels in the 1:5 h at 85:50% DO group and 50% DO group compared to the 85% DO group (p = 0.002 and p = 0.012 respectively) at the first sampling after 10 days. Thereafter no differences could be observed. Overall, the cortisol release rate (B) reflected the plasma cortisol levels as there was a tendency toward lower cortisol release rate in the 85% DO group (p = 0.1). Further, plasma cortisol levels on day 29 appeared to be reflected in the cortisol release rate on day 28. All data are expressed as means ± SEM and p < 0.05 was regarded as significant and indicated as *, p < 0.01 as ** and p < 0.001 indicated as ***.

Mentions: In this experiment plasma cortisol samples below limit of detection were removed in order not to violate the statistical analysis. At day 10, 14 fish from the 3 least extreme treatments (85% DO, 2:4 h at 85:50% DO, 1:5 h at 85:50% DO) and 9 fish from the 50% DO group were excluded (Figure 2A). At day 29, 10 samples were excluded from the 85% DO group, 8 samples from the 2:4 h at 85:50% DO group, 9 samples from the 1:5 h at 85:50% DO group and 16 from the 50% DO group (Figure 2A). Plasma cortisol levels were not affected by sampling occasion (p = 0.572) but slightly influenced by DO treatment levels (p = 0.088). An interaction was observed (p = 0.029) and Bonferroni corrected pair-wise comparison of plasma cortisol levels revealed elevated cortisol levels in the 1:5 h at 85:50% DO group and 50% DO group compared to the 85% DO group (p = 0.002 and p = 0.012 respectively) at the first sampling after 10 days (Figure 2A). Thereafter no differences could be observed. Moreover, all treatment groups showed the same pattern in time, ie. no difference between sampling occasions (p = 0.572). Also in this experiment, plasma cortisol levels were analysed in samples from the fish used for Ussing chamber experiments, but only in the the two extreme groups at day 36-38 but no differences could be revealed.


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 fixed and cyclic, low DO levels at high temperature (Experiment 2). This experiment aimed at mimicking DO levels measured in sea cages in fjords sheltered from waves, wind and strong currents. In these situations, cyclic drops in DO levels are frequently observed during slack water at tidal reverse and further decreased DO levels are observed during high temperatures. Four oxygen treatment regimes were initiated: fixed 50% or 85% DO levels, or 50% or 85% DO levels in two different 6 hour cycles (4:2 h at 85:50%; 1:5 h at 85:50%) at 16°C. Blood was sampled for plasma cortisol measurements from all treatment groups day 10 and 29, and from the fixed 85% and 50% DO groups between days 36-38. Cortisol levels in plasma at different time points after start of Experiment 2, assessing the impact of cyclic and fixed DO levels. Plasma cortisol samples below the limit of detection was removed and indicated in each bar (A). DO levels were not affected by sampling occasion (p = 0.572) but slightly influenced by DO treatment levels (p = 0.088). An interaction was observed (p = 0.029) and Bonferroni corrected pair-wise comparison of plasma cortisol levels revealed elevated cortisol levels in the 1:5 h at 85:50% DO group and 50% DO group compared to the 85% DO group (p = 0.002 and p = 0.012 respectively) at the first sampling after 10 days. Thereafter no differences could be observed. Overall, the cortisol release rate (B) reflected the plasma cortisol levels as there was a tendency toward lower cortisol release rate in the 85% DO group (p = 0.1). Further, plasma cortisol levels on day 29 appeared to be reflected in the cortisol release rate on day 28. All data are expressed as means ± SEM and p < 0.05 was regarded as significant and indicated as *, p < 0.01 as ** and p < 0.001 indicated as ***.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2992494&req=5

Figure 2: Plasma cortisol and cortisol release rate after fixed and cyclic, low DO levels at high temperature (Experiment 2). This experiment aimed at mimicking DO levels measured in sea cages in fjords sheltered from waves, wind and strong currents. In these situations, cyclic drops in DO levels are frequently observed during slack water at tidal reverse and further decreased DO levels are observed during high temperatures. Four oxygen treatment regimes were initiated: fixed 50% or 85% DO levels, or 50% or 85% DO levels in two different 6 hour cycles (4:2 h at 85:50%; 1:5 h at 85:50%) at 16°C. Blood was sampled for plasma cortisol measurements from all treatment groups day 10 and 29, and from the fixed 85% and 50% DO groups between days 36-38. Cortisol levels in plasma at different time points after start of Experiment 2, assessing the impact of cyclic and fixed DO levels. Plasma cortisol samples below the limit of detection was removed and indicated in each bar (A). DO levels were not affected by sampling occasion (p = 0.572) but slightly influenced by DO treatment levels (p = 0.088). An interaction was observed (p = 0.029) and Bonferroni corrected pair-wise comparison of plasma cortisol levels revealed elevated cortisol levels in the 1:5 h at 85:50% DO group and 50% DO group compared to the 85% DO group (p = 0.002 and p = 0.012 respectively) at the first sampling after 10 days. Thereafter no differences could be observed. Overall, the cortisol release rate (B) reflected the plasma cortisol levels as there was a tendency toward lower cortisol release rate in the 85% DO group (p = 0.1). Further, plasma cortisol levels on day 29 appeared to be reflected in the cortisol release rate on day 28. All data are expressed as means ± SEM and p < 0.05 was regarded as significant and indicated as *, p < 0.01 as ** and p < 0.001 indicated as ***.
Mentions: In this experiment plasma cortisol samples below limit of detection were removed in order not to violate the statistical analysis. At day 10, 14 fish from the 3 least extreme treatments (85% DO, 2:4 h at 85:50% DO, 1:5 h at 85:50% DO) and 9 fish from the 50% DO group were excluded (Figure 2A). At day 29, 10 samples were excluded from the 85% DO group, 8 samples from the 2:4 h at 85:50% DO group, 9 samples from the 1:5 h at 85:50% DO group and 16 from the 50% DO group (Figure 2A). Plasma cortisol levels were not affected by sampling occasion (p = 0.572) but slightly influenced by DO treatment levels (p = 0.088). An interaction was observed (p = 0.029) and Bonferroni corrected pair-wise comparison of plasma cortisol levels revealed elevated cortisol levels in the 1:5 h at 85:50% DO group and 50% DO group compared to the 85% DO group (p = 0.002 and p = 0.012 respectively) at the first sampling after 10 days (Figure 2A). Thereafter no differences could be observed. Moreover, all treatment groups showed the same pattern in time, ie. no difference between sampling occasions (p = 0.572). Also in this experiment, plasma cortisol levels were analysed in samples from the fish used for Ussing chamber experiments, but only in the the two extreme groups at day 36-38 but no differences could be revealed.

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