Warm acclimation and oxygen depletion induce species-specific responses in salmonids

Abstract

Anthropogenic activities are greatly altering the habitats of animals, whereby fish are already encountering several stressors simultaneously. The purpose of the current study was to investigate the capacity of fish to respond to two different environmental stressors (high temperature and overnight hypoxia) separately and together. We found that acclimation to increased temperature (from 7.7±0.02°C to 14.9±0.05°C) and overnight hypoxia (daily changes from normoxia to 63-67% oxygen saturation), simulating climate change and eutrophication, had both antagonistic and synergistic effects on the capacity of fish to tolerate these stressors. The thermal tolerance of Arctic char (Salvelinus alpinus) and landlocked salmon (Salmo salar m. sebago) increased with warm acclimation by 1.3 and 2.2°C, respectively, but decreased when warm temperature was combined with overnight hypoxia (by 0.2 and 0.4°C, respectively). In contrast, the combination of the stressors more than doubled hypoxia tolerance in salmon and also increased hypoxia tolerance in char by 22%. Salmon had 1.2°C higher thermal tolerance than char, but char tolerated much lower oxygen levels than salmon at a given temperature. The changes in hypoxia tolerance were connected to the responses of the oxygen supply and delivery system. The relative ventricle mass was higher in cold-than in warm-acclimated salmon but the thickness of the compact layer of the ventricle increased with the combination of warm and hypoxia acclimation in both species. Char had also significantly larger hearts and thicker compact layers than salmon. The results illustrate that while fish can have protective responses when encountering a single environmental stressor, the combination of stressors can have unexpected species-specific effects that will influence their survival capacity.

Warm acclimation improves hypoxia tolerance in Fundulus heteroclitus

“…The effect of thermal acclimation on hypoxia tolerance Acclimation to warm temperatures markedly improved hypoxia tolerance in killifish, and similar effects have been observed in salmon (Anttila et al, 2015). In killifish, this change was correlated with changes in gill morphology.…”

“…Remodelling of gill morphology has primarily been investigated in the context of acclimation to hypoxia (e.g. Crispo and Chapman, 2010), and this has been shown to occur via changes in the ILCM in a variety of fish species (Sollid et al, 2003(Sollid et al, , 2005aNilsson, 2007;Ong et al, 2007;Matey et al, 2008;Turko et al, 2012;Dhillon et al, 2013;Johannsson et al, 2014;Anttila et al, 2015) including killifish (Borowiec et al, 2015). Less is known about the effects of thermal acclimation on gill morphology, but decreases in the ILCM at warmer temperatures have been observed in crucian carp, goldfish (Sollid et al, 2005b;Mitrovic and Perry, 2009) and killifish (Barnes et al, 2014).…”

“…Changes at any step along the oxygen cascade have the potential to contribute to changes in hypoxia tolerance. For example, in Atlantic salmon (Salmo salar), increases in hypoxia tolerance with warm acclimation are not associated with changes in gill structure (Anttila et al, 2015), but instead increases in capillary density in the compact myocardium have been observed in various salmonids (Egginton and Cordiner, 1997;Anttila et al, 2015). Changes in haemoglobin oxygen affinity could also play a role.…”

Oxygen- and capacity-limited thermal tolerance: bridging ecology and physiology

“…The concept has recently been extended to incorporate the combined effects of various climate changeassociated drivers, such as ocean warming combined with acidification and hypoxia (Pörtner, 2010(Pörtner, , 2012. It should also be noted that the pattern of acclimatisation to one climate-related driver such as temperature can be modified by the combined effects of multiple drivers (Anttila et al, 2015), indicating that highly complex mechanisms shape sublethal and lethal thermal constraints.…”

Rates of hypoxia induction alter mechanisms of O2 uptake and the critical O2 tension of goldfish

“…Some fishes, including goldfish and numerous other species, also have the ability to dramatically increase lamellar surface area in response to hypoxia exposure through apoptotic reductions to the inter-lamellar cell mass (ILCM; Anttila et al, 2015;Borowiec et al, 2015;Crispo and Chapman, 2010;Dhillon et al, 2013;Ong et al, 2007;Sollid et al, 2003Sollid et al, , 2005Turko et al, 2012). While these modifications to different parts of the O 2 transport cascade function to improve O 2 uptake at low Pw O2 , the time courses over which these modifications are enacted differ and may potentially impact the critical P O2 (P crit ) of the rate of O 2 uptake (ṀO 2 ).…”