Warm acclimation improves hypoxia tolerance in Fundulus heteroclitus

Abstract

Human activities are increasing both the frequency of hypoxic episodes and the mean temperature of aquatic ecosystems, but few studies have considered the possibility that acclimation to one of these stressors could improve the ability to cope with the other stressor. Here, we used Atlantic killifish, Fundulus heteroclitus, to test this hypothesis. Hypoxia tolerance was measured as time to loss of equilibrium in hypoxia (LOE hyp ) at 0.4 kPa oxygen. Time to LOE hyp declined from 73.3±6.9 min at 15°C to 2.6±3.8 min at 23°C, and at 30°C no fish could withstand this level of hypoxia. Prior acclimation to warm temperatures significantly increased time to LOE hyp . Hypoxia tolerance of the southern subspecies of killifish, F. heteroclitus heteroclitus, was greater than that of the northern subspecies, F. heteroclitus macrolepidotus, measured both as critical oxygen tension (P crit ) and as time to LOE hyp . Warm acclimation offset the negative effects of temperature on time to LOE hyp to a similar extent in the two subspecies. Warm acclimation increased total lamellar surface area of the gill in both subspecies as a result of regression of an interlamellar cell mass (ILCM). However, differences in total lamellar surface area could not explain differences in time to LOE hyp between the subspecies, suggesting that the lower time to LOE hyp of northern fish is related to their higher routine metabolic rate. These data suggest that thermal plasticity in gill morphology can improve the capacity of this species to tolerate hypoxia, and shows how existing plasticity may help organisms to cope with the complex interacting stressors that they will encounter with increasing frequency as our climate changes.

Tropical fish in a warming world: thermal tolerance of Nile perchLates niloticus(L.) in Lake Nabugabo, Uganda

“…An extensive study on the genetic basis of tolerance to temperature and hypoxia in S. salar revealed a positive correlation between thermal tolerance (CTmax) and hypoxia tolerance (Anttila et al ., 2013). A potential explanation for this positive correlation is the fact that similar mechanisms are involved in tolerance to temperature and hypoxia (McBryan et al ., 2016). …”

“…Hypoxia and water temperature may also interact because both affect aerobic metabolism. By limiting the availability of environmental oxygen to fishes, hypoxia makes it more challenging to meet the increased metabolic demands driven by higher temperature (McBryan et al ., 2016). However, adaptations to either thermal stress or hypoxia could improve the ability of fishes to cope with the alternative stressor (McBryan et al ., 2016).…”

“…By limiting the availability of environmental oxygen to fishes, hypoxia makes it more challenging to meet the increased metabolic demands driven by higher temperature (McBryan et al ., 2016). However, adaptations to either thermal stress or hypoxia could improve the ability of fishes to cope with the alternative stressor (McBryan et al ., 2016). Conceptual models predict that the tolerance to aquatic hypoxia in ectotherms is maximal within the thermal optimum and that processes that mitigate effects of thermally induced hypoxaemia should improve hypoxia tolerance (Pörtner, 2010).…”

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

“…This represented a normoxic routine ṀO 2 that was likely close to standard ṀO 2 as a result of it being made following a habituation period that was ≥16 h. We then determined P crit as the intersection of this horizontal line with a linear regression through the ṀO 2 values that were >15% below the mean routine ṀO 2 value. This technique was carried out according to McBryan et al (2016).…”

Physiological and morphological investigation of Arctic grayling (Thymallus arcticus) gill filaments with high salinity exposure and recovery

“…Importantly, exposure to 17 ppt saline water resulted in gill remodelling and the appearance of an ILCM in the grayling that was not present in rainbow trout under the same treatments (Blair et al , 2016). Ionoregulatory and osmoregulatory perturbations have been shown to alter the ILCM in a variety of fish: hypoxia-induced changes in ILCM in goldfish and crucian carp (Sollid et al , 2003; Sollid and Nilsson, 2006; Nilsson et al , 2012); temperature variations in goldfish, crucian carp (Sollid et al , 2005; Mitrovic and Perry, 2009) and killifish (McBryan et al , 2016); high environmental ammonia on crucian carp (Sinha et al , 2014); air exposure and salinity on killifish (Ong et al , 2007; LeBlanc et al , 2010; Turko et al , 2011) and increases to ILCM of brook trout exposed to aluminium (Mueller et al , 1991). We hypothesized that the ILCM appearance in the Arctic grayling in response to salinity could be a protective mechanism limiting the uptake of salts (Na + /Cl – ) under hypertonic environments.…”