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Acute high temperature exposure impairs hypoxia tolerance in an intertidal fish.

ABSTRACT: Acute heat shock has previously been shown to improve subsequent low O2 (hypoxia) tolerance in an intertidal fish species, a process known as cross-tolerance, but it is not known whether this is a widespread phenomenon. This study examined whether a rock pool specialist, the triplefin fish Bellapiscis medius, exhibits heat shock induced cross-tolerance to hypoxia, i.e., longer time to loss of equilibrium (LOE) and lower critical O2 saturation (Scrit) after recovering from an acute heat challenge. Non-heat shock controls had a median time to loss of equilibrium (LOE50) of 54.4 min under severe hypoxia (7% of air saturation) and a Scrit of 15.8% air saturation. Contrary to expectations, however, treatments that received an 8 or 10°C heat shock showed a significantly shorter LOE50 in hypoxia (+8°C = 41.5 min; +10°C = 28.7 min) and no significant change in Scrit (+8°C = 17.0% air saturation; +10°C = 18.3% of air saturation). Thus, there was no evidence of heat shock induced cross-tolerance to hypoxia in B. medius because exposure to acute heat shock impaired hypoxia tolerance.

SUBMITTER: McArley TJ

PROVIDER: S-EPMC7117701 | biostudies-literature | 2020

REPOSITORIES: biostudies-literature

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Acute high temperature exposure impairs hypoxia tolerance in an intertidal fish.

McArley Tristan J TJ Hickey Anthony J R AJR Herbert Neill A NA

PloS one 20200402 4

Acute heat shock has previously been shown to improve subsequent low O2 (hypoxia) tolerance in an intertidal fish species, a process known as cross-tolerance, but it is not known whether this is a widespread phenomenon. This study examined whether a rock pool specialist, the triplefin fish Bellapiscis medius, exhibits heat shock induced cross-tolerance to hypoxia, i.e., longer time to loss of equilibrium (LOE) and lower critical O2 saturation (Scrit) after recovering from an acute heat challenge ...[more]

PMID: 32240240

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Project description:Persistent hypoxic or low-oxygen conditions in aquatic systems are becoming more frequent worldwide, causing large-scale mortalities to aquatic fauna. It is poorly understood, however, whether species can acclimate to long-term hypoxic conditions. In two experiments, we exposed juvenile freshwater fish (Murray cod, Maccullochella peelii) to low-oxygen conditions and investigated acclimation effects. Experiment 1 determined how responses could be modified by exposure to different temperatures (20, 24 and 28°C) and oxygen conditions (control 6-8 mgO2 L-1 and low-oxygen 3-4 mgO2 L-1) over 30 days. Experiment 2 determined the acclimation ability of fish exposed to two temperatures (20 and 28°C) and low-oxygen conditions (3-4 mgO2 L-1) for three different acclimation periods (7, 14 and 30 days). Responses were measured by determining critical oxygen tension (P crit), loss of equilibrium and aerobic capacity using resting respirometry. In experiment 1, resting oxygen requirements were negatively affected by long-term low-oxygen exposure except at the highest temperature (28°C). However, long-term acclimation in low-oxygen improved tolerance as measured by loss of equilibrium but not P crit. In experiment 2, fish could tolerate lower oxygen levels before reaching loss of equilibrium after 7 days acclimation, but this declined overtime. Murray cod were most tolerant to low-oxygen at the lowest temperature (20°C) and shortest exposure time (7 days). Extended low-oxygen exposure resulted in reduced aerobic capacity of fish particularly at the lowest temperature. While prior exposure to low-oxygen may allow fish to cope with hypoxic conditions better in the long-term, acclimation time was inversely related to tolerance, suggesting that resistance to hypoxia might decrease as a function of exposure time. Our study fills a much-needed gap in our understanding of how freshwater species acclimate to hypoxia, and in particular, how exposure to prolonged periods of low-oxygen and elevated temperatures affect organisms physiologically.

Project description:The theory for thermal plasticity of tropical ectotherms has centered on terrestrial and open-water marine animals which experience reduced variation in diurnal and seasonal temperatures, conditions constraining plasticity selection. Tropical marine intertidal animals, however, experience complex habitat thermal heterogeneity, circumstances encouraging thermal plasticity selection. Using the tropical rocky-intertidal gastropod, Echinolittorina malaccana, we investigated heat tolerance plasticity in terms of laboratory acclimation and natural acclimatization of populations from thermally-dissimilar nearby shorelines. Laboratory treatments yielded similar capacities of snails from either population to acclimate their lethal thermal limit (LT50 variation was ∼2°C). However, the populations differed in the temperature range over which acclimatory adjustments could be made; LT50 plasticity occurred over a higher temperature range in the warm-shore snails compared to the cool-shore snails, giving an overall acclimation capacity for the populations combined of 2.9°C. In addition to confirming significant heat tolerance plasticity in tropical intertidal animals, these findings reveal two plasticity forms, reversible (laboratory acclimation) and non-reversible (population or shoreline specific) plasticity. The plasticity forms should account for different spatiotemporal scales of the environmental temperature variation; reversible plasticity for daily and tidal variations in microhabitat temperature and non-reversible plasticity for lifelong, shoreline temperature conditions. Non-reversible heat tolerance plasticity, likely established after larvae settle on the shore, should be energetically beneficial in preventing heat shock protein overexpression, but also should facilitate widespread colonization of coasts that support thermally-diverse shorelines. This first demonstration of different plasticity forms in benthic intertidal animals supports the hypothesis that habitat heterogeneity (irrespective of latitude) drives thermal plasticity selection. It further suggests that studies not making reference to different spatial scales of thermal heterogeneity, nor seeking how these may drive different thermal plasticity forms, risk misinterpreting ectothermic responses to environmental warming.

Dataset Information

Acute high temperature exposure impairs hypoxia tolerance in an intertidal fish.

Publications

Acute high temperature exposure impairs hypoxia tolerance in an intertidal fish.

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