The effects of dissolved oxygen and aquatic surface respiration on the critical thermal maxima of three intermittent-stream fishes

132

151

Temperature-induced limitations on the capacity of the cardiorespiratory system to transport oxygen from the environment to the tissues, manifested as a reduced aerobic scope (maximum minus standard metabolic rate), have been proposed as the principal determinant of the upper thermal limits of fishes and other waterbreathing ectotherms. Consequently, the upper thermal niche boundaries of these animals are expected to be highly sensitive to aquatic hypoxia and other environmental stressors that constrain their cardiorespiratory performance. However, the generality of this dogma has recently been questioned, as some species have been shown to maintain aerobic scope at thermal extremes. Here, we experimentally tested whether reduced oxygen availability due to aquatic hypoxia would decrease the upper thermal limits (i.e. the critical thermal maximum, CT max ) of the estuarine red drum (Sciaenops ocellatus) and the marine lumpfish (Cyclopterus lumpus). In both species, CT max was independent of oxygen availability over a wide range of oxygen levels despite substantial (>72%) reductions in aerobic scope. These data show that the upper thermal limits of waterbreathing ectotherms are not always linked to the capacity for oxygen transport. Consequently, we propose a novel metric for classifying the oxygen dependence of thermal tolerance; the oxygen limit for thermal tolerance (P CTmax ), which is the water oxygen tension (Pw O2 ) where an organism's CT max starts to decline. We suggest that this metric can be used for assessing the oxygen sensitivity of upper thermal limits in water-breathing ectotherms, and the susceptibility of their upper thermal niche boundaries to environmental hypoxia.

Section: Discussionsupporting

confidence: 92%

Oxygen-dependence of upper thermal limits in fishes

Ern

Norin

Gamperl

et al. 2016

132

151

“…However, this substantial increase in AS under hyperoxia did not enhance the acute upper thermal limits of perch, as CT max was not significantly elevated when compared with control fish. Although these findings conflict with a study investigating the effects of increased environmental oxygen tension on acute thermal tolerance of goldfish (Carassius auratus) at hyperbaric pressures (Weatherley, 1970), they are consistent with findings from a range of other fish species exposed to hyperoxic conditions under ambient pressure (Healy and Schulte, 2012;Mark et al, 2002;Rutledge and Beitinger, 1989). Weatherley (1970) also observed that even in the presence of a superabundance of oxygen, enhanced thermal tolerance ended abruptly at a definite 'breakpoint' and thus was indicative of a physiological failure independent of oxygen limitation.…”

Section: Hyperoxia Increases Aerobic Scope But Not Acute Upper Thermasupporting

confidence: 64%

“…hypoxia; Healy and Schulte, 2012;Rutledge and Beitinger, 1989;Weatherley, 1970). While these results lend support to the idea that oxygen supply limits thermal tolerance, one would expect hyperoxia (i.e.…”

Section: Introductionsupporting

confidence: 55%

“…an increase in environmental oxygen availability) to increase the upper limit of thermal tolerance if oxygen supply is indeed the limiting factor. To date, few studies have investigated the effects of hyperoxia on the thermal tolerance of fishes, and results are conflicting, with some species displaying an increased thermal tolerance (Weatherley, 1970), while others remain unaffected (Healy and Schulte, 2012;Mark et al, 2002;Rutledge and Beitinger, 1989).…”

Section: Introductionmentioning

confidence: 99%

See 1 more Smart Citation

Experimental manipulations of tissue oxygen supply do not affect warming tolerance of European perch

Brijs

Jutfelt

Clark

et al. 2015

A progressive inability of the cardiorespiratory system to maintain systemic oxygen supply at elevated temperatures has been suggested to reduce aerobic scope and the upper thermal limit of aquatic ectotherms. However, few studies have directly investigated the dependence of thermal limits on oxygen transport capacity. By manipulating oxygen availability (via environmental hyperoxia) and blood oxygen carrying capacity (via experimentally induced anaemia) in European perch (Perca fluviatilis Linneaus), we investigated the effects of oxygen transport capacity on aerobic scope and the critical thermal maximum (CT max ). Hyperoxia resulted in a twofold increase in aerobic scope at the control temperature of 23°C, but this did not translate to an elevated CT max in comparison with control fish (34.6± 0.1 versus 34.0±0.5°C, respectively). Anaemia (∼43% reduction in haemoglobin concentration) did not cause a reduction in aerobic scope or CT max (33.8±0.3°C) compared with control fish. Additionally, oxygen consumption rates of anaemic perch during thermal ramping increased in a similar exponential manner to that in control fish, highlighting that perch have an impressive capacity to compensate for a substantial reduction in blood oxygen carrying capacity. Taken together, these results indicate that oxygen limitation is not a universal mechanism determining the CT max of fishes.

“…To establish causality requires showing that tissue hypoxia occurs at the onset of other adverse effects of temperature and that experimentally manipulating tissue hypoxia levels (e.g. through experimental hyperoxia) improves thermal tolerance in fishes (Weatherley, 1970;Rutledge and Beitinger, 1989).…”

Section: Ecological Relevance Of Aerobic Scope and T Optasmentioning

confidence: 99%

Aerobic scope measurements of fishes in an era of climate change: respirometry, relevance and recommendations

Clark

Sandblom

Jutfelt

2013

772

870

SummaryMeasurements of aerobic scope [the difference between minimum and maximum oxygen consumption rate (M O2,min and M O2,max , respectively)] are increasing in prevalence as a tool to address questions relating to fish ecology and the effects of climate change. However, there are underlying issues regarding the array of methods used to measure aerobic scope across studies and species. In an attempt to enhance quality control before the diversity of issues becomes too great to remedy, this paper outlines common techniques and pitfalls associated with measurements of M O2,min , M O2,max and aerobic scope across species and under different experimental conditions. Additionally, we provide a brief critique of the oxygen-and capacity-limited thermal tolerance (OCLTT) hypothesis, a concept that is intricately dependent on aerobic scope measurements and is spreading wildly throughout the literature despite little evidence for its general applicability. It is the intention of this paper to encourage transparency and accuracy in future studies that measure the aerobic metabolism of fishes, and to highlight the fundamental issues with assuming broad relevance of the OCLTT hypothesis.