Oxygen consumption of desert pupfish at ecologically relevant temperatures suggests a significant role for anaerobic metabolism

Abstract

Oxygen consumption is oftentimes used as a proxy for metabolic rate. However, pupfish acclimated to ecologically relevant temperatures may employ extended periods of anaerobism despite the availability of oxygen-a process we called paradoxical anaerobism. In this study, we evaluated data from pupfish exhibiting stable oxygen consumption. Routine oxygen consumption ([Formula: see text]) of a refuge population derived from Cyprinodon spp. acclimated to 28 and 33 °C was evaluated at the ecologically relevant assay temperatures of between 25 and 38 °C. Different interpretations of the data are available depending on normalization. For instance, [Formula: see text] of smaller fish, measured per fish, was remarkably stable over a wide range of assay temperatures and was not different between acclimation groups. However, when measured on a mass-specific basis, [Formula: see text] in these same smaller fish increases more predictably as temperature increased. [Formula: see text] of refuge fish and the closely related pupfish, C. nevadensis mionectes, measured near their respective acclimation temperatures, were essentially identical. However, [Formula: see text] of 28 °C acclimated fish of both species, when measured at 34 °C, was greater than that of the 33 °C acclimated fish measured at 28 °C. We suggest that this observed 'efficiency' may result from significant anaerobic metabolism use. Experiments investigating factorial aerobic scope ([Formula: see text]/[Formula: see text]) yielded values less than 1 in 21-36% of the 33 °C acclimated fish. These values indicate a substantial contribution of anaerobic metabolism to energy utilization by these fish. However, muscle lactate levels are not elevated in exercising fish-a result that is consistent with paradoxical anaerobism use.

The gut microbiome and its potential role in paradoxical anaerobism in pupfishes of the Mojave Desert

“…While this phenotype is frequently manifested by oxygen consumption that is more variable and lower than what may be otherwise expected, we believe a positive feedback mechanism resulting in more and more closure of the VDACs results in the paradoxical anaerobism characterized by negligible oxygen consumption. Consistent with this model are data from 33 °C-acclimated pupfish demonstrating a much higher frequency of a state of variable oxygen consumption (~20% of 33 °C-acclimated pupfish assayed for 2 h as compared to <4% of 28 °C-acclimated pupfish), lower than expected oxygen consumption, and lower aerobic scope (maximum oxygen consumption • rVO 2 -1 ) [2,3]. In other words, both 28-and 33°C…”

“…The Mojave Desert in the Southwestern United States is a home to isolated systems of springs that are geothermally or ambiently heated to 28 to 33 °C and are inhabited by pupfish in the genus Cyprinodon [1]. Previously, we demonstrated that two lineages of pupfish reared at 33 °C frequently entered a state of paradoxical anaerobism [2,3]. For periods of as much as 149 minutes, these pupfish consumed negligible oxygen despite its availability.…”

The gut microbiome and its potential role in paradoxical anaerobism in pupfishes of the Mojave Desert

“…While this phenotype is frequently manifested by oxygen consumption that is more variable and lower than what may be otherwise expected, we believe a positive feedback mechanism resulting in more and more closure of the VDACs results in the paradoxical anaerobism characterized by negligible oxygen consumption. Consistent with this model are data from 33 °C-acclimated pupfish demonstrating a much higher frequency of a state of variable oxygen consumption (~ 20% of 33 °C-acclimated pupfish assayed for 2 h as compared to < 4% of 28 °C-acclimated pupfish), lower than expected oxygen consumption, and lower aerobic scope (maximum oxygen consumption • rVO 2 − 1 ) [ 2 , 3 ]. In other words, both 28- and 33 °C-acclimated pupfish are likely using a mosaic of both paradoxical anaerobism and oxygen consumption.…”

“…Routine rates of oxygen consumption (rVO 2 ) were measured in fish showing minimal activity using flow-through respirometry (Fig. S1 ) [ 2 , 3 ]. Briefly, four fish at a time were placed individually in glass metabolic chambers (60 mL volume) that were connected to flow cells with Clark-type oxygen electrodes (Strathkelvin, Scotland).…”

“…The Mojave Desert in the Southwestern United States is home to isolated systems of springs that are geothermally or ambiently heated to 28 to 33 °C and are inhabited by pupfishes in the genus Cyprinodon [ 1 ]. Previously, we demonstrated that two lineages of pupfishes reared at 33 °C frequently entered a state of paradoxical anaerobism [ 2 , 3 ]. For periods of as much as 149 min, these pupfish consumed negligible oxygen despite its availability.…”