Elevated CO2 increases energetic cost and ion movement in the marine fish intestine.

Rachael M Heuer,Martin Grosell

doi:10.1038/srep34480

Rachael M Heuer, Martin Grosell

Open Access

https://doi.org/10.1038/srep34480

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Journal: Scientific Reports	Publication Date: Sep 29, 2016
Citations: 53	License type: CC BY 4.0

Affiliation: University of North Texas, University of Miami

Abstract

Energetic costs associated with ion and acid-base regulation in response to ocean acidification have been predicted to decrease the energy available to fish for basic life processes. However, the low cost of ion regulation (6–15% of standard metabolic rate) and inherent variation associated with whole-animal metabolic rate measurements have made it difficult to consistently demonstrate such a cost. Here we aimed to gain resolution in assessing the energetic demand associated with acid-base regulation by examining ion movement and O2 consumption rates of isolated intestinal tissue from Gulf toadfish acclimated to control or 1900 μatm CO2 (projected for year 2300). The active marine fish intestine absorbs ions from ingested seawater in exchange for HCO3− to maintain water balance. We demonstrate that CO2 exposure causes a 13% increase of intestinal HCO3− secretion that the animal does not appear to regulate. Isolated tissue from CO2-exposed toadfish also exhibited an 8% higher O2 consumption rate than tissue from controls. These findings show that compensation for CO2 leads to a seemingly maladaptive persistent base (HCO3−) loss that incurs an energetic expense at the tissue level. Sustained increases to baseline metabolic rate could lead to energetic reallocations away from other life processes at the whole-animal level.

Highlights

Energetic costs associated with ion and acid-base regulation in response to ocean acidification have been predicted to decrease the energy available to fish for basic life processes
This pH compensation is associated with a sustained increase of extra and intracellular concentration of HCO3− in response to the elevated partial pressure of CO211–15
CO2 acclimated toadfish exhibited significantly increased HCO3− secretion rates when compared to control tissue under identical conditions (Fig. 1). This result indicated prior acclimation to CO2 does not suppress but stimulates intestinal HCO3− transport by around 13%. Within both the control and CO2 acclimated fish, HCO3− secretion rates using serosal salines mimicking plasma conditions at 1900 μatm CO2 were significantly higher than HCO3− secretion rates under control serosal salines (Two-way ANOVA, Fish treatment P < 0.009, Saline P < 0.001, Fish treatment × saline P < 0.490, Fig. 1)

Summary

Introduction

Energetic costs associated with ion and acid-base regulation in response to ocean acidification have been predicted to decrease the energy available to fish for basic life processes. We aimed to gain resolution in assessing the energetic demand associated with acid-base regulation by examining ion movement and O2 consumption rates of isolated intestinal tissue from Gulf toadfish acclimated to control or 1900 μatm CO2 (projected for year 2300). Isolated tissue from CO2-exposed toadfish exhibited an 8% higher O2 consumption rate than tissue from controls These findings show that compensation for CO2 leads to a seemingly maladaptive persistent base (HCO3−) loss that incurs an energetic expense at the tissue level. After seeing a stimulation rather than a reduction of bicarbonate secretion rates, a second goal was to test the hypothesis that an increase in intestinal ion transport that occurs in response to elevated CO2 would be associated with an increased tissue metabolic demand. Experiments were conducted at 1900 μatm CO2, a level currently seen in certain coastal and upwelling zones[26,27] and predicted globally in year 230028

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