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

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.

You Better Repeat It: Complex CO2 × Temperature Effects in Atlantic Silverside Offspring Revealed by Serial Experimentation

“…While acclimation to chronic hypercapnia likely has small metabolic costs [86], over longer timescales tradeoffs associated with increased acid/base regulation could compromise other physiological processes [43]. In a previous study, we documented small but significant size reductions in M. menidia reared under~2200 µatm CO 2 and 17 • C for approximately a third of their lifespan [62].…”

Living in a high CO2 world: a global meta‐analysis shows multiple trait‐mediated fish responses to ocean acidification

“…More recently, the compensatory responses that occur during acid‐base regulation were found to influence fish calcification, behavior, and ion transport (Nilsson et al. , Heuer and Grosell , ). Calcification in fish occurs in the inner ear for formation of otoliths, carbonated structures playing a role in sound detection, acceleration, and orientation, and in the intestinal lumen, where calcium carbonate is precipitated to excrete excess calcium ions (Heuer and Grosell ).…”

“…Variability of CO 2 concentrations may also occur weekly or seasonally according to lunar cycles, river and terrestrial inputs, precipitation and decomposition rates, or coastal oceanography dynamics (i.e., upwelling currents), while anthropogenic forcing can cause CO 2 levels to change across different decades (e.g., Hofmann et al. , Baumann et al. , Boyd et al.…”

“…Consequently, fish may already experience a wide range of CO 2 concentrations, which are not predicted to occur in the open ocean even in the next centuries (e.g., Hofmann et al. ).…”

Intergenerational effects of CO2‐induced stream acidification in the Trinidadian guppy (Poecilia reticulata)

“…Fish must continually maintain optimum internal pH, which generally differs from the pH of surrounding water (freshwater or marine) and hence leads to a gradient between internal and external pH (Leduc, Munday, Brown, & Ferrari, ). Changes in pH that deviate from what aquatic organisms are adapted to could result in increased maintenance costs for the individual (Baker & Brauner, ; Heuer & Grosell, ). Higher maintenance costs decrease energy availability for growth and reproduction and hence have the potential to reduce overall fitness.…”