Changes to Intestinal Transport Physiology and Carbonate Production at Various CO₂Levels in a Marine Teleost, the Gulf Toadfish (Opsanus beta)

Abstract

Most marine teleosts defend blood pH during high CO2 exposure by sustaining elevated levels of HCO3(-) in body fluids. In contrast to the gill, where measures are taken to achieve net base retention, elevated CO2 leads to base loss in the intestine of marine teleosts studied to date. This loss is thought to occur through transport pathways previously demonstrated to be involved with routine osmoregulation in marine teleosts. The main objective of this study was to characterize the intestinal transport physiology of the gulf toadfish (Opsanus beta) when exposed to varied levels of CO2: control, 5,000, 10,000, and 20,000 μatm CO2 (0.04, 0.5, 1, and 2 kPa, respectively). Results of this study suggest that intestinal apical anion exchange is highly responsive to hypercarbia, evidenced by a dose-dependent increase in intestinal luminal HCO3(-) (mmol L(-1)) that was mirrored by a reduction in Cl(-) (mmol L(-1)). Despite activation of HCO3(-) transport pathways typically used during osmoregulation, fractional fluid absorption was only significantly lower at the highest level of CO2. Although increased HCO3(-) excretion could provide more substrate for intestinally produced carbonates, carbonate production was not significantly increased during hypercarbia at the levels tested. This study is among the first to thoroughly characterize how compensation for elevated CO2 affects transport physiology and carbonate production in the marine fish intestine. This deeper understanding may be particularly relevant when considering the impacts of future predicted ocean acidification, where prolonged base loss may alter the energetic cost of acid-base balance or osmoregulation in marine fish.

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

“…The demand to secrete HCO 3 − in the intestine to maintain water balance is well-conserved across marine teleosts 30 . Increased intestinal HCO 3 − secretion with CO 2 exposure as reported here has also been demonstrated at higher CO 2 levels in the plainfin midshipmen (~50,000 μatm CO 2 ) 46 , in the toadfish (5000–20,000 μatm CO 2 ) 23 , and suggested from gene expression and/or protein assays in the Japanese ricefish (7000 μatm CO 2 ) 34 and the Atlantic cod (1,200 and 2,200 μatm CO 2 ) 41 . These studies suggest that increased intestinal HCO 3 − secretion and metabolic demand during CO 2 exposure could be a ubiquitous response to elevated CO 2 throughout marine bony fishes.…”

“…Finally, intestinal HCO 3 − secretion results in formation and excretion of CaCO 3 by marine fish which amounts to at least 3–15% of the marine inorganic CaCO 3 production 24 . Although a study on the toadfish reported unaltered CaCO 3 excretion rates 22 at 1900 μatm a more recent study on toadfish 23 and an earlier study on midshipmen 46 may suggest otherwise. Thus, increased intestinal HCO 3 − loss at elevated CO 2 in other species may impact the magnitude of this globally important calcification process, a possibility worthy of further study.…”

“…More targeted estimates of ion transport using specific isolated organs suggest that the gills and intestine account for ~4% 20 and 5.6% 21 of standard metabolic rate, respectively, which combined would account for about 10% of whole-animal standard metabolic rate. Interestingly, despite the need for HCO 3 − retention during a CO 2 -induced acidosis, toadfish experience ~34% increase in HCO 3 − ion loss through the intestine when exposed to near-future CO 2 scenarios (1900 μatm CO 2 ) 22 , a trend also apparent at higher CO 2 levels 23 . Although the intestine is a metabolically active tissue central to water balance and survival in seawater, the functional consequence of this relatively high HCO 3 − loss during CO 2 acclimation has not been examined.…”

Phase heterogeneity in carbonate production by marine fish influences their roles in sediment generation and the inorganic carbon cycle

“…In part, changes could relate to rising levels of atmospheric CO 2 and subsequent elevations in surface seawater temperatures and pCO 2 , both of which are predicted to stimulate increased carbonate production rates at the level of individual fish 1 , albeit effects remain to be fully quantified 45 . Such a response would contrast with that predicted for many other calcifying organisms under elevated pCO 2 46 , and it is possible that fish will contribute an increasingly large proportion of total marine carbonate under future climate change scenarios.…”

“…Tank floor recovery is a widely adopted approach to sampling piscine gut carbonates 8, 12–14, 22, 45 but other methods include direct sampling from the intestinal tract (following animal euthanasia) 8, 22, 45 and collection in a surgically attached rectal sac 45 . Direct sampling from the intestine was unsuitable here for two reasons.…”