Ocean warming and acidification modulate energy budget and gill ion regulatory mechanisms in Atlantic cod (Gadus morhua)

Abstract

Ocean warming and acidification are threatening marine ecosystems. In marine animals, acidification is thought to enhance ion regulatory costs and thereby baseline energy demand, while elevated temperature also increases baseline metabolic rate. Here we investigated standard metabolic rates (SMR) and plasma parameters of Atlantic cod (Gadus morhua) after 3–4 weeks of exposure to ambient and future PCO2 levels (550, 1200 and 2200 µatm) and at two temperatures (10, 18 °C). In vivo branchial ion regulatory costs were studied in isolated, perfused gill preparations. Animals reared at 18 °C responded to increasing CO2 by elevating SMR, in contrast to specimens at 10 °C. Isolated gills at 10 °C and elevated PCO2 (≥1200 µatm) displayed increased soft tissue mass, in parallel to increased gill oxygen demand, indicating an increased fraction of gill in whole animal energy budget. Altered gill size was not found at 18 °C, where a shift in the use of ion regulation mechanisms occurred towards enhanced Na+/H+-exchange and HCO3− transport at high PCO2 (2200 µatm), paralleled by higher Na+/K+-ATPase activities. This shift did not affect total gill energy consumption leaving whole animal energy budget unaffected. Higher Na+/K+-ATPase activities in the warmth might have compensated for enhanced branchial permeability and led to reduced plasma Na+ and/or Cl− concentrations and slightly lowered osmolalities seen at 18 °C and 550 or 2200 µatm PCO2 in vivo. Overall, the gill as a key ion regulation organ seems to be highly effective in supporting the resilience of cod to effects of ocean warming and acidification.

Effects of ocean acidification on salinity tolerance and seawater growth of Atlantic salmon Salmo salar smolts

“…Thus, lower plasma chloride may be a common feature of the simultaneous exposure of euryhaline species to seawater and both moderate and severe hypercarbic conditions. In cod Gadus morhua L. 1758 plasma chloride was significantly lower after 4 weeks exposure to both 1200 and 2200 μatm CO 2 (Kreiss et al ., ), whereas in red drum Sciaenops ocellatus (L. 1766) there was no significant effect on plasma chloride after 2 weeks exposure to 1000 μatm CO 2 (Esbaugh et al ., ), while plasma Na + levels did not differ in either species.…”

Mucosal Barrier Functions of Fish under Changing Environmental Conditions

“…The interaction of CO 2 with other environmental variables, such as temperature and heavy metals, was also assessed in several studies. Hypercarbia at 10 • C resulted in an increase in gill tissue mass of Atlantic cod (Gadus morhua), but not at 18 • C [41]. The increase in size can be attributed to the response of fish to rapidly eliminate high CO 2 concentrations [42].…”

Water bicarbonate modulates the response of the shore crab Carcinus maenas to ocean acidification

“…Changing contributions of branchial H + -ATPase and Na + /K + -ATPases may translate into shifts in energy turnover and energy allocation (Pane and Barry 2007;Hu et al 2017). Changes in the activities and capacities of these transporters are difficult to quantify, but energetic implications due to life-style and environment have been discussed with respect to a species' resilience to OA and long-term performance (Pörtner et al 2000;Pane and Barry 2007;Kreiß et al 2015;Hu et al 2016;Michael et al 2016). Accordingly, a hypercapniainduced decrease in pH e led to a reduced rate of aerobic metabolism in S. nudus (Reipschläger and Pörtner 1996) by switching from the Na + /H + exchanger to the less energy consuming Na + -dependent Cl − /HCO 3 − exchanger (Pörtner et al 2000).…”