Ocean Acidification Leads to Counterproductive Intestinal Base Loss in the Gulf Toadfish (Opsanus beta)

Oceanic CO2 has increased from 280 to 380 μatm since preindustrial times and is expected to reach 1,900 μatm by 2300. In addition, regional upwelling zones exhibit levels up to 2,300 μatm, making exploration at future global projected CO2 levels ecologically relevant today. Recent work has demonstrated that CO2 exposure as low as 1,000 μatm induces acidosis in toadfish (Opansus beta), leading to metabolic compensation by retention of blood in an effort to defend pH. Since increased serosal translates to increased secretion rates in isolated intestinal tissue, we predicted that blood elevation of and Pco2 during exposure to 1,900 μatm CO2 would increase in vivo base secretion rates. Rectal fluid and CaCO3 excretions were collected from toadfish exposed to 380 (control) and 1,900 μatm CO2 for 72 h. Fluids were analyzed for pH, osmolality, ionic composition, and total CO2. Precipitated CaCO3 was analyzed for titratable alkalinity, Mg2+, and Ca2+ content. Fish exposed to 1,900 μatm CO2 exhibited higher rectal base excretion rates, higher rectal fluid (mmol L−1), and lower fluid Cl− (mmol L−1) than controls, suggesting increased intestinal anion exchange as a result of the compensated respiratory acidosis. This study verifies that imminent projected CO2 levels expected by the year 2300 lead to greater intestinal loss, a process that acts against compensation for a CO2-induced acidosis.

[1]  M. Grosell,et al.  Impacts of ocean acidification on respiratory gas exchange and acid–base balance in a marine teleost, Opsanus beta , 2012, Journal of Comparative Physiology B.

[2]  G. Nilsson,et al.  Near-future carbon dioxide levels alter fish behaviour by interfering with neurotransmitter function , 2012, Nature Climate Change.

[3]  S. Simpson,et al.  Ocean acidification erodes crucial auditory behaviour in a marine fish , 2011, Biology Letters.

[4]  S. Guffey,et al.  Regulation of apical H⁺-ATPase activity and intestinal HCO₃⁻ secretion in marine fish osmoregulation. , 2011, American journal of physiology. Regulatory, integrative and comparative physiology.

[5]  Steven E. Lohrenz,et al.  Acidification of subsurface coastal waters enhanced by eutrophication , 2011 .

[6]  C. Langdon,et al.  Ocean acidification impacts multiple early life history processes of the Caribbean coral Porites astreoides , 2011 .

[7]  M. Grosell Intestinal Anion Exchange in Marine Teleosts Is Involved in Osmoregulation and Contributes to the Oceanic Inorganic Carbon Cycle , 2022 .

[8]  P. Munday,et al.  Effect of ocean acidification on otolith development in larvae of a tropical marine fish , 2011 .

[9]  Howard L. Jelks,et al.  Fish as major carbonate mud producers and missing components of the tropical carbonate factory , 2011, Proceedings of the National Academy of Sciences.

[10]  P. Munday,et al.  Ocean acidification does not affect the early life history development of a tropical marine fish. , 2011 .

[11]  A. Farrell,et al.  The multifunctional gut of fish , 2011 .

[12]  J. Whittamore Osmoregulation and epithelial water transport: lessons from the intestine of marine teleost fish , 2011, Journal of Comparative Physiology B.

[13]  M. Byrne,et al.  Unshelled abalone and corrupted urchins: development of marine calcifiers in a changing ocean , 2011, Proceedings of the Royal Society B: Biological Sciences.

[14]  C. Faggio,et al.  Carbonate precipitates and bicarbonate secretion in the intestine of sea bass, Dicentrarchus labrax , 2010, Journal of Comparative Physiology B.

[15]  A. Körtzinger,et al.  Calcifying invertebrates succeed in a naturally CO 2 -rich coastal habitat but are threatened by high levels of future acidification , 2010 .

[16]  U. Riebesell,et al.  Impact of ocean acidification and elevated temperatures on early juveniles of the polar shelled pteropod Limacina helicina: mortality, shell degradation, and shell growth , 2010 .

[17]  Richard A. Feely,et al.  The combined effects of ocean acidification, mixing, and respiration on pH and carbonate saturation in an urbanized estuary , 2010 .

[18]  S. Perry,et al.  Acid–base regulation in the plainfin midshipman (Porichthys notatus): an aglomerular marine teleost , 2010, Journal of Comparative Physiology B.

[19]  W. Landman Climate change 2007: the physical science basis , 2010 .

[20]  H. Pörtner,et al.  Cuttlebone calcification increases during exposure to elevated seawater pCO2 in the cephalopod Sepia officinalis , 2010 .

[21]  R. Wilson,et al.  HCO (3)(-) secretion and CaCO3 precipitation play major roles in intestinal water absorption in marine teleost fish in vivo. , 2010, American journal of physiology. Regulatory, integrative and comparative physiology.

[22]  E. Mager,et al.  Basolateral NBCe1 plays a rate-limiting role in transepithelial intestinal HCO3– secretion, contributing to marine fish osmoregulation , 2010, Journal of Experimental Biology.

[23]  P. Munday,et al.  Ocean acidification disrupts the innate ability of fish to detect predator olfactory cues. , 2010, Ecology letters.

[24]  Kimberly K. Yates,et al.  Coral Reefs and Ocean Acidification , 2009 .

[25]  E. Mager,et al.  High rates of HCO3– secretion and Cl– absorption against adverse gradients in the marine teleost intestine: the involvement of an electrogenic anion exchanger and H+-pump metabolon? , 2009, Journal of Experimental Biology.

[26]  C. Brauner,et al.  Patterns of Acid–Base Regulation During Exposure to Hypercarbia in Fishes , 2009 .

[27]  V. Matey,et al.  Complete intracellular pH protection during extracellular pH depression is associated with hypercarbia tolerance in white sturgeon, Acipenser transmontanus. , 2009, American journal of physiology. Regulatory, integrative and comparative physiology.

[28]  R. Asch,et al.  Elevated CO2 Enhances Otolith Growth in Young Fish , 2009, Science.

[29]  Scott C. Doney,et al.  Ocean acidification: the other CO2 problem. , 2009, Annual review of marine science.

[30]  K. Døving,et al.  Ocean acidification impairs olfactory discrimination and homing ability of a marine fish , 2009, Proceedings of the National Academy of Sciences.

[31]  V. Christensen,et al.  Contribution of Fish to the Marine Inorganic Carbon Cycle , 2009, Science.

[32]  M. Hayashi,et al.  Long-term effects of predicted future seawater CO2 conditions on the survival and growth of the marine shrimp Palaemon pacificus , 2008 .

[33]  A. Farrell,et al.  Physiology and Climate Change , 2008, Science.

[34]  Stephen Widdicombe,et al.  Ocean acidification may increase calcification rates, but at a cost , 2008, Proceedings of the Royal Society B: Biological Sciences.

[35]  M. Grosell,et al.  Effects of salinity on intestinal bicarbonate secretion and compensatory regulation of acid–base balance in Opsanus beta , 2008, Journal of Experimental Biology.

[36]  M. Grosell,et al.  Basolateral NBC is the hinge of a mechanism serving both osmoregulation and acid-base balance in the marine teleost intestine , 2008 .

[37]  R. Feely,et al.  Evidence for Upwelling of Corrosive "Acidified" Water onto the Continental Shelf , 2008, Science.

[38]  Richard A. Feely,et al.  Impacts of ocean acidification on marine fauna and ecosystem processes , 2008 .

[39]  S. Perry,et al.  Intestinal carbonic anhydrase, bicarbonate, and proton carriers play a role in the acclimation of rainbow trout to seawater. , 2007, American journal of physiology. Regulatory, integrative and comparative physiology.

[40]  S. Perry,et al.  Is urea pulsing in toadfish related to environmental O2 or CO2 levels? , 2007, Comparative biochemistry and physiology. Part A, Molecular & integrative physiology.

[41]  K. Yates,et al.  Diurnal variation of oxygen and carbonate system parameters in Tampa Bay and Florida Bay , 2007 .

[42]  H. L. Miller,et al.  Global climate projections , 2007 .

[43]  S. Perry,et al.  Acid–base balance and CO2 excretion in fish: Unanswered questions and emerging models , 2006, Respiratory Physiology & Neurobiology.

[44]  M. Grosell Intestinal anion exchange in marine fish osmoregulation , 2006, Journal of Experimental Biology.

[45]  M. Grosell,et al.  Ouabain-sensitive bicarbonate secretion and acid absorption by the marine teleost fish intestine play a role in osmoregulation. , 2006, American journal of physiology. Regulatory, integrative and comparative physiology.

[46]  E. Maier‐Reimer,et al.  Anthropogenic ocean acidification over the twenty-first century and its impact on calcifying organisms , 2005, Nature.

[47]  F. Jensen,et al.  Bicarbonate secretion plays a role in chloride and water absorption of the European flounder intestine. , 2005, American journal of physiology. Regulatory, integrative and comparative physiology.

[48]  K. Choe,et al.  The multifunctional fish gill: dominant site of gas exchange, osmoregulation, acid-base regulation, and excretion of nitrogenous waste. , 2005, Physiological reviews.

[49]  Takashi Kikkawa,et al.  Effects of CO2 on Marine Fish: Larvae and Adults , 2004 .

[50]  U. Riebesell Effects of CO2 Enrichment on Marine Phytoplankton , 2004 .

[51]  H. Pörtner,et al.  Biological Impact of Elevated Ocean CO2 Concentrations: Lessons from Animal Physiology and Earth History , 2004 .

[52]  K. Caldeira,et al.  Oceanography: Anthropogenic carbon and ocean pH , 2003, Nature.

[53]  C. Wood,et al.  Branchial and renal handling of urea in the gulf toadfish, Opsanus beta: the effect of exogenous urea loading. , 2003, Comparative biochemistry and physiology. Part A, Molecular & integrative physiology.

[54]  P. B. Duffy,et al.  Anthropogenic carbon and ocean pH , 2001 .

[55]  Ulf Riebesell,et al.  Reduced calcification of marine plankton in response to increased atmospheric CO2 , 2000, Nature.

[56]  J. Serafy,et al.  Field studies on the ureogenic gulf toadfish in a subtropical bay. I. Patterns of abundance, size composition and growth , 1997 .

[57]  F. Jensen,et al.  Extra- and intracellular acid-base balance and ionic regulation in cod (Gadus morhua ) during combined and isolated exposures to hypercapnia and copper , 1997 .

[58]  Gilmour,et al.  Intestinal base excretion in the seawater-adapted rainbow trout: a role in acid-base balance? , 1996, The Journal of experimental biology.

[59]  Ando,et al.  Intestinal Na+ and Cl- levels control drinking behavior in the seawater-adapted eel Anguilla japonica , 1996, The Journal of experimental biology.

[60]  D. Evans,et al.  Acid-base balance and ion transfers in the spiny dogfish (Squalus acanthias) during hypercapnia : A role for ammonia excretion , 1992 .

[61]  P. Walsh,et al.  Carbonate deposits in marine fish intestines: A new source of biomineralization , 1991 .

[62]  E. Skadhauge,et al.  Coupling of transmural flows of NaCl and water in the intestine of the eel (Anguilla anguilla). , 1974, The Journal of experimental biology.

[63]  Homer W. Smith THE ABSORPTION AND EXCRETION OF WATER AND SALTS BY MARINE TELEOSTS , 1930 .