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Journal of Comparative Physiology B

, Volume 188, Issue 3, pp 421–435 | Cite as

Dropping the base: recovery from extreme hypercarbia in the CO2 tolerant Pacific hagfish (Eptatretus stoutii)

  • Alexander M. CliffordEmail author
  • Alyssa M. Weinrauch
  • Greg G. Goss
Original Paper

Abstract

Hagfish are capable of tolerating extreme hypercapnia (> 30 Torr) by mounting substantial plasma [HCO3] (hypercarbia) to compensate for CO2-mediated acidosis. The goal of this study was to characterize the mechanistic hypercarbia-recovery strategies in the highly CO2 tolerant hagfish. We exposed hagfish to hypercapnia (30 Torr) for 48 h and allowed a 24 h recovery period in normocapnic seawater. Within 8 h of the recovery period, the compensatory plasma [HCO3] load (~ 70 mmol L−1) was rapidly offloaded. While increases in both whole-animal HCO3 excretion and glomerular filtration were observed throughout recovery (2–8 h), neither can fully account for the observed rates of whole-animal HCO3 loss, which peaked at ~ 3.5 mmol kg−1 h−1. Inhibition of carbonic anhydrase via acetazolamide revealed that the restoration of plasma [HCO3] from hypercapnia-induced hypercarbia is likely facilitated in a dualistic manner, initially relying on both carbonic anhydrase mediated CO2 offloading and Cl/HCO3 exchange processes, both of which are likely either upregulated or further activated as recovery progresses.

Keywords

Cyclostome Agnatha Carbonic anhydrase Hypercapnia 

Notes

Acknowledgements

We thank Dr. Eric Clellend for his unwavering diligence in supporting this research, the BMSC Foreshore staff for their aid in obtaining research animals and Dr. Chris Wood for experimental advice.

Funding

A.M.C. was supported by an NSERC- PGSD, Alberta Innovates Technology Futures—Omics Scholarship, President’s Doctoral Prize of Distinction, Donald M. Ross Memorial Scholarship, R. E. (Dick) Peter Memorial Scholarship, Andrew Stewart Memorial Prize, Western Canadian Universities Marine Sciences Society Graduate Student Award and the Dick and Leona Peter BMSC residential bursary. A.M.W was supported by a NSERC-PGSD, The Presidents Doctoral Prize of Distinction, Queen Elizabeth II Scholarship, Sigurd Tviet Memorial Scholarship, Dick and Leona Peter BMSC Residential bursary and the John Boom Scholarship. This research was supported by an NSERC Discovery Grant (203736) to GGG.

References

  1. Alper SL, Chernova MN, Stewart AK (2001) Regulation of Na+-independent Cl/HCO3 exchangers by pH. JOP 2:171–175PubMedGoogle Scholar
  2. Alt JM, Stolte H, Eisenbach GM, Walvig F (1981) Renal electrolyte and fluid excretion in the Atlantic hagfish Myxine glutinosa. J Exp Biol 91:323–330Google Scholar
  3. Axelsson M, Farrell AP, Nilsson S (1990) Effects of hypoxia and drugs on the cardiovascular dynamics of the Atlantic hagfish Myxine glutinosa. J Exp Biol 151:297–316Google Scholar
  4. Baker DW, Matey V, Huynh KT et al (2009) Complete intracellular pH protection during extracellular pH depression is associated with hypercarbia tolerance in white sturgeon, Acipenser transmontanus. Am J Physiol Regul Integr Comp Physiol 296:R1868–R1880.  https://doi.org/10.1152/ajpregu.90767.2008 CrossRefPubMedGoogle Scholar
  5. Baker DW, Sardella B, Rummer JL et al (2015) Hagfish: champions of CO2 tolerance question the origins of vertebrate gill function. Sci Rep 5:11182.  https://doi.org/10.1038/srep11182 CrossRefPubMedPubMedCentralGoogle Scholar
  6. Bornancin M, De Renzis G, Maetz J (1977) Branchial Cl transport, anion-stimulated ATPase and acid–base balance in Anguilla anguilla adapted to freshwater: effects of hyperoxia. J Comp Physiol-B 117:313–322.  https://doi.org/10.1007/BF00691557 CrossRefGoogle Scholar
  7. Boutilier RG, Heming TA, Iwama GK (1984) Appendix: physicochemical parameters for use in fish respiratory physiology. In: Hoar WS, Randall D (eds) Gills—anatomy, gas transfer, and acid–base regulation. Elsevier, Orlando, pp 403–430CrossRefGoogle Scholar
  8. Braun MH, Perry SF (2010) Ammonia and urea excretion in the Pacific hagfish Eptatretus stoutii: evidence for the involvement of Rh and UT proteins. Comp Biochem Physiol A 157:405–415CrossRefGoogle Scholar
  9. Cameron JN, Iwama GK (1987) Compensation of progressive hypercapnia in channel catfish and blue crabs. J Exp Biol 133:183–197Google Scholar
  10. Clifford AM, Guffey SC, Goss GG (2014) Extrabranchial mechanisms of systemic pH recovery in hagfish (Eptatretus stoutii). Comp Biochem Physiol A 168:82–89.  https://doi.org/10.1016/j.cbpa.2013.11.009 CrossRefGoogle Scholar
  11. Clifford AM, Goss GG, Roa JN, Tresguerres M (2015a) Acid/base and ionic regulation in hagfish. Hagfish Biol.  https://doi.org/10.1201/b18935-12 Google Scholar
  12. Clifford AM, Goss GG, Wilkie MP (2015b) Adaptations of a deep sea scavenger: high ammonia tolerance and active NH4 + excretion by the Pacific hagfish (Eptatretus stoutii). Comp Biochem Physiol A 182C:64–74.  https://doi.org/10.1016/j.cbpa.2014.12.010 CrossRefGoogle Scholar
  13. Clifford AM, Zimmer AM, Wood CM, Goss GG (2016) It’s all in the gills: evaluation of O2 uptake in Pacific hagfish refutes a major respiratory role for the skin. J Exp Biol 219:2814–2818.  https://doi.org/10.1242/jeb.141598 CrossRefPubMedGoogle Scholar
  14. Clifford AM, Bury NR, Schultz AG et al (2017a) Regulation of plasma glucose and sulfate excretion in Pacific hagfish, Eptatretus stoutii is not mediated by 11-deoxycortisol. Gen Comp Endocrinol 247:107–115.  https://doi.org/10.1016/j.ygcen.2017.01.022 CrossRefPubMedGoogle Scholar
  15. Clifford AM, Weinrauch AM, Edwards SL et al (2017b) Flexible ammonia handling strategies using both cutaneous and branchial epithelia in the highly ammonia tolerant Pacific hagfish. Am J Physiol Regul Integr Comp Physiol 313:R78–R90.  https://doi.org/10.1152/ajpregu.00351.2016 CrossRefPubMedGoogle Scholar
  16. Cox GK, Sandblom E, Richards JG, Farrell AP (2011) Anoxic survival of the Pacific hagfish (Eptatretus stoutii). J Comp Physiol B 181:361–371CrossRefPubMedGoogle Scholar
  17. Crocker CE, Cech JJ Jr (1998) Effects of hypercapnia on blood-gas and acid–base status in the white sturgeon, Acipenser transmontanus. J Comp Physiol B 168:50–60.  https://doi.org/10.1007/s003600050120 CrossRefGoogle Scholar
  18. Damsgaard C, Gam LTH, Tuong DD et al (2015) High capacity for extracellular acid–base regulation in the air-breathing fish Pangasianodon hypophthalmus. J Exp Biol 218:1290–1294.  https://doi.org/10.1242/jeb.117671 CrossRefPubMedGoogle Scholar
  19. Edsall JT (1968) Carbon dioxide, carbonic acid and bicarbonate ion: physical properties and kinetics of interconversion. CO2: chemical, biochemical, and physiological aspects. NASA SP 188:15–27Google Scholar
  20. Ellory JC, Wolowyk MW, Young JD (1987) Hagfish (Eptatretus stouti) erythrocytes show minimal chloride transport activity. J Exp Biol 129:377–383PubMedGoogle Scholar
  21. Esbaugh AJ, Gilmour KM, Perry SF (2009) Membrane-associated carbonic anhydrase in the respiratory system of the Pacific hagfish (Eptatretus stouti). Respir Physiol Neurobiol 166:107–116.  https://doi.org/10.1016/j.resp.2009.02.005 CrossRefPubMedGoogle Scholar
  22. Evans DH (1984) Gill Na+/H+ and Cl/HCO3 exchange systems evolved before the vertebrates entered fresh water. J Exp Biol 113:465–469PubMedGoogle Scholar
  23. Forster ME, Davison W, Axelsson M, Farrell AP (1992) Cardiovascular responses to hypoxia in the hagfish, Eptatretus cirrhatus. Resp Physiol 88:373–386.  https://doi.org/10.1016/0034-5687(92)90010-T CrossRefGoogle Scholar
  24. Forster ME, Russell MJ, Hambleton DC, Olson KR (2001) Blood and extracellular fluid volume in whole body and tissues of the Pacific hagfish, Eptatretus stoutii. Physiol Biochem Zool 74:750–756.  https://doi.org/10.1086/323032 CrossRefPubMedGoogle Scholar
  25. Gilmour KM, Perry SF (2004) Branchial membrane-associated carbonic anhydrase activity maintains CO2 excretion in severely anemic dogfish. Am J Physiol Regul Integr Comp Physiol 286:R1138–R1148.  https://doi.org/10.1152/ajpregu.00219.2003 CrossRefPubMedGoogle Scholar
  26. Gilmour KM, Henry RP, Wood CM, Perry SF (1997) Extracellular carbonic anhydrase and an acid–base disequilibrium in the blood of the dogfish Squalus acanthias. J Exp Biol 200:173–183PubMedGoogle Scholar
  27. Glover C, Bucking C, Wood C (2011) Adaptations to in situ feeding: novel nutrient acquisition pathways in an ancient vertebrate. Proc R Soc B 278:3096–3101.  https://doi.org/10.1098/rspb.2010.2784 CrossRefPubMedPubMedCentralGoogle Scholar
  28. Goss GG, Perry SF (1994) Different mechanisms of acid–base regulation in rainbow trout (Oncorhynchus mykiss) and American eel (Anguilla rostrata) during NaHCO3 infusion. Physiol Zool 67:381–406.  https://doi.org/10.2307/30163854?ref=search-gateway:dba53bba673c16586f69c61e2431155b CrossRefGoogle Scholar
  29. Heisler N (1986) Acid-base regulation in fishes. In: Heisler N (ed) Acid-base regulation in animals. Elsevier Biomedical Press, Amsterdam, pp 309–356Google Scholar
  30. Heisler N, Weitz AM (1976) Extracellular and intracellular pH with changes of temperature in the dogfish Scyliorhinus stellaris. Respir Physiol Neurobiol 26:249–263CrossRefGoogle Scholar
  31. Hobe H, Wood CM, Wheatly MG (1984) The mechanisms of acid–base and ionoregulation in the freshwater rainbow trout during environmental hyperoxia and subsequent normoxia. I. Extra- and intracellular acid–base status. Respir Physiol Neurobiol 55:139–154CrossRefGoogle Scholar
  32. Hyde DA, Perry SF (1987) Acid–base and ionic regulation in the American eel (Anguilla rostrata) during and after prolonged aerial exposure: branchial and renal adjustments. J Exp Biol 133:429–447Google Scholar
  33. Hyde DA, Perry SF (1989) Differential approaches to blood acid–base regulation during exposure to prolonged hypercapnia in two freshwater teleosts: the rainbow trout (Salmo gairdneri) and the American eel (Anguilla rostrata). Physiol Zool 62:1164–1186.  https://doi.org/10.2307/30156207?ref=search-gateway:51d91158b4023192f9ccb99be60cba25 CrossRefGoogle Scholar
  34. Jensen FB, Nikinmaa M, Weber RE (1993) Environmental perturbations of oxygen transport in teleost fishes: causes, consequences and compensations. In: Rankin JC, Jensen FB (eds) Fish Ecophysiol. Chapman & Hall, Dordrecht, pp 161–179Google Scholar
  35. Kirsch R (1972) The kinetics of peripheral exchanges of water and electrolytes in the Silver eel (Anguilla Anguilla L.) in fresh water and in sea water. J Exp Biol 57:489–512Google Scholar
  36. Larsen BK, Jensen FB (1997) Influence of ionic composition on acid–base regulation in rainbow trout (Oncorhynchus mykiss) exposed to environmental hypercapnia. Fish Physiol Biochem 16:157–170.  https://doi.org/10.1007/BF00004672 CrossRefGoogle Scholar
  37. Martini FH (1998) The ecology of hagfishes. In: Jørgensen JM, Lomholt JP, Weber RE, Malte H  (eds) The biology of hagfishes. Springer, Dordrecht, pp 57–77CrossRefGoogle Scholar
  38. McDonald DG, Cavdek V, Calvert L, Milligan CL (1991) Acid–base regulation in the Atlantic hagfish Myxine glutinosa. J Exp Biol 161:201–215Google Scholar
  39. Morris R (1965) Studies on salt and water balance in Myxine glutinosa (L.). J Exp Biol 42:359–371Google Scholar
  40. Munger RS, Reid SD, Wood CM (1991) Extracellular fluid volume measurements in tissues of the rainbow trout (Oncorhynchus mykiss) in vivo and their effects on intracellular pH and ion calculations. Fish Physiol Biochem 9:313–323.  https://doi.org/10.1007/BF02265152 CrossRefPubMedGoogle Scholar
  41. Parks SK, Tresguerres M, Goss GG (2007) Blood and gill responses to HCl infusions in the Pacific hagfish (Eptatretus stoutii). Can J Zool 85:855–862.  https://doi.org/10.1139/Z07-068 CrossRefGoogle Scholar
  42. Perry SF (2011) Carbon dioxide excretion in fishes. Can J Zool.  https://doi.org/10.1139/z86-083 Google Scholar
  43. Perry SF, Gilmour KM, Bernier NJ, Wood CM (1999) Does gill boundary layer carbonic anhydrase contribute to carbon dioxide excretion: a comparison between dogfish (Squalus acanthias) and rainbow trout (Oncorhynchus mykiss). J Exp Biol 202:749–756PubMedGoogle Scholar
  44. Peters T, Forster RE, Gros G (2000) Hagfish (Myxine glutinosa) red cell membrane exhibits no bicarbonate permeability as detected by 18O exchange. J Exp Biol 203:1551–1560.  https://doi.org/10.1002/jez.1402640104 PubMedGoogle Scholar
  45. Rahn H, Reeves RB, Howell BJ (1975) Hydrogen ion regulation, temperature, and evolution. Am Rev Respir Dis 112:165–172.  https://doi.org/10.1164/arrd.1975.112.2.165 PubMedGoogle Scholar
  46. Read LJ (1975) Absence of ureogenic pathways in liver of the hagfish Bdellostoma cirrhatum. Comp Biochem Physiol Part B 51:139–141.  https://doi.org/10.1016/0305-0491(75)90372-7 CrossRefGoogle Scholar
  47. Schultz AG, Guffey SC, Clifford AM, Goss GG (2014) Phosphate absorption across multiple epithelia in the Pacific hagfish (Eptatretus stoutii). Am J Physiol Regul Integr Comp Physiol 307:R643–R652.  https://doi.org/10.1152/ajpregu.00443.2013 CrossRefPubMedPubMedCentralGoogle Scholar
  48. Smith CR, Baco AR (2003) Ecology of whale falls at the deep-sea floor. Oceanogr Mar Biol 41:311–354Google Scholar
  49. Stewart PA (1981) How to understand acid–base: a quantitative acid–base primer for biology and medicine. Elsivier, New YorkGoogle Scholar
  50. Stewart PA (1983) Modern quantitative acid–base chemistry. Can J Physiol Pharmacol 61:1444–1461CrossRefPubMedGoogle Scholar
  51. Tresguerres M, Parks SK, Goss GG (2007) Recovery from blood alkalosis in the Pacific hagfish (Eptatretus stoutii): Involvement of gill V-H+-ATPase and Na+/K+-ATPase. Comp Biochem Physiol A 148:133–141CrossRefGoogle Scholar
  52. Verdouw H, Van Echteld C, Dekkers E (1978) Ammonia determination based on indophenol formation with sodium salicylate. Water Res 12:399–402CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2017

Authors and Affiliations

  • Alexander M. Clifford
    • 1
    • 2
    • 3
    Email author
  • Alyssa M. Weinrauch
    • 1
    • 2
  • Greg G. Goss
    • 1
    • 2
  1. 1.Department of Biological SciencesUniversity of AlbertaEdmontonCanada
  2. 2.Bamfield Marine Sciences CentreBamfieldCanada
  3. 3.Department of ZoologyUniversity of British ColumbiaVancouverCanada

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