Skip to main content
SpringerLink
Log in

Nitrogen metabolism, acid–base regulation, and molecular responses to ammonia and acid infusions in the spiny dogfish shark (Squalus acanthias)

  • Original Paper
  • Published:
Journal of Comparative Physiology B Aims and scope Submit manuscript

Abstract

Although they are ureotelic, marine elasmobranchs express Rh glycoproteins, putative ammonia channels. To address questions raised by a recent study on high environmental ammonia (HEA) exposure, dogfish were intravascularly infused for 24 h at 3 ml kg−1 h−1 with isosmotic NaCl (500 mmol l−1, control), NH4HCO3 (500 mmol l−1), NH4Cl (500 mmol l−1), or HCl (as 125 mmol l−1 HCl + 375 mmol l−1 NaCl). While NaCl had no effect on arterial acid–base status, NH4HCO3 caused mild alkalosis, NH4Cl caused strong acidosis, and HCl caused lesser acidosis, all predominantly metabolic in nature. Total plasma ammonia (TAmm) and excretion rates of ammonia (J Amm) and urea-N (J Urea-N) were unaffected by NaCl or HCl. However, despite equal loading rates, plasma TAmm increased to a greater extent with NH4Cl, while J Amm increased to a greater extent with NH4HCO3 due to much greater increases in blood-to-water PNH3 gradients. As with HEA, both treatments caused large (90 %) elevations of J Urea-N, indicating that urea-N synthesis by the ornithine-urea cycle (OUC) is driven primarily by ammonia rather than HCO3 −. Branchial mRNA expressions of Rhbg and Rhp2 were unaffected by NH4HCO3 or NH4Cl, but v-type H +-ATPase was down-regulated by both treatments, and Rhbg and Na+/H+ exchanger NHE2 were up-regulated by HCl. In the kidney, Rhbg was unresponsive to all treatments, but Rhp2 was up-regulated by HCl, and the urea transporter UT was up-regulated by HCl and NH4Cl. These responses are discussed in the context of current ideas about branchial, renal, and OUC function in this nitrogen-limited predator.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Anderson WG, Dasiewicz PJ, Liban S, Ryan C, Taylor JR, Grosell M, Weihrauch D (2010) Gastro-intestinal handling of water and solutes in three species of elasmobranch fish, the white-spotted bamboo shark, Chiloscyllium plagiosum, little skate, Leucoraja erinacea, and the clear nose skate, Raja eglanteria. Comp Biochem Physiol 155A:493–502

    Article  CAS  Google Scholar 

  • Anderson WG, Nawata CM, Wood CM, Piercey-Normore MD, Weihrauch D (2012) Body fluid osmolytes and urea and ammonia flux in the colon of two chondrichthyan fishes, the ratfish, Hydrolagus colliei, and spiny dogfish, Squalus acanthias. Comp Biochem Physiol 161A:27–35

    Article  Google Scholar 

  • Atkinson DE (1992) Functional roles of urea synthesis in vertebrates. Physiol Zool 65:243–267

    CAS  Google Scholar 

  • Atkinson DE, Bourke E (1984) The role of ureagenesis in pH homeostasis. Trends Biochem Sci 9:297–300

    Article  CAS  Google Scholar 

  • Bakouh N, Benjelloun F, Hulin P, Brouillard F, Edelman A, Cherif-Zahar B, Planelles G (2004) NH3 is involved in the NH4 + transport induced by the functional expression of the human Rh C glycoprotein. J Biol Chem 279:15975–15983

    Article  CAS  PubMed  Google Scholar 

  • Ballantyne JS (1997) Jaws: the inside story. The metabolism of elasmobranch fishes. Comp Biochem Physiol 118B:703–742

    Article  CAS  Google Scholar 

  • Barimo JF, Steele SL, Wright PA, Walsh PJ (2004) The ontogeny of urea synthesis and excretion in the gulf toadfish, Opsanus beta. J Exp Biol 207:2011–2020

    Article  CAS  PubMed  Google Scholar 

  • Boutilier RG, Heming TA, Iwama GK (1984) Appendix: physicochemical parameters for use in fish respiratory physiology. In: Hoar WS, Randall DJ (eds) Fish physiology, vol 10A. Academic Press, Orlando, pp 403–430

    Google Scholar 

  • Boylan JW (1967) Gill permeability in Squalus acanthias. In: Gilbert PW, Mathewson RF, Rall DP (eds) Sharks, skates and rays. Johns Hopkins Press, Baltimore, pp 197–206

    Google Scholar 

  • Bustin SA (2000) Absolute quantification of mRNA using real-time reverse transcription polymerase chain reaction assays. J Mol Endocrinol 25:169–193

    Article  CAS  PubMed  Google Scholar 

  • Bustin SA (2002) Quantification of mRNA using real-time reverse transcription PCR (RT-PCR): trends and problems. J Mol Endocrinol 29:23–39

    Article  CAS  PubMed  Google Scholar 

  • Cameron JN, Heisler N (1983) Studies of ammonia in the trout: physicochemical parameters, acid–base behaviour and respiratory clearance. J Exp Biol 105:107–125

    CAS  Google Scholar 

  • Cameron JN, Kormanik GA (1982) The acid-base responses of gills and kidneys to infused acid and base loads in the channel catfish, Ictalurus punctatus. J Exp Biol 99:143–160

    CAS  PubMed  Google Scholar 

  • Choe KP, Kato A, Hirose S, Plata C, Sindic A, Romero MF, Claiborne JB, Evans DH (2005) NHE3 in an ancestral vertebrate: primary sequence, distribution, localization and function in gills. Am J Physiol 289:R1520–R1534

    CAS  Google Scholar 

  • Claiborne JB, Evans DH (1988) Ammonia and acid-base balance during high ammonia exposure in a marine teleost (Myoxocephalus octodecimspinosus). J Exp Biol 140:89–105

    CAS  Google Scholar 

  • Claiborne JB, Choe KP, Morrison-Shetlar AI, Weakley JC, Havird J, Freiji A, Evans DH, Edwards SL (2008) Molecular detection and immunological localization of gill Na+/H+ exchanger in the dogfish (Squalus acanthias). Am J Physiol 294:R1092–R1102

    CAS  Google Scholar 

  • Cooper AR, Morris S (2004) Osmotic, sodium, carbon dioxide, and acid-base state of the Port Jackson shark, Heterodontus portusjacksoni, in response to lowered salinity. J Comp Physiol B 174:211–222

    Article  CAS  PubMed  Google Scholar 

  • De Boeck G, Wood CM (2015) Does ammonia trigger hyperventilation in the elasmobranch Squalus acanthias suckleyi? Respir Physiol Neurobiol 206:25–35

    Article  PubMed  Google Scholar 

  • De Boeck G, Grosell M, Wood CM (2001) Sensitivity of the spiny dogfish (Squalus acanthias) to waterborne silver exposure. Aquat Toxicol 54:261–275

    Article  PubMed  Google Scholar 

  • Ebert DA, White WT, Goldman KJ, Compagno LJV, Daly-Engel TS, Ward RD (2010) Resurrection and redescription of Squalus suckleyi Girard from the North Pacific, with comments on the Squalus acanthias subgroup (Squaliformes: Squalidae). Zootaxa 2612:22–40

    Google Scholar 

  • Edwards SL, Donald JA, Toop T, Donowitz M, Tse CM (2002) NHE-like immunoreactivity in the gills of elasmobranchs. Comp Biochem Physiol 131:257–265

    Article  CAS  Google Scholar 

  • Endeward V, Cartron J-P, Ripoche G, Gros G (2006) Red cell membrane CO2 permeability in normal human blood and in blood deficient in various blood groups, and effect of DIDS. Transfus Clin Biol. 13:123–127

    Article  CAS  PubMed  Google Scholar 

  • Evans D (1982) Mechanisms of acid extrusion by two marine fishes: the teleost, Opsanus beta, and the elasmobranch, Squalus acanthias. J Exp Biol 97:289–299

    CAS  Google Scholar 

  • Evans DH, More KJ (1988) Modes of ammonia transport across the gill epithelium of the dogfish pup (Squalus acanthias). J Exp Biol 138:375–397

    CAS  Google Scholar 

  • Fines GA, Ballantyne JS, Wright PA (2001) Active urea transport and an unusual basolateral membrane composition in the gills of a marine elasmobranch. Am J Physiol 280:R16–R24

    CAS  Google Scholar 

  • Haywood GP (1973) Hypo-osmotic regulation coupled with reduced metabolic urea in the dogfish Poraderma africanum: an analysis of serum osmolality, chloride, and urea. Mar Biol 23:121–127

    Article  CAS  Google Scholar 

  • Huang C-H, Peng J (2005) Evolutionary conservation and diversification of Rh family genes and proteins. Proc Natl Acad Sci USA 102:15512–15517

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Kajimura M, Walsh PJ, Mommsen TP, Wood CM (2006) The dogfish shark (Squalus acanthias) activates both hepatic and extra-hepatic ornithine urea cycle enzyme activities for nitrogen conservation after feeding. Physiol Biochem Zool 79:602–613

    Article  CAS  PubMed  Google Scholar 

  • Kajimura M, Walsh PJ, Wood CM (2008) The dogfish shark (Squalus acanthias) maintains its osmolytes during long term starvation. J Fish Biol 72:656–670

    Article  CAS  Google Scholar 

  • King PA, Goldstein L (1983) Renal ammoniagenesis and acid excretion in the dogfish, Squalus acanthias. Am J Physiol 245:R581–R589

    CAS  PubMed  Google Scholar 

  • Klein JD, Rouillard P, Roberts BR, Sands JM (2002) Acidosis mediates the upregulation of UT-A protein in livers from uremic rats. J Am Soc Nephrol 13:581–587

    CAS  PubMed  Google Scholar 

  • Kustu S, Inwood W (2006) Biological gas channels for NH3 and CO2: evidence that Rh (Rhesus) proteins are CO2 channels. Transfus Clin Biol 13:103–110

    Article  CAS  PubMed  Google Scholar 

  • Lu Z, Gui H, Yao L, Yan L, Martens H, Aschenbach JR, Shen Z (2014) Short-chain fatty acids and acidic pH up-regulate UT-B, GPR41, and GPR4 in rumen epithelial cells of goats. Am J Physiol. doi:10.1152/ajpregu.00323.2014

    Google Scholar 

  • Marini A-M, Matassi G, Raynal V, André B, Cartron J-P, Chérif-Zahar B (2000) The human Rhesus-associated RhAG protein and a kidney homologue promote ammonium transport in yeast. Nat Genet 26:341–344

    Article  CAS  PubMed  Google Scholar 

  • Maxime V, Peyraud-Waitzenegger M, Claireaux G, Peyraud C (1990) Effects of rapid transfer from sea water to fresh water on respiratory variables, blood acid-base status and O2 affinity of haemoglobin in Atlantic salmon (Salmo salar L.). J Comp Physiol 160B:31–39

    Google Scholar 

  • McDonald DG, Prior ET (1988) Branchial mechanisms of ion and acid- base regulation in the freshwater rainbow trout Salmo gairdneri. Can J Zool 66:2699–2708

    Article  CAS  Google Scholar 

  • Milligan CL, McDonald DG, Prior T (1991) Acid and ammonia fluxes in response to alkalosis and acidosis in two marine teleosts: coho salmon (Oncorhynchus kisutch) and starry flounder (Platichthys stellatus). Physiol Zool 64:169–192

    Google Scholar 

  • Mondzac A, Ehrlich GE, Seegmiller JE (1965) An enzymatic determination of ammonia in biological fluids. J Lab Clin Med 66:526–531

    CAS  PubMed  Google Scholar 

  • Mouro-Chanteloup I, Cochet S, Chami M, Genetet S, Zidi-Yahiaoui N, Engel A, Colin Y, Bertrand O, Ripoche P (2010) Functional reconstitution into liposomes of purified human RhCG ammonia channel. PLoS One 5:e8921

    Article  PubMed Central  PubMed  Google Scholar 

  • Murdaugh HV, Robin ED (1967) Acid–base metabolism in the dogfish shark. In: Gilbert PW, Mathewson RF, Rall DP (eds) Sharks, skates and rays. Johns Hopkins Press, Baltimore, pp 249–264

    Google Scholar 

  • Nakada T, Westhoff CM, Kato A, Hirose S (2007) Ammonia secretion from fish gill depends on a set of Rh glycoproteins. FASEB J 21:1067–1074

    Article  CAS  PubMed  Google Scholar 

  • Nakada T, Westhoff CM, Yamaguchi Y, Hyodo S, Li X, Muro T, Kato A, Nakamura Hirose S (2010) Rhesus glycoprotein P2 (Rhp2) is a novel member of the Rh family of ammonia transporters highly expressed in shark kidney. J Biol Chem 285:2653–2664

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Nawata CM, Wood CM (2008) The effects of CO2 and external buffering on ammonia excretion and Rhesus glycoprotein mRNA expression in rainbow trout. J Exp Biol 211:3226–3236

    Article  CAS  PubMed  Google Scholar 

  • Nawata CM, Hung CCY, Tsui TKN, Wilson JM, Wright PA, Wood CM (2007) Ammonia excretion in rainbow trout (Oncorhynchus mykiss): evidence for Rh glycoprotein and H+-ATPase involvement. Physiol Genomics 31:463–474

    Article  CAS  PubMed  Google Scholar 

  • Nawata CM, Hirose S, Nakada T, Wood CM, Kato A (2010a) Rh glycoprotein expression is modulated in pufferfish (Takifugu rubripes) during high environmental ammonia exposure. J Exp Biol 213:3150–3160

    Article  CAS  PubMed  Google Scholar 

  • Nawata CM, Wood CM, O’Donnell MJ (2010b) Functional characterization of Rhesus glycoproteins from an ammoniotelic teleost, the rainbow trout, using oocyte expression and SIET analysis. J Exp Biol 213:1049–1059

    Article  CAS  PubMed  Google Scholar 

  • Nawata CM, Walsh PJ, Wood CM (2015) Physiological and molecular responses of the spiny dogfish shark (Squalus acanthias) to high environmental ammonia: scavenging for nitrogen. J Exp Biol 218:238–248

    Article  PubMed  Google Scholar 

  • Pärt P, Wright PA, Wood CM (1998) Urea and water permeability in dogfish (Squalus acanthias) gills. Comp Biochem Physiol 199A:117–123

    Article  Google Scholar 

  • Payan P, Maetz J (1973) Branchial sodium transport mechanisms in Scyliorhinis canicula; evidence for Na+/NH4 + and Na+/H+ exchanges and for a role of carbonic anhydrase. J Exp Biol 58:487–502

    CAS  Google Scholar 

  • Perry SF, Braun MH, Noland M, Dawdy J, Walsh PJ (2010) Do zebrafish Rh proteins act as dual ammonia–CO2 channels? J Exp Zool 313A:618–621

    Article  CAS  Google Scholar 

  • Piermarini PM, Evans DH (2001) Immunochemical analysis of the vacuolar proton-ATPase B- subunit in the gills of a euryhaline stingray (Dasyatis sabina): effects of salinity and relation to Na+/K+-ATPase. J Exp Biol 204:3251–3259

    CAS  PubMed  Google Scholar 

  • Piermarini PM, Verlander JW, Royaux IE, Evans DH (2002) Pendrin immunoreactivity in the gill epithelium of a euryhaline elasmobranch. Am J Physiol 283:R983–R992

    Google Scholar 

  • Rahmatullah M, Boyde TRC (1980) Improvements in the determination of urea using diacetyl monoxime; methods with and without deproteinisation. Clin Chim Acta 107:3–9

    Article  CAS  PubMed  Google Scholar 

  • Reilly BD, Cramp RL, Wilson JM, Campbell HA, Franklin CE (2011) Branchial osmoregulation in the euryhaline bull shark, Carcharhinus leucas: a molecular analysis of ion transporters. J Exp Biol 214:2883–2895

    Article  CAS  PubMed  Google Scholar 

  • Ripoche P, Bertrand O, Gane P, Birkenmeier C, Colin Y, Cartron J-P (2004) Human Rhesus- associated glycoprotein mediates facilitated transport of NH3 into red blood cells. Proc Natl Acad Sci USA 101:17222–17227

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Roa JN, Munevar CL, Tresguerres M (2014) Feeding induces translocation of vacuolar proton ATPase and pendrin to the membrane of leopard shark (Triakis semifasciata) mitochondrion-rich gill cells. Comp Biochem Physiol 174A:29–37

    Article  Google Scholar 

  • Salama A, Morgan IJ, Wood CM (1999) The linkage between sodium uptake and ammonia excretion in rainbow trout—kinetic analysis, the effects of (NH4)2 SO4 and NH4 HCO3 infusion, and the influence of gill boundary layer pH. J Exp Biol 202:697–709

    CAS  PubMed  Google Scholar 

  • Shankar RA, Anderson PM (1985) Purification and properties of glutamine synthetase from liver of Squalus acanthias. Arch Biochem Biophys 239:248–259

    Article  CAS  PubMed  Google Scholar 

  • Smith HW (1929) The composition of the body fluids of elasmobranchs. J Biol Chem 81:407–419

    CAS  Google Scholar 

  • Smith HW (1936) The retention and physiological role of urea in the elasmobranchii. Biol Rev 11:49–82

    Article  CAS  Google Scholar 

  • Soupene E, Inwood W, Kustu S (2004) Lack of the Rhesus protein Rh1 impairs growth of the green alga Chlamydomonas reinhardtii at high CO2. Proc Natl Acad Sci USA 101:7787–7792

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Stewart PA (1981) How to understand acid-base: a quantitative acid-base primer for biology and medicine. Elsevier North Holland Inc, New York

    Google Scholar 

  • Tresguerres M, Katoh F, Fenton H, Jasinska E, Goss GG (2005) Regulation of branchial V-H+-ATPase, Na+/K+-ATPase and NHE2 in response to acid and base infusions in the Pacific spiny dogfish (Squalus acanthias). J Exp Biol 208:345–354

    Article  CAS  PubMed  Google Scholar 

  • Tresguerres M, Parks SK, Katoh F, Goss GG (2006) Microtubule-dependent relocation of branchial V-H+-ATPase to the basolateral membrane in the Pacific spiny dogfish (Squalus acanthias): a role in base secretion. J Exp Biol 209:599–609

    Article  CAS  PubMed  Google Scholar 

  • Tresguerres M, Parks SK, Wood CM, Goss GG (2007) V-H+-ATPase translocation during blood alkalosis in dogfish gills: interaction with carbonic anhydrase and involvement in the post-feeding alkaline tide. Am J Physiol 292:R2012–R2019

    CAS  Google Scholar 

  • Verdouw H, van Echted CJA, Dekkers EMJ (1978) Ammonia determination based on indophenol formation with sodium salicylate. Water Res 12:399–402

    Article  CAS  Google Scholar 

  • Walker RL, Wilkes PRH, Wood CM (1989) The effects of hypersaline exposure on the blood oxygen affinity of the freshwater teleost Catastomus commersoni. J Exp Biol 142:125–142

    Google Scholar 

  • Walsh PJ, Danulat E, Mommsen TP (1990) Variation in urea excretion in the gulf toadfish Opsanus beta. Mar Biol 106:323–328

    Article  CAS  Google Scholar 

  • Weihrauch D, Morris S, Towle DW (2004) Ammonia excretion in aquatic and terrestrial crabs. J Exp Biol 207:4491–4504

    Article  CAS  PubMed  Google Scholar 

  • Weihrauch D, Donini A, O’Donnell MJ (2012) Ammonia transport by terrestrial and aquatic insects. J Insect Physiol 58:473–487

    Article  CAS  PubMed  Google Scholar 

  • Wilson RW, Taylor EW (1992) Transbranchial ammonia gradients and acid base responses to high external ammonia concentration in rainbow trout (Oncorhynchus mykiss) acclimated to different salinities. J Exp Biol 166:95–112

    CAS  PubMed  Google Scholar 

  • Wilson RW, Wright PM, Munger S, Wood CM (1994) Ammonia excretion in fresh water rainbow trout (Oncorhynchus mykiss) and the importance of gill boundary layer acidification: lack of evidence for Na+/NH4 + exchange. J Exp Biol 191:37–58

    CAS  PubMed  Google Scholar 

  • Wood CM, Perry SF, Wright PA, Bergman HL, Randall DJ (1989) Ammonia and urea dynamics in the Lake Magadi tilapia, a ureotelic teleost fish adapted to an extremely alkaline environment. Respir Physiol 77:1–20

    Article  CAS  PubMed  Google Scholar 

  • Wood CM, Pärt P, Wright PA (1995) Ammonia and urea metabolism in relation to gill function and acid-base balance in a marine elasmobranch, the spiny dogfish (Squalus acanthias). J Exp Biol 198:1545–1558

    PubMed  Google Scholar 

  • Wood CM, Kajimura M, Mommsen TP, Walsh PJ (2005) Alkaline tide and nitrogen conservation after feeding in the elasmobranch Squalus acanthias. J Exp Biol 208:2693–2705

    Article  CAS  PubMed  Google Scholar 

  • Wood CM, Bucking CP, Fitzpatrick J, Nadella SR (2007a) The alkaline tide goes out and the nitrogen stays in after feeding in the dogfish shark, Squalus acanthias. Respir Physiol Neurobiol 159:163–170

    Article  CAS  PubMed  Google Scholar 

  • Wood CM, Kajimura M, Bucking CP, Walsh PJ (2007b) Osmoregulation, ionoregulation, and acid-base regulation by the gastrointestinal tract after feeding in the dogfish shark. J Exp Biol 210:1335–1349

    Article  CAS  PubMed  Google Scholar 

  • Wood CM, Munger SR, Thompson J, Shuttleworth TJ (2007c) Control of rectal gland secretion by blood acid-base status in the intact dogfish shark (Squalus acanthias). Respir Physiol Neurobiol 156:220–228

    Article  CAS  PubMed  Google Scholar 

  • Wood CM, Kajimura M, Mommsen TP, Walsh PJ (2008) Is the alkaline tide a signal to activate metabolic or ionoregulatory enzymes in the dogfish shark (Squalus acanthias)? Physiol Biochem Zool 81:278–287

    Article  CAS  PubMed  Google Scholar 

  • Wood CM, Liew HJ, De Boeck G, Walsh PJ (2013a) A perfusion study of the handling of urea and urea analogues by the gills of the dogfish shark (Squalus acanthias). Peer J 1:e33. doi:10.7717/peerj.33

    Article  PubMed Central  PubMed  Google Scholar 

  • Wood CM, Nawata CM, Wilson JM, Laurent P, Chevalier C, Bergma HL, Bianchini A, Maina JN, Johannson OE, Bianchini LF, Kavembe GD, Papah MB, Ojoo RO (2013b) Rh proteins and NH4 +-activated Na+-ATPase in the Magadi tilapia (Alcolapia grahami), a 100% ureotelic teleost fish. J Exp Biol 216:2998–3007

    Article  CAS  PubMed  Google Scholar 

  • Wright PA, Wood CM (1985) An analysis of branchial ammonia excretion in the freshwater rainbow trout: effects of environmental pH change and sodium uptake blockade. J Exp Biol 114:329–353

    CAS  Google Scholar 

  • Zhang L, Wood CM (2009) Ammonia as a stimulant to ventilation in rainbow trou Oncorhynchus mykiss. Respir Physiol Neurobiol 168:261–271

    Article  CAS  PubMed  Google Scholar 

  • Zhang L, Nawata CM, Wood CM (2013) Sensitivity in ventilation and brain metabolism to ammonia exposure in rainbow trout, Oncorhynchus mykiss. J Exp Biol 216:4025–4037

    Article  CAS  PubMed  Google Scholar 

  • Zhang L, Nawata CM, DeBoeck G, Wood CM (2014) Rh protein expression in branchial neuroepithelial cells, and the role of ammonia in ventilatory control in fish. Comp Biochem Physiol A. doi:10.1016/j.cbpa.2014.10.004

    Google Scholar 

Download references

Acknowledgments

We thank Bruce Cameron, former Research Co-ordinator at Bamfield Marine Sciences Centre, for invaluable logistical assistance; Linda Diao and Tania Ng for excellent technical help; Sue Edwards for helpful input; and four anonymous reviewers for constructive comments. We are supported by the Discovery Grants from the Natural Sciences and Engineering Research Council of Canada (NSERC) to CMW and PJW, who were both supported by the Canada Research Chairs Program.

Author information

Authors and Affiliations

  1. Bamfield Marine Sciences Centre, 100 Pachena Road, Bamfield, BC, V0R 1B0, Canada

    C. Michele Nawata, Patrick J. Walsh & Chris M. Wood

  2. Department of Biology, McMaster University, 1280 Main St. West, Hamilton, ON, L8S 4K1, Canada

    C. Michele Nawata & Chris M. Wood

  3. Department of Physiology, University of Arizona, 1501 N. Campbell Ave., Tucson, AZ, 85724, USA

    C. Michele Nawata

  4. Department of Biology and Centre for Advanced Research in Environmental Genomics, University of Ottawa, Ottawa, ON, K1N 6N5, Canada

    Patrick J. Walsh

  5. Department of Zoology, University of British Columbia, #4321-6270 University Blvd., Vancouver, BC, V6T 1Z4, Canada

    Chris M. Wood

Authors
  1. C. Michele Nawata
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Patrick J. Walsh
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Chris M. Wood
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to C. Michele Nawata.

Additional information

Communicated by G. Heldmaier.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Nawata, C.M., Walsh, P.J. & Wood, C.M. Nitrogen metabolism, acid–base regulation, and molecular responses to ammonia and acid infusions in the spiny dogfish shark (Squalus acanthias). J Comp Physiol B 185, 511–525 (2015). https://doi.org/10.1007/s00360-015-0898-4

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00360-015-0898-4

Keywords

Search

Navigation