Skip to main content

The physiology of the Tambaqui (Colossoma macropomum) at pH 8.0

Abstract

The Tambaqui is a model neotropical teleost which is of great economic and cultural importance in artisanal fisheries and commercial aquaculture. It thrives in ion-poor, often acidic Amazonian waters and exhibits excellent regulation of physiology down to water pH 4.0. Curiously, however, it is reported to perform poorly in aquaculture at pH 8.0, an only slightly alkaline pH which would be benign for most freshwater fish. In initial experiments with Tambaqui of intermediate size (30–50 g), we found that ammonia excretion rate was unchanged at pH 4, 5, 6, and 7, but elevated after 20–24 h at pH 8, exactly opposite the pattern seen in most teleosts. Subsequent experiments with large Tambaqui (150–300 g) demonstrated that only ammonia, and not urea excretion was increased at pH 8.0, and that the elevation was proportional to a general increase in MO2. There was an accompanying elevation in net acidic equivalent excretion and/or basic equivalent uptake which occurred mainly at the gills. Net Na+ balance was little affected while Cl balance became negative, implicating a disturbance of Cl versus base exchange rather than Na+ versus acid exchange. Arterial blood pH increased by 0.2 units at pH 8.0, reflecting combined metabolic and respiratory alkaloses. Most parameters recovered to control levels by 18–24 h after return to pH 6.0. With respect to large Tambaqui, we conclude that a physiology adapted to acidic pH performs inappropriately at moderately alkaline pH. In small Tambaqui (4–15 g), the responses were very different, with an initial inhibition of ammonia excretion rate at pH 8.0 followed by a subsequent restoration of control levels. Elevated ammonia excretion rate occurred only after return to pH 6.0. Furthermore, MO2, plasma cortisol, and branchial vH+ATPase activities all declined during pH 8.0 exposure in small Tambaqui, in contrast to the responses in larger fish. Overall, small Tambaqui appear to cope better at pH 8.0, a difference that may correlate with their natural history in the wild.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10
Fig. 11

References

  • Albers C (1970) Acid–base balance. In: Hoar WS, Randall DJ (eds) Fish physiology, vol 4. Academic Press, San Diego, pp 173–208

    Google Scholar 

  • Araujo-Lima C, Goulding M (1997) So fruitful a fish: ecology, conservation, and aquaculture of the Amazon’s Tambaqui. Columbia University Press, New York

    Google Scholar 

  • Aride PHR, Roubach R, Val AL (2004) Water pH in central Amazon and its importance for Tambaqui (Colossoma macropomum) culture. World Aquac 35:24–28

    Google Scholar 

  • Aride PHR, Roubach R, Val AL (2007) Tolerance response of Tambaqui Colossoma macropomum (Cuvier) to water pH. Aquac Res 38:588–594

    CAS  Article  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 

  • Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

    CAS  Article  PubMed  Google Scholar 

  • Bucking C, Wood CM (2008) The alkaline tide and ammonia excretion after voluntary feeding in freshwater rainbow trout. J Exp Biol 211:2533–2541

    CAS  Article  PubMed  Google Scholar 

  • Cameron JN (1978) Regulation of blood pH in teleost fish. Respir Physiol 33:129–144

    CAS  Article  PubMed  Google Scholar 

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

    CAS  Google Scholar 

  • Chagas EC, Val AL (2006) Ascorbic acid reduces the effects of hypoxia on the Amazon fish Tambaqui. J Fish Biol 69:608–612

    CAS  Article  Google Scholar 

  • Cooper CA, Wilson RW (2008) Post-prandial alkaline tide in freshwater rainbow trout: effects of meal anticipation on recovery from acid–base and ion regulatory disturbances. J Exp Biol 211:2542–2550

    CAS  Article  PubMed  Google Scholar 

  • Da Silva Nunes JDR, Liu S, Pértille F, Perazza CA, Villela PMS, de Almeida-Val VMF, Hilsdorf AWS, Liu Z, Coutinho LL (2017) Large-scale SNP discovery and construction of a high-density genetic map of Colossoma macropomum through genotyping-by-sequencing. Sci Rep 7:46112. https://doi.org/10.1038/srep46112

    Article  Google Scholar 

  • Dejours P (1975) Principles of comparative respiratory physiology. North-Holland Publishing Company, Amsterdam

    Google Scholar 

  • Duarte RM, Ferreira MS, Wood CM, Val AL (2013) Effect of low pH exposure on Na+ regulation in two cichlid fish species of the Amazon. Comp Biochem Physiol A 166:441–448

    CAS  Article  Google Scholar 

  • Duarte RM, Smith DS, Val AL, Wood CM (2016) Dissolved organic carbon from the upper Rio Negro protects zebrafish (Danio rerio) against ionoregulatory disturbances caused by low pH exposure. Sci Rep 6:20377. https://doi.org/10.1038/srep20377

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Evans DH (2011) Freshwater fish gill ion transport: August Krogh to morpholinos and microprobes. Acta Physiol 202:349–359

    CAS  Article  Google Scholar 

  • Florindo LH, Leite CA, Kalinin AL, Reid SG, Milsom WK, Rantin FT (2006) The role of branchial and orobranchial O2 chemoreceptors in the control of aquatic surface respiration in the neotropical fish Tambaqui (Colossoma macropomum): progressive responses to prolonged hypoxia. J Exp Biol 209:1709–1715

    Article  PubMed  Google Scholar 

  • Golombieski JI, Koakoski G, Becker AJ, Almeida APG, Toni C, Finamor IA, Pavanato MA, de Almeida TM, Baldisserotto B (2013) Nitrogenous and phosphorus excretions in juvenile silver catfish (Rhamdia quelen) exposed to different water hardness, humic acid, and pH levels. Fish Physiol Biochem 39:837–849

    CAS  Article  PubMed  Google Scholar 

  • Gonzalez RJ, Preest M (1999) Ionoregulatory specializations for exceptional tolerance of ion-poor,acidic waters in the neon tetra (Paracheirodon innesi). Physiol Biochem Zool 72:156–163

    CAS  Article  PubMed  Google Scholar 

  • Gonzalez RJ, Wilson RW (2001) Patterns of ion regulation in acidophilic fish native to the ion-poor, acidic Rio Negro. J Fish Biol 58:1680–1690

    Article  Google Scholar 

  • Gonzalez RJ, Dalton VM, Patrick ML (1997) Ion regulation in ion-poor, acidic water by the blackskirt tetra (Gymnocorymbus ternetzi), a fish native to the Amazon River. Physiol Zool 70:428–435

    CAS  Article  PubMed  Google Scholar 

  • Gonzalez RJ, Wood CM, Wilson RW, Patrick ML, Bergman HL, Narahara A, Val AL (1998) Effects of water pH and Ca2+ concentration on ion balance in fish of the Rio Negro. Physiol Zool 71:15–22

    CAS  Article  PubMed  Google Scholar 

  • Gonzalez RJ, Wilson RW, Wood CM, Patrick ML, Val AL (2002) Diverse strategies for ion regulation in fish collected from the ion-poor, acidic Rio Negro. Physiol Biochem Zool 75:37–47

    CAS  Article  PubMed  Google Scholar 

  • Gonzalez RJ, Wilson RW, Wood CM (2005) Ionoregulation in tropical fish from ion-poor, acidic blackwaters. In: Val AL, Almeida-Val VMF, Randall DJ (eds) The physiology of tropical fish. Fish physiology, vol 22. Academic Press, San Diego, pp 397–437

    Chapter  Google Scholar 

  • Goulding M, Carvalho ML (1982) Life history and management of the Tambaqui (Colossoma macropomum, Characidae): an important Amazonian food fish. Rev Bras Zool 1:107–133

    Article  Google Scholar 

  • Hills AG (1973) Acid–base balance-chemistry, physiology, pathophysiology. Williams and Wilkins, Baltimore

    Google Scholar 

  • Hirata T, Kaneko T, Ono T, Nakazato T, Furukawa N, Hasegawa S, Wakabayashi S, Shigekawa M, Chang MH, Romero MF, Hirose S (2003) Mechanism of acid adaptation of a fish living in a pH 3.5 lake. Am J Physiol 284:R1199–R1212

    CAS  Google Scholar 

  • Ito Y, Kobayashi S, Nakamura N, Esaki M, Miyagi H, Hoshijima K, Hirose S (2013) Close association of carbonic anhydrase (CA2a & CA15a), Na+/H+ exchanger (Nhe3b), and ammonia transporter Rhcg1 in zebrafish ionocytes responsible for Na+ uptake. Front Physiol 4:59. https://doi.org/10.3389/fphys.2013.00059

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Johansen K, Maloiy GMO, Lykkeboe G (1975) A fish in extreme alkalinity. Respir Physiol 24:159–162

    CAS  Article  PubMed  Google Scholar 

  • Kirschner LB (2004) The mechanism of sodium chloride uptake in hyperregulating aquatic animals. J Exp Biol 207:1439–1452

    CAS  Article  PubMed  Google Scholar 

  • Kültz D, Somero GN (1995) Osmotic and thermal effects on in situ ATPase activity in permeabilized gill epithelial cells of the fish Gillichthys mirabilis. J Exp Biol 198:1883–1894

    Google Scholar 

  • Kumai Y, Perry SF (2011) Ammonia excretion via Rhcg1 facilitates Na+ uptake in larval zebrafish, Danio rerio, in acidic water. Am J Physiol 301:R1517–R1528

    CAS  Google Scholar 

  • Kwong RWM, Kumai Y, Perry SF (2014) The physiology of fish at low pH: the zebrafish as a model system. J Exp Biol 217:651–662

    CAS  Article  PubMed  Google Scholar 

  • Lauff RF, Wood CM (1996) Respiratory gas exchange, nitrogenous waste excretion and fuel usage during aerobic swimming in juvenile rainbow trout. J Comp Physiol B 166:501–509

    CAS  Article  Google Scholar 

  • Lawrence MJ, Wright PA, Wood CM (2015) Physiological and molecular responses of the goldfish kidney (Carassius auratus) to metabolic acidosis, and potential mechanisms of renal ammonia transport. J Exp Biol 218:2124–2135

    Article  PubMed  Google Scholar 

  • Lin CC, Lin LY, Hsu HH, Thermes V, Prunet P, Horng JL, Hwang PP (2012) Acid secretion by mitochondrion-rich cells of medaka (Oryzias latipes) acclimated to acidic freshwater. Am J Physiol Regul Integr Comp Physiol 302:R283–R291

    CAS  Article  PubMed  Google Scholar 

  • Matsuo AYO, Val AL (2007) Acclimation to humic substances prevents whole body sodium loss and stimulates branchial calcium uptake capacity in the cardinal tetras, Paracheirodon axelrodi (Schultz) subjected to extremely low pH. J Fish Biol 70:989–1000

    CAS  Article  Google Scholar 

  • Matsuo AYO, Wood CM, Val AL (2005) Effects of copper and cadmium on ion transport and gill metal binding in the Amazonian teleost Tambaqui (Colossoma macropomum) in extremely soft water. Aquat Toxicol 74:351–364

    CAS  Article  PubMed  Google Scholar 

  • McDonald DG (1983) The interaction of environmental calcium and low pH on the physiology of the rainbow trout, Salmo gairdneri: I. Branchial and renal net ion and H+ fluxes. J Exp Biol 102:123–140

    Google Scholar 

  • McDonald DG, Wood CM (1981) Branchial and renal acid and ion fluxes in the rainbow trout, Salmo gairdneri, at low environmental pH. J Exp Biol 93:101–118

    CAS  Google Scholar 

  • McGeer JC, Eddy FB (1998) Ionic regulation and nitrogenous excretion in rainbow trout exposed to buffered and unbuffered freshwater of pH 10.5. Physiol Zool 71:179–190

    CAS  Article  PubMed  Google Scholar 

  • Mommsen TP, Vijayan MM, Moon TW (1999) Cortisol in teleosts: dynamics, mechanisms of action, and metabolic regulation. Rev Fish Biol Fish 9:211–268

    Article  Google Scholar 

  • Moss BR (2009) Ecology of fresh waters: man and medium, past to future. Wiley, London

    Google Scholar 

  • Pelster B, Wood CM, Speers-Roesch B, Driedzic WR, Almeida-Val V, Val AL (2015) Gut transport characteristics in herbivorous and carnivorous serrasalmid fish from ion poor Rio Negro water. J Comp Physiol B 185:225–241

    CAS  Article  PubMed  Google Scholar 

  • Prado-Lima M, Val AL (2016) Transcriptomic characterization of Tambaqui (Colossoma macropomum Cuvier, 1818) exposed to three climate change scenarios. PLoS One. https://doi.org/10.1371/journal.pone.0152366

    PubMed  PubMed Central  Google Scholar 

  • Preest MR, Gonzalez RJ, Wilson RW (2005) A pharmacological examination of Na+ and Cl transport in two species of freshwater fish. Physiol Biochem Zool 78:259–272

    CAS  Article  PubMed  Google Scholar 

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

    CAS  Article  Google Scholar 

  • Randall DJ, Brauner C, Wilson J (1996) Acid excretion in Amazonian fish. In: Val AL, Almeida-Val VMF, Randall DJ (eds) Physiology and biochemistry of the fishes of the Amazon. INPA, Manaus, pp 91–100

    Google Scholar 

  • Robertson LM, Val AL, Almeida-Val VF, Wood CM (2015) Ionoregulatory aspects of the osmorespiratory compromise during acute environmental hypoxia in 12 tropical and temperate teleosts. Physiol Biochem Zool 88:357–370

    Article  PubMed  Google Scholar 

  • Saint-Paul U (1984) Physiological adaptation to hypoxia of a neotropical characoid fish Colossoma macropomum, Serrasalmidae. Environ Biol Fish 11:53–62

    Article  Google Scholar 

  • Severinghaus JW, Stupfel M, Bradley AF (1956) Variations of serum carbonic acid pK1 with pH and temperature. J Appl Physiol 9:197–200

    CAS  Article  PubMed  Google Scholar 

  • Shih T-H, Horng J-L, Liu ST, Hwang P-P, Lin Y-H (2012) Rhcg1 and NHE3b are involved in ammonium-dependent sodium uptake by zebrafish larvae acclimated to low-sodium water. Am J Physiol 302:R84–R93

    CAS  Google Scholar 

  • Souza-Bastos LR, Val AL, Wood CM (2016) Are Amazonian fish more sensitive to ammonia? Toxicity of ammonia to eleven native species. Hydrobiologia. https://doi.org/10.1007/s10750-0pp1-13

    Google Scholar 

  • Tresguerres M, Katoh F, Orr E, Parks SK, Goss GG (2006) Chloride uptake and base secretion in freshwater fish: a transepithelial ion-transport metabolon? Physiol Biochem Zool 79:981–996

    CAS  Article  PubMed  Google Scholar 

  • Tsui TKN, Hung CYC, Nawata M, Wilson JM, Wright PA, Wood CM (2009) Ammonia transport in cultured gill epithelium of freshwater rainbow trout: the importance of Rhesus glycoproteins and the presence of an apical Na+/NH4 + exchange complex. J Exp Biol 212:878–898

    CAS  Article  PubMed  Google Scholar 

  • Val AL, Almeida-Val VMF (1995) Fishes of the Amazon and their environment. Physiological and biochemical features. Springer, Berlin

    Book  Google Scholar 

  • Van Waarde A (1983) Aerobic and anaerobic ammonia production by fish. Comp Biochem Physiol 74B:675–684

    Google Scholar 

  • Van den Thillart G, Kesbeke F (1978) Anaerobic production of carbon dioxide and ammonia by goldfish Carassius auratus (L.). Comp Biochem Physiol 59A:393–400

    Article  Google Scholar 

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

    CAS  Article  Google Scholar 

  • Weihrauch D, Wilkie MP, Walsh PJ (2009) Ammonia and urea transporters in gills of fish and aquatic crustaceans. J Exp Biol 212:1716–1730

    CAS  Article  PubMed  Google Scholar 

  • Wilkie MP (2002) Ammonia excretion and urea handling by fish gills: present understanding and future research challenges. J Exp Zool 293:284–301

    CAS  Article  PubMed  Google Scholar 

  • Wilkie MP, Wood CM (1991) Nitrogenous waste excretion, acid–base regulation, and ionoregulation in rainbow trout (Onchorhynchus mykiss) exposed to extremely alkaline water. Physiol Zool 64:1069–1086

    CAS  Article  Google Scholar 

  • Wilkie MP, Wood CM (1996) The adaptations of fish to extremely alkaline environments. Comp Biochem Physiol 113B:665–673

    CAS  Article  Google Scholar 

  • Wilkie MP, Wright PA, Iwama GK, Wood CM (1994) The physiological adaptations of the Lahontan cutthroat trout (Oncorhynchus clarki henshawi) following transfer from well water to the highly alkaline waters of Pyramid Lake, Nevada (pH 9.4). Physiol Zool 67:355–380

    Article  Google Scholar 

  • Wilkie MP, Simmons HE, Wood CM (1996) Physiological adaptations to chronically elevated water pH (pH = 9.5) in rainbow trout (Oncorhynchus mykiss). J Exp Zool 274:1–14

    Article  Google Scholar 

  • Wilkie MP, Laurent P, Wood CM (1999) The physiological basis for altered Na+ and Cl movements across the gills of rainbow trout (Oncorhynchus mykiss) in alkaline (pH = 9.5) water. Physiol Biochem Zool 72:360–368

    CAS  Article  PubMed  Google Scholar 

  • Wilson RW (1996) Ammonia excretion in fish adapted to an ion-poor environment. In: Val AL, Almeida-Val VMF, Randall DJ (eds) Physiology and biochemistry of the fishes of the Amazon. INPA, Manaus, pp 123–138

    Google Scholar 

  • Wilson RW, Wood CM, Gonzalez RJ, Patrick M, Bergman HL, Narahara A, Val AL (1999) Net ion fluxes during gradual acidification of extremely softwater in three species of Amazonian fish. Physiol Biochem Zool 72:277–285

    CAS  Article  PubMed  Google Scholar 

  • Wolf K (1963) Physiological salines for fresh-water teleosts. Progress Fish Cultur 25:135–140

    CAS  Article  Google Scholar 

  • Wood CM (1993) Ammonia and urea metabolism and excretion. In: Evans D (ed) The physiology of fishes. CRC Press, Boca Raton, pp 379–425

    Google Scholar 

  • Wood CM (2001) The influence of feeding, exercise, and temperature on nitrogen metabolism and excretion. In: Anderson PA, Wright PA (eds) Fish physiology, vol 20. Academic Press, Orlando, pp 201–238

    Google Scholar 

  • Wood CM, Patrick ML (1994) Methods for assessing kidney and urinary bladder function in fish. In: Hochachka PW, Mommsen TP (eds) Biochemistry and molecular biology of fishes, vol 3. Elsevier, New York, pp 127–143

    Google Scholar 

  • Wood CM, Wilson RW, Gonzalez RJ, Patrick ML, Bergman HL, Narahara A, Val AL (1998) Responses of an Amazonian teleost, the Tambaqui (Colossoma macropomum) to low pH in extremely soft water. Physiol Zool 71:658–670

    CAS  Article  PubMed  Google Scholar 

  • Wood CM, Milligan LM, Walsh PJ (1999) Renal responses of trout to chronic respiratory and metabolic acidosis and metabolic alkalosis. Am J Physiol 277:R482–R492

    CAS  PubMed  Google Scholar 

  • Wood CM, Matsuo AYO, Wilson RW, Gonzalez RJ, Patrick ML, Playle RC, Val AL (2003) Protection by blackwater against disturbances in ion fluxes caused by low pH exposure in freshwater stingrays endemic to the Rio Negro. Physiol Biochem Zool 76:12–27

    Article  PubMed  Google Scholar 

  • Wood CM, Robertson LM, Johannsson OE, Val AL (2014) Mechanisms of Na+ uptake, ammonia excretion, and their potential linkage in native Rio Negro tetras (Paracheirodon axelrodi, Hemigrammus rhodostomus, and Moenkhausia diktyota). J Comp Physiol B 184:877–890

    CAS  Article  PubMed  Google Scholar 

  • Wood CM, de Souza Netto JG, Wilson JM, Duarte, RM, Val AL (2017) Nitrogen metabolism in Tambaqui (Colossoma macropomum), a neotropical model teleost: hypoxia, temperature, exercise, feeding, fasting, and high environmental ammonia. J Comp Physiol B 186:431–445

    Article  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 

  • Wright PA, Wood CM (2009) A new paradigm for ammonia excretion in aquatic animals: role of Rhesus (Rh) glycoproteins. J Exp Biol 212:2303–2312

    CAS  Article  PubMed  Google Scholar 

  • Wright PA, Wood CM (2012) Seven things fish know about ammonia and we do not. Respir Physiol Neurobiol 184:231–240

    CAS  Article  PubMed  Google Scholar 

  • Wright PA, Iwama GK, Wood CM (1993) Ammonia and urea excretion in Lahontan cutthroat trout (Oncorhynchus clarki henshawi) adapted to highly alkaline Pyramid Lake (pH 9.4). J Exp Biol 175:153–172

    CAS  Google Scholar 

  • Wright PA, Wood CM, Wilson JM (2014) Rh vs pH: the role of Rhesus glycoproteins in renal ammonia excretion during metabolic acidosis in a freshwater teleost fish. J Exp Biol 217:2855–2865

    Article  PubMed  Google Scholar 

  • Wright PA, Wood CM, Hiroi J, Wilson JM (2015) (Uncommon) mechanisms of branchial ammonia excretion in the common carp, Cyprinus carpio, in response to environmentally induced metabolic acidosis. Physiol Biochem Zool 89:26–40

    Article  Google Scholar 

  • Zall DM, Fisher D, Garner MQ (1956) Photometric determination of chloride in water. Anal Chem 28:1665–1668

    CAS  Article  Google Scholar 

Download references

Acknowledgements

Supported in Brazil by FAPEAM and CNPq through the INCT-ADAPTA grant to ALV, and a Science Without Borders Program grant to ALV and CMW (CNPq Process Number: 401303/2014-4), and in Canada by a Discovery grant to CMW from the Natural Sciences and Engineering Research Council of Canada (NSERC). CMW was supported by the Canada Research Chairs program and a visiting fellowship from the Science Without Borders Program (CNPq-Brazil). RJG was supported by a Faculty Research Grant and an International Opportunities Grant from the University of San Diego. MSF is the recipient of a Post-Doctoral Fellowship from the Brazilian Centre for Improvement of Higher Education Personnel (CAPES). SBM is the recipient of an MSc Fellowship from CAPES. ALV received a Research Fellowship from CNPq. We thank Mike Wilkie for advice, and Bernd Pelster, Ora Johannsson, Ellen Jung, and Sunita Nadella for assistance, and four anonymous reviewers whose constructive comments improved the manuscript.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Chris M. Wood.

Additional information

Communicated by G. Heldmaier.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Wood, C.M., Gonzalez, R.J., Ferreira, M.S. et al. The physiology of the Tambaqui (Colossoma macropomum) at pH 8.0. J Comp Physiol B 188, 393–408 (2018). https://doi.org/10.1007/s00360-017-1137-y

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00360-017-1137-y

Keywords

  • Alkalinity
  • Ammonia
  • Urea
  • Oxygen consumption
  • Nitrogen quotient
  • Acid–base regulation
  • Ionoregulation