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Nitrogen metabolism in tambaqui (Colossoma macropomum), a neotropical model teleost: hypoxia, temperature, exercise, feeding, fasting, and high environmental ammonia

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Abstract

The total rate of N-waste excretion (M N) in juvenile tambaqui living in ion-poor Amazonian water comprised 85 % ammonia-N (M Amm-N) and 15 % urea-N (M Urea-N). Both occurred mainly across the gills with only ~5 % of M Amm-N and ~39 % of M Urea-N via the urine. Tambaqui were not especially tolerant to high environmental ammonia (HEA), despite their great resistance to other environmental factors. Nevertheless, they were able to maintain a continued elevation of M Amm-N during and after 48-h exposure to 2.5 mmol L−1 HEA. The normally negative transepithelial potential (−18 mV) increased to −9 mV during the HEA period, which would help to reduce branchial NH4 + entry. During 3 h of acute environmental hypoxia (30 % saturation), M Amm-N declined, and recovered thereafter, similar to the response seen in other hypoxia-tolerant teleosts; M Urea-N did not change. However, during gradual hypoxia, M Amm-N remained constant, but M Urea-N eventually fell. The acute temperature sensitivities of M Amm-N and M N were low from 28 °C (acclimation) to 33 °C (Q10 ~1.5), but high (~3.8) from 33 to 38 °C, relative to \( M_{{{\text{O}}_{ 2} }} \) (~1.9 throughout). In contrast, M Urea-N exhibited a different pattern over these temperature ranges (Q10 2.6 and 2.1, respectively). The nitrogen quotient (NQ = 0.16–0.23) was high at all temperatures, indicating a 60–85 % reliance on protein to fuel aerobic metabolism in these fasting animals. During steady-state aerobic exercise, \( M_{{{\text{O}}_{ 2} }} \) and M Urea-N increased in parallel with velocity (up to 3.45 body lengths s−1), but M Amm (and thus M N) remained approximately constant. Therefore, the NQ fell progressively, indicating a decreasing reliance on protein-based fuels, as work load increased. In group feeding trials using 45 % protein commercial pellets, tambaqui excreted 82 % (range 39–170 %) of the dietary N within 24 h; N-retention efficiency was inversely related to the ration voluntarily consumed. M Amm-N peaked at 4–6 h, and M Urea-N at 6–9-h post-feeding, with an additional peak in M Amm-N only at 21 h. During subsequent fasting, M N stabilized at a high endogenous rate from 2 through 8 days post-feeding. Possible reasons for the high wasting of protein-N during both fasting and feeding are discussed.

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References

  • Alsop DH, Wood CM (1997) The interactive effects of feeding and exercise on oxygen consumption, swimming performance and protein usage in juvenile rainbow trout. J Exp Biol 200:2337–2346

    CAS  PubMed  Google Scholar 

  • Alsop DH, Kieffer JD, Wood CM (1999) The effects of temperature and swimming speed on instantaneous fuel use and nitrogenous waste excretion of the Nile tilapia. Physiol Biochem Zool 72:474–483

    Article  CAS  PubMed  Google Scholar 

  • Anderson JT, Rojas JS, Flecker AS (2009) High-quality seed dispersal by fruit-eating fishes in Amazonian floodplain habitats. Oecologia 161:279–290

    Article  PubMed  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 

  • Arbelaez-Rojas GA, Fracalossi DM, Fim JD (2002) Composicao corporal de tambaqui, Colossoma macropomum, e matrinxa, Brycon cephalus, em sistemas de cultivo intensive, em igarape, e semi-intensivo, em viveiros. R Bras Zootec 31:1059–1069

    Article  Google Scholar 

  • Braum E, Junk WJ (1982) Morphological adaptation of two Amazonian characoids (Pisces) for surviving in oxygen deficient waters. Int Rev Gesamten Hydrobiol 67:869–886

    Google Scholar 

  • Brett JR, Zala CA (1975) Daily pattern of nitrogen excretion and oxygen consumption of sockeye salmon (Oncorhynchus nerka) under controlled conditions. J Fish Res Board Can 32:2479–2486

    Article  Google Scholar 

  • Cameron JN, Wood CM (1978) Renal function and acid-base regulation in two Amazonian Erythrinid fishes: Hoplias malabaricus, a water-breather, and Hoplerythrinus unitaeniatus, a facultative air-breather. Can J Zool 56:917–930

    Article  CAS  Google Scholar 

  • Caraballo P, Forsberg BR, Almeida FF, Leite RG (2014) Diel patterns of temperature, conductivity and dissolved oxygen in an Amazon floodplain lake: description of a friagem phenomenon. Acta Limnol Bras 26:318–331

    CAS  Google Scholar 

  • Chew SF, Wilson JM, Ip YK, Randall DJ (2005) Nitrogen excretion and defense against ammonia toxicity. In: Val AL, Almeida-Val VMF, Randall DJ (eds) Fish physiology, vol 21, The physiology of tropical fishes. Academic Press, San Diego, pp 307–379

    Google Scholar 

  • Cho CY (1990) Fish nutrition, feeds, and feeding, with special emphasis on salmonid aquaculture. Food Rev Int 6:333–357

    Article  CAS  Google Scholar 

  • Clarke A, Johnston NM (1999) Scaling of metabolic rate with body mass and temperature in teleost fish. J Anim Ecol 68:893–905

    Article  Google Scholar 

  • Conceição LE, Aragão C, Dias J, Costas B, Terova G, Martins C, Tort L (2012) Dietary nitrogen and fish welfare. Fish Physiol Biochem 38:119–141

    Article  PubMed  Google Scholar 

  • Couceiro SR, Hamada N, Luz SL, Forsberg BR, Pimentel TP (2007) Deforestation and sewage effects on aquatic macroinvertebrates in urban streams in Manaus, Amazonas, Brazil. Hydrobiologia 575:271–284

    Article  CAS  Google Scholar 

  • Davison W (1997) The effects of exercise training on teleost fish, a review of recent literature. Comp Biochem Physiol 117A:67–75

    Article  CAS  Google Scholar 

  • De Boeck G, Alsop G, Wood CM (2001) Cortisol effects on aerobic and anaerobic metabolism, nitrogen excretion, and whole body composition in juvenile rainbow trout. Physiol Biochem Zool 74:858–868

    Article  PubMed  Google Scholar 

  • De Boeck G, Wood CM, Iftikar FI, Matey V, Scott GR, Sloman KA, da Silva MDNP, Almeida-Val VMF, Val AL (2013) Interactions between hypoxia tolerance and food deprivation in Amazonian oscars, Astronotus ocellatus. J Exp Biol 216:4590–4600

    Article  PubMed  Google Scholar 

  • Florindo LH, Reid SG, Kalinin AL, Milsom WK, Rantin FT (2004) Cardiorespiratory reflexes and aquatic surface respiration in the neotropical fish tambaqui (Colossoma macropomum): acute responses to hypercarbia. J Comp Physiol B 174:319–328

    Article  PubMed  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 

  • Gilmour KM, Milsom WK, Rantin FT, Reid SG, Perry SF (2005) Cardiorespiratory responses to hypercarbia in tambaqui Colossoma macropomum: chemoreceptor orientation and specificity. J Exp Biol 208:1095–1107

    Article  CAS  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

    Article  CAS  PubMed  Google Scholar 

  • Goulding M (1980) The fishes and the forest: explorations in Amazonian natural history. University of California Press, Berkeley

    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

    Google Scholar 

  • Hickman CP, Trump BF (1969) The kidney. In: Hoar WS, Randall DJ (eds) Fish physiology, vol 1. Academic Press, New York, pp 1–89

    Google Scholar 

  • Houlihan DF, Laurent P (1987) Effects of exercise training on the performance, growth, and protein turnover of rainbow trout (Salmo gairdneri). Can J Fish Aquat Sci 44:1614–1621

    Article  Google Scholar 

  • Hunn JB (1985) Role of calcium in gill function in freshwater fishes. Comp Biochem Physiol 82A:543–547

    Article  CAS  Google Scholar 

  • Ip YK, Chew SF (2010) Ammonia production, excretion, toxicity and defense in fish: a review. Frontiers Physiol 1:1–20

    Article  Google Scholar 

  • Ismino-Orbe RAI, Araujo-Lima C, de Carvalho Gomes L (2003) Excreção de amônia por tambaqui (Colossoma macropomum) de acordo com variações na temperatura da água e massa do peixe. Pesqui Agropecu Bras 38:1243–1247

    Article  Google Scholar 

  • Kieffer JD, Alsop D, Wood CM (1998) A respirometric analysis of fuel use during aerobic swimming at different temperatures in rainbow trout (Oncorhynchus mykiss). J Exp Biol 201:3123–3133

    PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Lauff RF, Wood CM (1996b) Respiratory gas exchange, nitrogenous waste excretion, and fuel usage during starvation in juvenile rainbow trout. J Comp Physiol B 165:542–551

    Article  CAS  PubMed  Google Scholar 

  • Liew HJ, Sinha AK, Nawata CM, Blust R, Wood CM, De Boeck G (2013) Differential responses in ammonia excretion, sodium fluxes and gill permeability explain different sensitivities to acute high environmental ammonia in three freshwater teleosts. Aquat Toxicol 126:63–76

    Article  CAS  PubMed  Google Scholar 

  • Maetz J (1972) Branchial sodium exchange and ammonia excretion in the goldfish Carassius auratus. Effects of ammonia loading and temperature changes. J Exp Biol 56:601–620

    Google Scholar 

  • Martinez CBR, Azevedo F, Winkaler EU (2006) Toxicidade e efeitos da amônia em peixes neotropicais. In: Cyrino JEP, Urbinati EC (eds) Tópicos especiais em biologia aquática e aqüicultura. Sociedade Brasileira de Aqüicultura e Biologia Aquática, Jaboticabal, pp 81–95

    Google Scholar 

  • Milsom WK, Reid SG, Rantin FT, Sundin L (2002) Extrabranchial chemoreceptors involved in respiratory reflexes in the neotropical fish Colossoma macropomum (the tambaqui). J Exp Biol 205:1765–1774

    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 Genom 31:463–474

    Article  CAS  Google Scholar 

  • Nawata CM, Hirose S, Nakada T, Wood CM, Kato A (2010) 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 

  • Olson KR, Fromm PO (1971) Excretion of urea by two teleosts exposed to different concentrations of ambient ammonia. Comp Biochem Physiol 40A:9991–10007

    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

    Article  CAS  PubMed  Google Scholar 

  • Perz SG (2000) The quality of urban environments in the Brazilian Amazon. Soc Indic Res 49:181–212

    Article  Google Scholar 

  • Rahmatullah M, Boyde TR (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 

  • Randall DJ, Tsui TKN (2002) Ammonia toxicity in fish. Mar Pollut Bull 45:17–23

    Article  CAS  PubMed  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 

  • Reid SG, Perry SF, Gilmour KM, Milsom WK, Rantin FT (2005) Reciprocal modulation of O2 and CO2 cardiorespiratory chemoreflexes in the tambaqui. Respir Physiol Neurobiol 146:175–194

    Article  PubMed  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 

  • Roubach R, Saint-Paul U (1994) Use of fruits and seeds from Amazonian inundated forests in feeding trials with Colossoma macropomum (Cuvier, 1818) (Pisces, Characidae). J Appl Ichthyol 10:134–140

    Article  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 

  • Sinha AK, Liew HJ, Nawata CM, Blust R, Wood CM, De Boeck G (2013) Modulation of Rh glycoproteins, ammonia excretion and Na+ fluxes in three freshwater teleosts when exposed chronically to high environmental ammonia. J Exp Biol 216:2917–2930

    Article  CAS  PubMed  Google Scholar 

  • Smith HW (1929) The excretion of ammonia and urea by the gills of fishes. J Biol Chem 81:727–742

    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. doi:10.1007/s10750-015-2623-4

  • Sukumaran N, Kutty MN (1977) Oxygen consumption and ammonia excretion in the catfish Mystus armatus, with special reference to swimming speed and ambient oxygen. Proc Indian Acad Sci 86B:195–206

    CAS  Google Scholar 

  • Sundin LE, Reid SG, Rantin FT, Milsom WK (2000) Branchial receptors and cardiorespiratory reflexes in a neotropical fish, the tambaqui (Colossoma macropomum). J Exp Biol 203:1225–1239

    CAS  PubMed  Google Scholar 

  • U.S. EPA—United States Environmental Protection Agency (2013) Aquatic life ambient water quality criteria for ammonia-freshwater. EPA-822-R-13-001. EPA, Washington

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

    Book  Google Scholar 

  • Val AL, Honczaryk A (1995) Criando peixes na Amazônia. INPA, Manaus

    Google Scholar 

  • Val AL, de Menezes GC, Wood CM (1998) Red blood cell adrenergic responses in Amazonian teleosts. J Fish Biol 52:82–93

    Article  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 

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

    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 

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

    Article  CAS  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

    Article  CAS  PubMed  Google Scholar 

  • Wilson RW, Bergman HL, Wood CM (1994) Metabolic costs and physiological consequences of acclimation to aluminum in juvenile rainbow trout (Oncorhynchus mykiss). 2: gill morphology, swimming performance, and aerobic scope. Can J Fish Aquat Sci 51:536–544

    Article  CAS  Google Scholar 

  • Wilson RW, Wood CM, Gonzalez R, Patrick ML, Bergman HL, Narahara AB, Val AL (1999) Ion and acid-base balance in three species of Amazonian fish during gradual acidification of extremely soft water. Physiol Biochem Zool 72:277–285

    Article  CAS  PubMed  Google Scholar 

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

  • 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, Grosell M (2008) A critical analysis of transepithelial potential in intact killifish (Fundulus heteroclitus) subjected to acute and chronic changes in salinity. J Comp Physiol B 178:713–727

    Article  CAS  PubMed  Google Scholar 

  • Wood CM, Nawata CM (2011) A nose-to-nose comparison of physiological and molecular responses of trout to high environmental ammonia in seawater versus freshwater. J Exp Biol 214:3557–3569

    Article  CAS  PubMed  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

    Article  CAS  PubMed  Google Scholar 

  • Wood CM, Kajimura M, Sloman KA, Scott GR, Walsh PJ, Almeida-Val VMF, Val AL (2007) Rapid regulation of Na+ fluxes and ammonia excretion in response to acute environmental hypoxia in the Amazonian oscar, Astronotus ocellatus. Am J Physiol 292:R2048–R2058

    CAS  Google Scholar 

  • Wood CM, Iftikar FI, Scott GR, De Boeck G, Sloman KA, Matey V, Valdez Domingos FA, Duarte RM, Almeida-Val VMF, Val AL (2009) Regulation of gill transcellular permeability and renal function during acute hypoxia in the Amazonian oscar (Astronotus ocellatus): new angles to the osmo-respiratory compromise. J Exp Biol 212:1949–1964

    Article  CAS  PubMed  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

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Zimmer AM, Brauner CJ, Wood CM (2014) Ammonia transport across the skin of adult rainbow trout (Oncorhynchus mykiss) exposed to high environmental ammonia (HEA). J Comp Physiol B 184:77–90

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

We thank two anonymous reviewers for constructive comments. 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). RMD received a postdoctoral fellowship from the same program (CNPq process number: 151083/2013-4). JGSN received a PCI fellowship from INPA/CNPq. JMW was supported by the INCT-ADAPTA grant to ALV and a Portuguese Foundation for Science and Technology grant (FCT) PTDC/MAR/98035 and the European Regional Development Fund (COMPETE—Operational Competitiveness Program) and national funds through FCT (Pest-C/MAR/LA0015/2011). ALV received a research fellowship from CNPq.

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Authors and Affiliations

  1. Department of Zoology, University of British Columbia, Vancouver, BC, V6T 1Z4, Canada

    Chris M. Wood

  2. Department of Biology, McMaster University, Hamilton, ON, Canada

    Chris M. Wood

  3. Rosenstiel School of Marine and Atmospheric Science, University of Miami, Coral Gables, FL, USA

    Chris M. Wood

  4. Laboratório de Ecofisiologia e Evolução Molecular, Instituto Nacional de Pesquisas da Amazônia (INPA), Manaus, Amazonas, Brazil

    Chris M. Wood, José Gadelha de Souza Netto, Jonathan M. Wilson, Rafael M. Duarte & Adalberto Luis Val

  5. Laboratório de Fisologia Molecular, Centro Interdisciplinar de Investigação Marinha e Ambiental, Porto, Portugal

    Jonathan M. Wilson

  6. Department of Biology, Wilfrid Laurier University, Waterloo, ON, Canada

    Jonathan M. Wilson

  7. Instituto de Biociências, Universidade do Estado de São Paulo, Campus do Litoral Paulista, Sao Vicente, SP, Brazil

    Rafael M. Duarte

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Wood, C.M., de Souza Netto, J.G., Wilson, J.M. et al. Nitrogen metabolism in tambaqui (Colossoma macropomum), a neotropical model teleost: hypoxia, temperature, exercise, feeding, fasting, and high environmental ammonia. J Comp Physiol B 187, 135–151 (2017). https://doi.org/10.1007/s00360-016-1027-8

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