Skip to main content
SpringerLink
Log in

Nitrogen Excretion in Aquatic Crustaceans

  • Chapter
  • First Online:
Acid-Base Balance and Nitrogen Excretion in Invertebrates

Abstract

This chapter summarizes the current knowledge of processes involved in nitrogen excretion in aquatic crustaceans with focus on the species-rich (up to 10,000 species) infraorder Brachyura, the true crabs (Martin and Davis 2001). Besides the introduction that briefly covers pathways of the synthesis of nitrogenous waste products and the toxicity of ammonia, organs involved in the excretory processes will be introduced, such as the antennal gland and the gills. More emphasis will be given toward the gills and their capability to actively excrete ammonia in different haline species including the marine crabs Cancer pagurus and Metacarcinus magister, brackish water living Carcinus maenas, as well as freshwater dwelling Eriocheir sinensis. In more detail this chapter reviews the branchial ammonia excretion mechanisms in the green shore crab C. maenas, which is summarized in a working model at the end. Here the potential roles of the Na+/K+-ATPase, K+-channels, Rh-proteins, V-type H+-ATPase, the microtubule network, Na+/H+ exchangers (NHEs), ammonia transporters (AMTs), and aquaporins (AQPs) will be discussed. Besides cited literature, this chapter contains original data as well as cross-references to corresponding chapters within this book.

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

Access this chapter

Log in via an institution
eBook
USD 16.99
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 54.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 54.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Similar content being viewed by others

References

  • Adlimoghaddam A, Boeckstaens M, Marini AM, Treberg JR, Brassinga AK, Weihrauch D (2015) Ammonia excretion in Caenorhabditis elegans: mechanism and evidence of ammonia transport of the Rh-protein CeRhr-1. J Exp Biol 218:675–683

    Article  PubMed  PubMed Central  Google Scholar 

  • Bellwood O (2002) The occurrence, mechanics and significance of burying behaviour in crabs (Crustacea: Brachyura). J Nat Hist 36:1223–1238

    Article  Google Scholar 

  • Cameron JN, Batterton CV (1978) Antennal gland function in the freshwater crab Callinectes sapidus: water, electrolyte acid-base and ammonia excretion. J Com Physiol 123:143–148

    Google Scholar 

  • Carrisoza-Gaytan R, Rangel C, Salvador C, Saldana-Meyer R, Escalona C, Satlin LM, Liu W, Zavilowitz B, Trujillo J, Bobadilla NA et al (2011) The hyperpolarization-activated cyclic nucleotide-gated HCN2 channel transports ammonium in the distal nephron. Kidney Int 80:832–840

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Chen J-C, Cheng S-Y (1995) Hemolymph oxygen content, oxyhemocyanin, protein levels and ammonia excretion in the shrimp Penaeus monodon exposed to ambient nitrite. J Com Physiol B 164:530–535

    CAS  Google Scholar 

  • Chen JC, Lin CY (1992) Lethal effects of ammonia on Penaeus chinensis Osbeck juveniles at different salinity levels. J Exp Mar Biol Ecol 156(1):139–148

    Article  CAS  Google Scholar 

  • Claybrook DL (1983) The biology of crustacea. In: Mantel LH (ed) In Internal anatomy and physiological regulation. Academic Press, London, pp 163–213

    Chapter  Google Scholar 

  • Cole GA, Brown RJ (1967) The chemistry of artemia habitats. Ecology 48:858–861

    Article  Google Scholar 

  • Cruz MJ, Sourial MM, Treberg JR, Fehsenfeld S, Adlimoghaddam A, Weihrauch D (2013) Cutaneous nitrogen excretion in the African clawed frog Xenopus laevis: effects of high environmental ammonia (HEA). Aquat Toxicol 136–137:1–12

    Google Scholar 

  • DeVries MC, Wolcott DL, Holliday CW (1994) High ammonia and low ph in the urine of the ghost crab, Ocypode quadrata. Biol Bull 186:342–348

    Article  CAS  Google Scholar 

  • Durand F, Regnault M (1998) Nitrogen metabolism of two portunid crabs, Carcinus maenas and Necora puber, during prolonged air exposure and subsequent recovery: a comparative study. J Exp Biol 201(Pt 17):2515–2528

    PubMed  CAS  Google Scholar 

  • Durand F, Devillers N, Lallier FH, Regnault M (2000) Nitrogen excretion and changes in blood components during emersion of the subtidal spider crab Maia squinado (L.). Comp Biochem Physiol A Mol Integr Physiol 127:259–271

    Google Scholar 

  • Edelmann L, Hanson PI, Chapman ER, Jahn R (1995) Synaptobrevin binding to synaptophysin: a potential mechanism for controlling the exocytotic fusion machine. EMBO J 14:224–231

    PubMed  PubMed Central  CAS  Google Scholar 

  • Ehrenfeld J (1974) Aspects of ionic transport mechanisms in crayfish Astacus leptodactylus. J Exp Biol 61:57–70

    Google Scholar 

  • Endeward V, Cartron JP, Ripoche P, Gros G (2008) RhAG protein of the Rhesus complex is a CO2 channel in the human red cell membrane. FASEB J 22:64–73

    Google Scholar 

  • Enoksson V, Samuelsson M-O (1987) Nitrification and dissimilatory ammonium production and the effects on nitrogen flux over the sediment-water interface in bioturbated coastal sediments. Mar Ecol Prog Ser 36:181–189

    Article  CAS  Google Scholar 

  • Fehsenfeld S, Weihrauch D (2016) The role of an ancestral hyperpolarization-activated cyclic nucleotide-gated K+ channel in branchial acid-base regulation in the green crab, Carcinus maenas. J Exp Biol 219:887–896

    Google Scholar 

  • Fellows FCI, Hird FJR (1979) Nitrogen metabolism and excretion in the freshwater crayfish Cherax destructor. Com Biochem Physiol 64B:235–238

    CAS  Google Scholar 

  • Freire CA, Onken H, McNamara JC (2008) A structure-function analysis of ion transport in crustacean gills and excretory organs. Comp Biochem Physiol A Mol Integr Physiol 151:272–304

    Article  PubMed  CAS  Google Scholar 

  • Greenaway P (1991) Nitrogenous excretion in aquatic and terrestrial Crustacea. Mem Qld Mas 31:215–227

    Google Scholar 

  • Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W, Gascuel O (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 59:307–321

    Article  PubMed  CAS  Google Scholar 

  • Harris RR, Coley S, Collins S, McCabe R (2001) Ammonia uptake and its effects on ionoregulation in the freshwater crayfish Pacifastacus leniusculus (Dana). J Comp Physiol B 171:681–693

    Google Scholar 

  • Hartenstein R (1970) Nitrogen metabolism in non-insect arthropods. In: Campbell JW (ed) In comparative biochemistry of nitrogen metabolism. Academic Press, New York, pp 299–385

    Google Scholar 

  • Hazel RH, Burkhead CE, Huggins DG (1982) Development of water quality criteria for ammonia and total residual chlorine for the protection of aquatic life in two Johnson County, Kansas Streams. In: Pearson JG, Foster RB, Bishop WE (ed) Proceedings of annual symposium on aquatic toxicology, 5th edn. Philadelphia, pp 381–388

    Google Scholar 

  • Henry RP, Lucu C, Onken H, Weihrauch D (2012) Multiple functions of the crustacean gill: osmotic/ionic regulation, acid-base balance, ammonia excretion, and bioaccumulation of toxic metals. Front Physiol 3:431

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Holm LM, Jahn TP, Moller AL, Schjoerring JK, Ferri D, Klaerke DA, Zeuthen T (2005) NH3 and NH4 + permeability in aquaporin-expressing Xenopus oocytes. Pflugers Arch 450:415–428

    Google Scholar 

  • Huang CH, Peng J (2005) Evolutionary conservation and diversification of Rh family genes and proteins. Proc Natl Acad Sci U S A 102:15512–15517

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Hunter KC, Kirschner LB (1986) Sodium absorption coupled to ammonia excretion in osmoconforming marine invertebrates. Am J Physiol 251:R957–R962

    PubMed  CAS  Google Scholar 

  • Johnson KE, Perreau L, Charmantier G, Charmantier-Daures M, Lee CE (2014) Without gills: localization of osmoregulatory function in the copepod Eurytemora affinis. Physiol Biochem Zool 87:310–324

    Google Scholar 

  • Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S, Buxton S, Cooper A, Markowitz S, Duran C et al (2012) Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28:1647–1649

    Article  PubMed  PubMed Central  Google Scholar 

  • Kinsella JL, Aronson PS (1981) Interaction of NH4 + and Li+ with the renal microvillus membrane Na+ -H+ exchanger. Am J Physiol 241:C220–C226

    Google Scholar 

  • Kleyman TR, Cragoe EJ Jr (1988) Amiloride and its analogs as tools in the study of ion transport. J Membr Biol 105:1–21

    Article  PubMed  CAS  Google Scholar 

  • Knepper MA (1994) The aquaporin family of molecular water channels. Proc Natl Acad Sci U S A 91:6255–6258

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Krishnamoorthy RV, Srihari K (1973) Changes in the patterns of the freshwater field crab Paratelphusa hydrodromous upon adaptation to higher salinities. Mar Biol 21:341–348

    Article  Google Scholar 

  • Larsen EH, Deaton LE, Onken H, O’Donnell M, Grosell M, Dantzler WH, Weihrauch D (2014) Osmoregulation and excretion. Compr Physiol 4:405–573

    Article  PubMed  Google Scholar 

  • Le Moullac G, Haffner P (2000) Environmental factors affecting immune responses in Crustacea. Aquaculture 191:121–131

    Article  Google Scholar 

  • Lignon JM (1987) Ionic permeabilities of the isolated gill cuticle of the shore crab Carcinus maenas. J Exp Biol 131:159–174

    Google Scholar 

  • Litman T, Sogaard R, Zeuthen T (2009) Ammonia and urea permeability of mammalian aquaporins. Handb Exp Pharmacol 190:327–358

    Article  CAS  Google Scholar 

  • Lohse L, Malschaert JFP, Slomp CP, Helder W, Van Raaphorst W (1993) Nitrogen cycling in North Sea sediments: Interaction of denitrification and nitrification in offshore and coastal areas. Mar Ecol Prog Ser 101:283–296

    Article  CAS  Google Scholar 

  • Lowenstein JM (1972) Ammonia production in muscle and other tissues: the purine nucleotide cycle. Physiol Rev 52:382–414

    PubMed  CAS  Google Scholar 

  • Lucu C, Devescovi M, Siebers D (1989) Do amiloride and ouabain affect ammonia fluxes in perfused Carcinus gill epithelia? J Exp Zool 249:1–5

    Article  PubMed  CAS  Google Scholar 

  • Ludewig U, von Wiren N, Frommer WB (2002) Uniport of NH4 + by the root hair plasma membrane ammonium transporter LeAMT1;1. J Biol Chem 277:13548–13555

    Google Scholar 

  • Mantel LH, Farmer IL (1983) Osmotic and ionic regulation. In: Mantel BA (ed) The biology of crustacea. Academic Press, London, pp 54–126

    Google Scholar 

  • Martin JW, and Davis GE (2001) An updated classification of the recent crustacea. Natural History Museum of Los Angeles County, Science Series 39. Los Angeles, California. ISSN 1-891276-27-1

    Google Scholar 

  • Martin M, Fehsenfeld S, Sourial MM, Weihrauch D (2011) Effects of high environmental ammonia on branchial ammonia excretion rates and tissue Rh-protein mRNA expression levels in seawater acclimated Dungeness crab Metacarcinus magister. Comp Biochem Physiol A Mol Integr Physiol 160:267–277

    Google Scholar 

  • Masui DC, Mantelatto FL, McNamara JC, Furriel RP, Leone FA (2009) Na+, K+ -ATPase activity in gill microsomes from the blue crab, Callinectes danae, acclimated to low salinity: novel perspectives on ammonia excretion. Comp Biochem Physiol A Mol Integr Physiol 153:141–148

    Google Scholar 

  • McGaw IJ (2004) Ventilatory and cardiovascular modulation associated with burying behaviour in two sympatric crab species, Cancer magister and Cancer productus. J Exp Mar Biol Ecol 303:47–63

    Article  Google Scholar 

  • Musa-Aziz R, Chen LM, Pelletier MF, Boron WF (2009) Relative CO2/NH3 selectivities of AQP1, AQP4, AQP5, AmtB, and RhAG. Proc Natl Acad Sci U S A 106:5406–5411

    Article  PubMed  PubMed Central  Google Scholar 

  • Nehrke K, Melvin JE (2002) The NHX family of Na+ -H+ exchangers in Caenorhabditis elegans. J Biol Chem 277:29036–29044

    Google Scholar 

  • Onken H, Riestenpatt S (2002) Ion transport across posterior gills of hyperosmoregulating shore crabs (Carcinus maenas): amiloride blocks the cuticular Na(+) conductance and induces current-noise. J Exp Biol 205:523–531

    Google Scholar 

  • Orlowski J, Grinstein S (2004) Diversity of the mammalian sodium/proton exchanger SLC9 gene family. Pflugers Arch 447:549–565

    Article  PubMed  CAS  Google Scholar 

  • Ostrensky A, Marchiori MA, Poersch LH (1992) Aquatic toxicity of ammonia in the metamorphosis of post-larvae Penaeus paulensis Perez-Farfante. An Acad Bras Cienc 64(4):383–389

    PubMed  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 A Ecol Genet Physiol 313:618–621

    Article  PubMed  CAS  Google Scholar 

  • Pitts RJ, Derryberry SL Jr, Pulous FE, Zwiebel LJ (2014) Antennal-expressed ammonium transporters in the malaria vector mosquito Anopheles gambiae. PLoS One 9:e111858

    Google Scholar 

  • Postel U (2001) Physiologie der Pleopoden mariner Asseln (Crustacea, Isopoda). VWFS (Akademische Abhandlungen zur Biologie), Berlin

    Google Scholar 

  • Postel U, Becker W, Brandt A, Luck-Kopp S, Riestenpatt S, Weihrauch D, Siebers D (2000) Active osmoregulatory ion uptake across the pleopods of the isopod Idotea baltica (Pallas): electrophysiological measurements on isolated split endo- and exopodites mounted in a micro-ussing chamber. J Exp Biol 203(Pt 7):1141–1152

    Google Scholar 

  • Quijada-Rodriguez AR, Treberg JR, Weihrauch D (2015) Mechanism of ammonia excretion in the freshwater leech Nephelopsis obscura: characterization of a primitive Rh protein and effects of high environmental ammonia. Am J Physiol Regul Integr Comp Physiol Ajpregu 00482:2014

    Google Scholar 

  • Ren Q, Pan L, Zhao Q, Si L (2015) Ammonia and urea excretion in the swimming crab Portunus trituberculatus exposed to elevated ambient ammonia-N. Comp Biochem Physiol A Mol Integr Physiol 187:48–54

    Google Scholar 

  • Riestenpatt S (1995) Die osmoregulatorische NaCl-Aufnahme über die Kiemen decapoder Crustaceen (Crustacea, Decapoda). In: Akademische Abhandlungen zur Biologie. Verlag für Wissenschaft und Forschung, Berlin, pp 1–131

    Google Scholar 

  • Riestenpatt S, Onken H, Siebers D (1996) Active absorption of Na+ and Cl− across the gill epithelium of the shore crab Carcinus maenas: voltage-clamp and ion-flux studies. J Exp Biol 199:1545–1554

    Google Scholar 

  • Saparov SM, Liu K, Agre P, Pohl P (2007) Fast and selective ammonia transport by aquaporin-8. J Biol Chem 282:5296–5301

    Article  PubMed  CAS  Google Scholar 

  • Schoffeniels E, Gilles R (1970) Nitrogenous constituents and nitrogen metabolism in arthropods. In: Florkin M, Sheer B (eds) Chemical zoology. Academic Press, New York, pp 199–227

    Chapter  Google Scholar 

  • Skou JC (1965) Enzymatic Basis For Active Transport Of Na+ And K+ Across Cell Membrane. Physiol Rev 45:596–617

    Google Scholar 

  • Spargaaren DH (1990) The effect of environmental ammonia concentrations on the ion-exchange of shore crabs, Carcinus maenas (L.). Com Biochem Physiol 97C:87–91

    Google Scholar 

  • Taylor HH, Taylor EW (1992) Gills and lungs: the exchange of gases and ions. In: Harrison WF, Humes AG (eds) Microscopic anatomy of invertebrates. Wiley-Liss, New York, pp 203–293

    Google Scholar 

  • Towle DW, Smith CM (2006) Gene discovery in Carcinus maenas and Homarus americanus via expressed sequence tags. Integr Comp Biol 46:912–918

    Article  PubMed  CAS  Google Scholar 

  • Towle DW, Rushton ME, Heidysch D, Magnani JJ, Rose MJ, Amstutz A, Jordan MK, Shearer DW, Wu WS (1997) Sodium/proton antiporter in the euryhaline crab Carcinus maenas: molecular cloning, expression and tissue distribution. J Exp Biol 200(Pt 6):1003–1014

    PubMed  CAS  Google Scholar 

  • Towle DW, Paulsen RS, Weihrauch D, Kordylewski M, Salvador C, Lignot JH, Spanings-Pierrot C (2001) Na(+) + K(+)-ATPase in gills of the blue crab Callinectes sapidus: cDNA sequencing and salinity-related expression of alpha-subunit mRNA and protein. J Exp Biol 204:4005–4012

    Google Scholar 

  • Tsai JR, Lin HC (2014) Functional anatomy and ion regulatory mechanisms of the antennal gland in a semi-terrestrial crab, Ocypode stimpsoni. Biol Open 3:409–417

    Google Scholar 

  • Weihrauch D (1999) Zur Stickstoff-Exkretion aquatischer Brachyuren: Carcinus maenas (Linnaeus 1758, Decapoda, Portunidae), Cancer pagurus Linnaeus 1758 (Decapoda, Cancridae) und Eriocheir sinensis H. Milne Edwards 1853 (Decapoda, Grapsidae). Verlag fuer Wissenschaft und Forschung, Berlin

    Google Scholar 

  • Weihrauch D (2006) Active ammonia absorption in the midgut of the Tobacco hornworm Manduca sexta L.: Transport studies and mRNA expression analysis of a Rhesus-like ammonia transporter. Insect Biochem Mol Biol 36:808–821

    Google Scholar 

  • Weihrauch D, O’Donnell MJ (2015) Links between Osmoregulation and Nitrogen-Excretion in Insects and Crustaceans. Integr Comp Biol 55(5):816–829

    Article  PubMed  CAS  Google Scholar 

  • Weihrauch D, Becker W, Postel U, Riestenpatt S, Siebers D (1998) Active excretion of ammonia across the gills of the shore crab Carcinus maenas and its relation to osmoregulatory ion uptake. J Comp Physiol B 168:364–376

    Article  CAS  Google Scholar 

  • Weihrauch D, Becker W, Postel U, Luck-Kopp S, Siebers D (1999a) Potential of active excretion of ammonia in three different haline species of crabs. J Comp Physiol B 169:25–37

    Article  CAS  Google Scholar 

  • Weihrauch D, Siebers D, Towle D (1999b) High levels of urea maintained in the hemolymph of the ammoniotelic euryhaline crabs Carcinus maenas and Eriocheir sinensis. In: Hochachka PW, Mommsen TP (eds) Fifth International Congress of Comparative Physiology and Biochemistry. Elsevier, Calgary/Alberta, p S81

    Google Scholar 

  • Weihrauch D, Ziegler A, Siebers D, Towle DW (2001) Molecular characterization of V-type H(+)-ATPase (B-subunit) in gills of euryhaline crabs and its physiological role in osmoregulatory ion uptake. J Exp Biol 204:25–37

    Google Scholar 

  • Weihrauch D, Ziegler A, Siebers D, Towle DW (2002) Active ammonia excretion across the gills of the green shore crab Carcinus maenas: participation of Na(+)/K(+)-ATPase, V-type H(+)-ATPase and functional microtubules. J Exp Biol 205:2765–2775

    Google Scholar 

  • Weihrauch D, McNamara JC, Towle DW, Onken H (2004a) Ion-motive ATPases and active, transbranchial NaCl uptake in the red freshwater crab, Dilocarcinus pagei (Decapoda, Trichodactylidae). J Exp Biol 207:4623–4631

    Google Scholar 

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

    Article  PubMed  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  PubMed  CAS  Google Scholar 

  • Weihrauch D, Chan AC, Meyer H, Doring C, Sourial MM, O’Donnell MJ (2012) Ammonia excretion in the freshwater planarian Schmidtea mediterranea. J Exp Biol 215:3242–3253

    Google Scholar 

  • Young-Lai WW, Charmantier-Daures M, Charmantier G (1991) Effect of ammonia on survival and osmoregulation in different life stages of the lobster Homarus americanus. Mar Biol 110:293–300

    Article  CAS  Google Scholar 

  • Zachos NC, Tse M, Donowitz M (2005) Molecular physiology of intestinal Na+/H+ exchange. Annu Rev Physiol 67:411–443

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Biological Sciences, University of Manitoba, Winnipeg, MB, Canada

    Dirk Weihrauch & Alex Quijada-Rodriguez

  2. Department of Zoology, University of British Columbia, #4200-6270 University Blvd., Vancouver, BC, V6T 1Z4, Canada

    Sandra Fehsenfeld

Authors
  1. Dirk Weihrauch
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Sandra Fehsenfeld
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Alex Quijada-Rodriguez
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Dirk Weihrauch .

Editor information

Editors and Affiliations

  1. University of Manitoba, Winnipeg, Manitoba, Canada

    Dirk Weihrauch

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

    Michael O’Donnell

Rights and permissions

Reprints and permissions

Copyright information

© 2017 Springer International Publishing Switzerland

About this chapter

Cite this chapter

Weihrauch, D., Fehsenfeld, S., Quijada-Rodriguez, A. (2017). Nitrogen Excretion in Aquatic Crustaceans. In: Weihrauch, D., O’Donnell, M. (eds) Acid-Base Balance and Nitrogen Excretion in Invertebrates. Springer, Cham. https://doi.org/10.1007/978-3-319-39617-0_1

Download citation

Publish with us

Policies and ethics

Search

Navigation