Skip to main content
SpringerLink
Log in

Nitrogen Excretion in Nematodes, Platyhelminthes, and Annelids

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

Abstract

Aquatic invertebrates primarily excrete their nitrogenous waste in the form of ammonia, a highly toxic waste product of amino acid catabolism. However, very little is known about the mechanism and for that fact the tissues that are actually responsible for ammonia excretion in freshwater and soil-dwelling invertebrates. This chapter provides an overview of the current literature examining the ammonia excretion mechanisms in three phyla: Nematoda, Platyhelminthes, and Annelida. The introduction will briefly cover the challenges faced by freshwater and soil-dwelling invertebrates in terms of their ionoregulatory capabilities in addition to a general overview of nitrogenous waste excretion in aquatic invertebrates. Subsequently, nitrogenous waste excretion in the nematodes, annelids, and platyhelminthes will be discussed with an emphasis placed on the potential tissues involved in ammonia excretion, e.g., the nephridial system, epidermis, hypodermis, intestine, and the nematode-specific excretory system. This chapter will also provide an extensive review of the cutaneous ammonia excretion mechanism in two freshwater representatives of the phyla Annelida and Platyhelminthes, the ribbon leech (Nephelopsis obscura) and planarian (Schmidtea mediterranea). Additionally, the mechanisms of hypodermal ammonia excretion in the soil nematode (Caenorhabditis elegans) will be discussed in comparison with the mechanisms seen in N. obscura and S. mediterranea. Here a focus will be placed on the role of Na+/K+-ATPase, Na+/H+ exchangers (NHEs), H+-ATPase, Rhesus (Rh) proteins, and vesicular transport. With increasing studies on freshwater and soil-dwelling invertebrates, common mechanisms to that seen in more widely studied vertebrates are becoming more and more evident.

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, Weihrauch D, O’Donnell MJ (2014) Localization of K+, H+, Na+ and Ca2+ fluxes to the excretory pore in Caenorhabditis elegans: application of scanning ion-selective microelectrodes. J Exp Biol 217:4119–4122

    Google Scholar 

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

    Google Scholar 

  • Adlimoghaddam A, Donnell MJO, Kormish J, Banh S, Treberg JR, Merz D, Weihrauch D (2016) Ammonia excretion in Caenorhabditis elegans: physiological and molecular characterization of the rhr-2 knock-out mutant. Comp Biochem Physiol Part A 195:46–54

    Google Scholar 

  • Ahmed ST, Rahemo ZIF (2013) Studies on the histology of the body wall of two species of leeches, Erpobdella octoculata and Haemopis sanguisuga (Annelida: Hirudinea). Adv J Biol Sci Res 1:1–7

    Google Scholar 

  • Anderson WG, McCabe C, Brandt C, Wood CM (2015) Examining urea flux across the intestine of the spiny dogfish, Squalus acanthias. Comp Biochem Physiol A Mol Integr Physiol 181:71–78

    Google Scholar 

  • Avella M, Bornancin M (1989) A new analysis of ammonia and sodium transport through the gills of the freshwater rainbow trout (Salmo gairdneri). J Exp Biol 142:155–175

    Google Scholar 

  • Bianchini A, Wood CM (2008) Sodium uptake in different life stages of crustaceans: the water flea Daphnia magna Strauss. J Exp Biol 211:539–547

    Google Scholar 

  • Boisen AM, Amstrup J, Novak I, Grosell M (2003) Sodium and chloride transport in soft water and hard water acclimated zebrafish (Danio rerio). Biochim Biophys Acta – Biomembr 1618:207–218

    Google Scholar 

  • Boucher-Rodoni R, Mangold K (1989) Respiration and nitrogen excretion by the squid Loligo forbesi. Mar Biol 103:333–338

    Google Scholar 

  • Braissant O, McLin VA, Cudalbu C (2013) Ammonia toxicity to the brain. J Inherit Metab Dis 36:595–612

    Article  PubMed  CAS  Google Scholar 

  • Braun MH, Steele SL, Perry SF (2009) The responses of zebrafish (Danio rerio) to high external ammonia and urea transporter inhibition: nitrogen excretion and expression of rhesus glycoproteins and urea transporter proteins. J Exp Biol 212:3846–3856

    Google Scholar 

  • Britto DT, Kronzucker HJ (2002) NH4 + toxicity in higher plants: a critical review. J Plant Physiol 159:567–584

    Google Scholar 

  • Brusca RC, Brusca G (2003) Invertebrates, 2nd edn. Sinauer Associates, Sunderland, MA

    Google Scholar 

  • Bury NR, Wood CM (1999) Mechanism of branchial apical silver uptake by rainbow trout is via the proton-coupled Na+ channel. Am J Physiol – Regul Integr Comp Physiol 277:R1385–R1391

    Google Scholar 

  • Cohen S, Lewis H (1949) The nitrogenous metabolism of the earthworm (Lumbricus terrestris). J Biol Chem 180:79–91

    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 

  • Diets TH, Alvarado RH (1970) Osmotic and ionic regulation in Lumbricus terrestris L. Biol Bull 138:247–261

    Google Scholar 

  • Duerr FG (1968) Excretion of ammonia and urea in seven species of marine prosobranch snails. Comp Biochem Physiol 26:1051–1059

    Article  CAS  Google Scholar 

  • Dy DT, Yap HT (2000) Ammonium and phosphate excretion in three common echinoderms from Philippine coral reefs. J Exp Mar Bio Ecol 251:227–238

    Article  PubMed  CAS  Google Scholar 

  • Dymowska AK, Schultz AG, Blair SD, Chamot D, Goss GG (2014) Acid-sensing ion channels are involved in epithelial Na+ uptake in the rainbow trout Oncorhynchus mykiss. Am J Physiol Cell Physiol 307:C255–C265

    Google Scholar 

  • Edwards SL, Tse CM, Toop T (1999) Immunolocalisation of NHE3-like immunoreactivity in the gills of the rainbow trout (Oncorhynchus mykiss) and the blue-throated wrasse (Pseudolabrus tetrious). J Anat 195:465–469

    Google Scholar 

  • Endeward V, Cartron JP, Ripoche P, Gros G (2007) RhAG protein of the Rhesus complex is a CO2 channel in the human red cell membrane. FASEB J 22:64–73

    Google Scholar 

  • Glover CN, Bucking C, Wood CM (2013) The skin of fish as a transport epithelium: a review. J Comp Physiol B 183:877–891

    Article  PubMed  CAS  Google Scholar 

  • Gruswitz F, Chaudhary S, Ho JD, Schlessinger A, Pezeshki B, Ho C, Sali A, Westhoff CM, Stroud RM (2010) Function of human Rh based on structure of RhCG at 2.1 Ã…. Proc Natl Acad Sci U S A 107(21):9638–9643

    Article  PubMed  PubMed Central  Google Scholar 

  • Gu R, Duan F, An X, Zhang F, von Wirén N, Yuan L (2013) Characterization of AMT-mediated high-affinity ammonium uptake in roots of maize (Zea mays L.). Plant Cell Physiol 54:1515–1524

    Article  PubMed  CAS  Google Scholar 

  • Handlogten ME, Hong S, Zhang L, Vander AW, Steinbaum ML, Campbell-thompson M, Weiner ID, Mary E, Allen W (2005) Expression of the ammonia transporter proteins Rh B glycoprotein and Rh C glycoprotein in the intestinal tract. Am J Physiol Gastrointest Liver Physiol 288(5):1036–1047

    Article  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Hiroi J, Yasumasu S, McCormick SD, Hwang PP, Kaneko T (2008) Evidence for an apical Na-Cl cotransporter involved in ion uptake in a teleost fish. J Exp Biol 211:2584–2599

    Article  PubMed  CAS  Google Scholar 

  • Hoeger U, Mommsen TP, O’Dors R, Webber D (1987) Oxygen uptake and nitrogen excretion in two cephalopods, octopus and squid. Comp Biochem Physiol 87A:63–67

    Article  CAS  Google Scholar 

  • Horng JL, Lin LY, Huang CJ, Katoh F, Kaneko T, Hwang PP (2007) Knockdown of V-ATPase subunit A (atp6v1a) impairs acid secretion and ion balance in zebrafish (Danio rerio). Am J Physiol Regul Integr Comp Physiol 292:R2068–R2076

    Google Scholar 

  • Horng JL, Hwang PP, Shih TH, Wen ZH, Lin CS, Lin LY (2009) Chloride transport in mitochondrion-rich cells of euryhaline tilapia (Oreochromis mossambicus) larvae. Am J Physiol Cell Physiol 297:C845–C854

    Google Scholar 

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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Hwang PP (2009) Ion uptake and acid secretion in zebrafish (Danio rerio). J Exp Biol 212:1745–1752

    Google Scholar 

  • Hwang PP, Lee TH, Lin LY (2011) Ion regulation in fish gills: recent progress in the cellular and molecular mechanisms. Am J Physiol Regul Integr Comp Physiol 301:R28–R47

    Article  PubMed  CAS  Google Scholar 

  • Inokuchi M, Hiroi J, Watanabe S, Lee KM, Kaneko T (2008) Gene expression and morphological localization of NHE3, NCC and NKCC1a in branchial mitochondria-rich cells of Mozambique tilapia (Oreochromis mossambicus) acclimated to a wide range of salinities. Comp Biochem Physiol A Mol Integr Physiol 151:151–158

    Google Scholar 

  • Inokuchi M, Hiroi J, Watanabe S, Hwang PP, Kaneko T (2009) Morphological and functional classification of ion-absorbing mitochondria-rich cells in the gills of Mozambique tilapia. J Exp Biol 212:1003–1010

    Article  PubMed  CAS  Google Scholar 

  • Ji Q, Hashmi S, Liu Z, Zhang J, Chen Y, Huang CH (2006) CeRh1 (rhr-1) is a dominant Rhesus gene essential for embryonic development and hypodermal function in Caenorhabditis elegans. Proc Natl Acad Sci U S A 103:5881–5886

    Google Scholar 

  • Kerstetter TH, Kirschner LB, Rafuse DD (1970) On the mechanisms of sodium ion transport by the irrigated gills of rainbow trout (Salmo gairdneri). J Gen Physiol 56:342–359

    Google Scholar 

  • Khademi S, O’Connell J III, Remis J, Robles-Colmenares Y, Miercke LJW, Stroud RM (2004) Mechanism of ammonia transport by Amt/MEP/Rh: structure of AmtB at 1.35 A. Science 305:1587–1594

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Kleyman TR, Cragoe EJ (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, Packer R, Good DW (1989) Ammonium transport in the kidney. Physiol Rev 69:179–249

    PubMed  CAS  Google Scholar 

  • Krogh A (1938) The active absorption of ions in some freshwater animals. Zeitschrift Vergleichende Physiol 25:335–350

    Google Scholar 

  • Kulkarni G, Kulkarni V, Rao AB (1989) Nephridial excretion of ammonia and urea in the freshwater leech, Poecilobdella viridis as a function of the temperature and photoperiod. Proc Indian Natn Acad B55:345–352

    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 Regul Integr Comp Physiol 301:R1517–R1528

    Google Scholar 

  • Kumai Y, Perry SF (2012) Mechanisms and regulation of Na(+) uptake by freshwater fish. Respir Physiol Neurobiol 184:249–256

    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 

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

    Article  PubMed  CAS  Google Scholar 

  • Lutz P, Siddiq AH (1971) Nonprotein nitrogenous composition of the protonephridial fluid of the trematode Fasciola gigantica. Comp Biochem Physiol 40A:453–457

    Google Scholar 

  • Mallery CH (1983) A carrier enzyme basis for ammonium excretion in teleost gill NH4 + −stimulated Na+ dependent ATPase activity in Opsanus beta. Comp Biochem Physiol 74:889–897

    Google Scholar 

  • Marini A, Matassi G, Raynal V, André B, Cartron J, 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  PubMed  CAS  Google Scholar 

  • Marshall WS (2002) Na(+), Cl(−), Ca(2+) and Zn(2+) transport by fish gills: retrospective review and prospective synthesis. J Exp Zool 293:264–283

    Google Scholar 

  • Martin G (1978) Zoomorphologie a new function of rhabdites: mucus production for ciliary gliding. Zoomorphologie 91:235–248

    Article  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 D, Furriel RP, McNamara J, Mantelatto FL, Leone F (2002) Modulation by ammonium ions of gill microsomal (Na+, K+)-ATPase in the swimming crab Callinectes danae: a possible mechanism for regulation of ammonia excretion. Comp Biochem Physiol Part C Toxicol Pharmacol 132:471–482

    Google Scholar 

  • McKay SJ, Johnsen R, Khattra J, Asano J, Baillie DL, Chan S, Dube N, Fang L, Goszczynski B, Ha E et al (2003) Gene expression profiling of cells, tissues, and developmental stages of the nematode C. elegans. Cold Spring Harb Symp Quant Biol 68:159–169

    Google Scholar 

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

    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  PubMed  CAS  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

    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 

  • Nelson F, Riddle D (1984) Functional study of the Caenorhabditis elegans secretory-excretory system using laser microsurgery. J Exp Zool 231:45–56

    Google Scholar 

  • Nelson FK, Albert PS, Riddle DL (1983) Fine structure of the Caenorhabditis elegans secretory—excretory system. J Ultrastruct Res 82:156–171

    Google Scholar 

  • Nesdoly RG, Van Rees KCJ (1998) Redistribution of extractable nutrients following disc trenching on Luvisols and Brunisols in Saskatchewan. Can J Soil Sci 78(2):367–376

    Article  Google Scholar 

  • O’Donnell MJ (1997) Mechanisms of excretion and ion transport in invertebrates. In: Dantzler WH (ed) Comparative physiology. Oxford University Press, New York, pp 1207–1289

    Google Scholar 

  • Onken H, Mcnamara JC (2002) Hyperosmoregulation in the red freshwater crab Dilocarcinus pagei (Brachyura, Trichodactylidae): structural and functional asymmetries of the posterior gills. J Exp Biol 205:167–175

    Google Scholar 

  • Onken H, Putzenlechner MAX (1995) A V-ATPase drives active, electrogenic and Na + −independent Cl− absorption across the gills of Eriocheir sinensis. J Exp Biol 198:767–774

    Google Scholar 

  • Onken H, Schöbel A, Kraft JAN, Putzenlechner MAX (2000) Active NaCl absorption across split lamellae of posterior gills of the Chinese crab Eriocheir sinensis: stimulation by eyestalk extract. J Exp Biol 203:1373–1381

    Google Scholar 

  • Parks SK, Tresguerres M, Goss GG (2008) Theoretical considerations underlying Na(+) uptake mechanisms in freshwater fishes. Comp Biochem Physiol C Toxicol Pharmacol 148:411–418

    Google Scholar 

  • Patrick ML, Aimanova K, Sanders HR, Gill SS (2006) P-type Na+/K + −ATPase and V-type H + −ATPase expression patterns in the osmoregulatory organs of larval and adult mosquito Aedes aegypti. J Exp Biol 209:4638–4651

    Google Scholar 

  • Peixoto CA, De Souza W (1995) Freeze-fracture and deep-etched view of the cuticle of Caenorhabditis elegans. Tissue Cell 27:561–568

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

    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 309(6):R692–R705. doi:10.1152/ajpregu.00482.2014

  • Reitze M, Schottler UDO (1989) The time dependence of adaption to reduced salinity in the lugworm Arenicola marina L. (Annelida: Polychaeta). Comp Biochem Physiol 93:549–559

    Google Scholar 

  • Riegel BYJA (1968) Analysis of the distribution of sodium, potassium and osmotic pressure in the urine of crayfishes. J Exp Biol 48:587–596

    PubMed  CAS  Google Scholar 

  • Roots BI (1955) The water relations of earthworms II. Resistance to desiccation and immersion, and behaviour when submerged and when allowed choice of environment. J Exp Biol 33:29–44

    Google Scholar 

  • Rothstein M (1963) Nematode biochemistry-III. Excretion products. Comp Biochem Physiol 9:51–59

    Article  PubMed  CAS  Google Scholar 

  • Rubino JG, Zimmer AM, Wood CM (2014) Intestinal ammonia transport in freshwater and seawater acclimated rainbow trout (Oncorhynchus mykiss): evidence for a Na(+) coupled uptake mechanism. Comp Biochem Physiol A Mol Integr Physiol 183C:45–56

    Google Scholar 

  • Sabourin TD, Stickle WB (1981) Effects of salinity on respiration and nitrogen excretion in two species of echinoderms. Mar Biol 65:91–99

    Article  CAS  Google Scholar 

  • Shih TH, Horng JL, Hwang PP, Lin LY (2008) Ammonia excretion by the skin of zebrafish (Danio rerio) larvae. Am J Physiol Cell Physiol 295:C1625–C1632

    Google Scholar 

  • Shih TH, Horng JL, Liu ST, Hwang PP, Lin LY (2012) Rhcg1 and NHE3b are involved in ammonium-dependent sodium uptake by zebrafish larvae acclimated to low-sodium water. Am J Physiol Regul Integr Comp Physiol 302:R84–R93

    Article  PubMed  CAS  Google Scholar 

  • Skou JC (1965) Enzymatic basis for active transport of Na+ and K+ across cell membrane. Physiol Rev 45:596–617

    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 U S A 101:7787–7792

    Google Scholar 

  • Tavakkoli E, Fatehi F, Coventry S, Rengasamy P, McDonald GK (2011) Additive effects of Na+ and Cl−ions on barley growth under salinity stress. J Exp Bot 62:2189–2203

    Google Scholar 

  • Tillinghast EK (1967) Excretory pathways of ammonia and urea in the earthworm Lumbricus terrestris L. J Exp Zool 166:295–300

    Google Scholar 

  • Tillinghast EK, McInnes D, Duffill R (1969) The effect of temperature and water availability on the output of ammonia and urea by the earthworm Lumbricus terrestris L. Comp Biochem Physiol 29:1087–1092

    Google Scholar 

  • Tillinghast EK, O’Donnell R, Eves D, Calvert E, Taylor J (2001) Water-soluble luminal contents of the gut of the earthworm Lumbricus terrestris L. and their physiological significance. Comp Biochem Physiol Part A Mol Integr Physiol 129:345–353

    Google Scholar 

  • Towle DW, Paulsen RS, Weihrauch D, Kordylewski M, Salvador C, Lignot J, Spanings-pierrot C, Island D, Cove S, College LF et al (2001) Na+ + K+ −ATPase in gills of the blue crab Callinectes sapidus: cDNA sequencing and salinity-related expression of α -subunit mRNA and protein. J Exp Biol 204:4005–4012

    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

    Article  PubMed  CAS  Google Scholar 

  • Tresguerres M, Parks SK, Sabatini SE, Goss GG, Luquet CM (2008) Regulation of ion transport by pH and [HCO3-] in isolated gills of the crab Neohelice (Chasmagnathus) granulata. Am J Physiol Regul Integr Comp Physiol 294:R1033–R1043

    Google Scholar 

  • Tschoerner P, Zebe E (1989) Ammonia formation in the medicinal leech, Hirudo medicinalis-in vivo and in vitro investigations. Comp Biochem Physiol 94A:187–194

    Google Scholar 

  • Tsui TKN, Hung CYC, Nawata CM, 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 212:878–892

    Google Scholar 

  • Wall SM, Koger LM (1994) NH4 + transport mediated by Na+ −K+ −ATPase in rat inner medullary collecting duct. Am J Physiol 267:F660–F670

    Google Scholar 

  • Wang YF, Tseng YC, Yan JJ, Hiroi J, Hwang PP (2009) Role of SLC12A10.2, a Na-Cl cotransporter-like protein, in a Cl uptake mechanism in zebrafish (Danio rerio). Am J Physiol Regul Integr Comp Physiol 296:R1650–R1660

    Google Scholar 

  • Weber WM, Blank U, Clauss W (1995) Regulation of electrogenic Na+ transport across leech skin. Am J Physiol Regul Integr Comp Physiol 268:605–613

    Google Scholar 

  • Webster LA, Wilson RA (1970) The chemical composition of protonephridial canal fluid from the cestode Hymenolepis diminuta. Comp Biochem Physiol 35:201–209

    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, 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, Döring C, Sourial M, O’Donnell MJ (2012) Ammonia excretion in the freshwater planarian Schmidtea mediterranea. J Exp Biol 215:3242–3253

    Google Scholar 

  • Weiner ID, Verlander JW (2014) Ammonia transport in the kidney by Rhesus glycoproteins. Am J Physiol Renal Physiol 306:F1107–F1120

    Article  PubMed  PubMed Central  CAS  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  PubMed  CAS  Google Scholar 

  • Wilson RW, Wright PM, Munger S, Wood CM (1994) Ammonia excretion in freshwater 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

    Google Scholar 

  • Wilson JM, Laurent P, Tufts BL, Benos DJ, Donowitz M, Vogl AW, Randall DJ (2000) NaCl uptake by the branchial epithelium in freshwater teleost fish: an immunological approach to ion-transport protein localization. J Exp Biol 203:2279–2296

    PubMed  CAS  Google Scholar 

  • Wilson JM, Moreira-Silva J, Delgado ILS, Ebanks SC, Vijayan MM, Coimbra J, Grosell M (2013) Mechanisms of transepithelial ammonia excretion and luminal alkalinization in the gut of an intestinal air-breathing fish, Misgurnus anguilliacaudatus. J Exp Biol 216:623–632

    Google Scholar 

  • Wood CM, Bucking C (2011) The role of feeding in salt and water balance. In: Grosell M, Farrell AP, Brauner CJ (eds) The multifunctional gut of fish. Academic, Amsterdam/Boston, pp 165–212

    Google Scholar 

  • Wright PA (1995) Nitrogen excretion : three end products, many physiological roles. J Exp Biol 198:273–281

    PubMed  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

    Article  PubMed  CAS  Google Scholar 

  • Wu SC, Horng JL, Liu ST, Hwang PP, Wen ZH, Lin CS, Lin LY (2010) Ammonium-dependent sodium uptake in mitochondrion-rich cells of medaka (Oryzias latipes) larvae. Am J Physiol Cell Physiol 298:C237–C250

    Google Scholar 

  • Zerbst-Boroffka I, Bazin B, Wenning A (1997) Chloride secretion drives urine formation in leech nephridia. J Exp Biol 200:2217–2227

    PubMed  CAS  Google Scholar 

  • Zidi-Yahiaoui N, Callebaut I, Genetet S, Le Van Kim C, Cartron JP, Colin Y, Ripoche P, Mouro-Chanteloup I (2009) Functional analysis of human RhCG: comparison with E. coli ammonium transporter reveals similarities in the pore and differences in the vestibule. Am J Physiol Cell Physiol 297:C537–C547

    Google Scholar 

  • Zimmer AM, Nawata CM, Wood CM (2010) Physiological and molecular analysis of the interactive effects of feeding and high environmental ammonia on branchial ammonia excretion and Na+ uptake in freshwater rainbow trout. J Comp Physiol B 180:1191–1204

    Google Scholar 

Download references

Author information

Authors and Affiliations

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

    Alex R. Quijada-Rodriguez, Aida Adlimoghaddam & Dirk Weihrauch

Authors
  1. Alex R. Quijada-Rodriguez
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Aida Adlimoghaddam
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Dirk Weihrauch
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Alex R. Quijada-Rodriguez .

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

Quijada-Rodriguez, A.R., Adlimoghaddam, A., Weihrauch, D. (2017). Nitrogen Excretion in Nematodes, Platyhelminthes, and Annelids. 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_5

Download citation

Publish with us

Policies and ethics

Search

Navigation