Journal of Comparative Physiology B

, Volume 175, Issue 1, pp 67–75

Diel variation in ammonia excretion, glutamine levels, and hydration status in two species of terrestrial isopods

Original Paper


Terrestrial isopods (suborder Oniscidea) excrete most nitrogen diurnally as volatile ammonia, and ammonia-loaded animals accumulate nonessential amino acids, which may constitute the major nocturnal nitrogen pool. This study explored the relationship between ammonia excretion, glutamine storage/mobilization, and water balance, in two sympatric species Ligidium lapetum (section Diplocheta), a hygric species; and Armadillidium vulgare (Section Crinocheta), a xeric species capable of water-vapor absorption (WVA). Ammonia excretion (12-h), tissue glutamine levels, and water contents were measured following field collection of animals at dusk and dawn. In both species, diurnal ammonia excretion exceeded nocturnal excretion four- to fivefold while glutamine levels increased four- to sevenfold during the night. Most glutamine was accumulated in the somatic tissues (“body wall”). While data support the role of glutamine in nocturnal nitrogen storage, potential nitrogen mobilization from glutamine breakdown (162 μmol g−1 in A. vulgare) exceeds measured ammonia excretion (2.5 μmol g−1) over 60-fold. This may serve to generate the high hemolymph ammonia concentrations \(({\text{and high}}\;P_{{\text{NH}}_3 } )\) seen during volatilization. The energetic cost of ammonia volatilization is discussed in the light of these findings. Mean water contents were similar at dusk and dawn in both species, indicating that diel cycles of water depletion and replenishment were not occurring.


Glutamine Ammonia Excretion Isopod Onsicidea 


  1. Bishop SH, Ellis LL, Burcham JM (1983) Amino acid metabolism in molluscs. In: Hochachka PW (ed) The Mollusca, vol 1. Academic, New York, pp 243–327Google Scholar
  2. Burcham JM, Grenwaldt DE, Bishop SH (1980) Amino acid metabolism in euryhaline bivalves: the L-amino acid oxidase from ribbed mussel gill tissue. Mar Biol Lett 1:329–340Google Scholar
  3. Campbell JW (1991) Excretory nitrogen metabolism. In: Ladd Prosser C (ed) Environmental and metabolic animal physiology, 4th edn. Wiley-Liss, New York, pp 277–324Google Scholar
  4. Campbell JW (1995) Excretory nitrogen metabolism in reptiles and birds. In: Walsh PJ, Wright P (eds) Nitrogen metabolism and excretion, chap. 10. CRC Press, Boca Raton, pp 147–178Google Scholar
  5. Claybrook DL (1983) Nitrogen metabolism. In: Mantel LH (ed) Biology of Crustacea, vol 5, chap. 3. Academic, New York, pp 163–213Google Scholar
  6. Cochran DG (1985) Nitrogenous excretion. In: Kerkut GA, Gilbert LI (eds) Comprehensive insect physiology, biochemistry and pharmacology. Regulation, digestion, nutrition and excretion, vol 4. Pergamon Press, Oxford, pp 467–506Google Scholar
  7. De Vries MC, Wolcott DL (1993) Gaseous ammonia evolution is coupled to reprocessing of urine at the gills of ghost crabs. J Exp Zool 267:97–103Google Scholar
  8. DeFur PL, McMahon BR (1984) Physiological compensation to short-term air exposure in red rock crabs Cancer productus Randall, from littoral and sublittoral habitats. II. Acid-base balance. Physiol Zool 57:151–160Google Scholar
  9. Den Boer PJ (1961) The ecological significance of activity patterns in the woodlouse Porcellio scaber Latr. (Isopoda). Arch Néerl Zool 14:283–409Google Scholar
  10. Dresel EB, Moyle V (1950) Nitrogenous excretion in amphipods and isopods. J Exp Biol 27:210–225PubMedGoogle Scholar
  11. Durand F, Regnault M (1998) Nitrogen metabolism in two portunid crabs, Carcinus maenas and Necora puber, during prolonged air exposure and subsequent recovery: a comparative study. J Exp Biol 201:2515–2528PubMedGoogle Scholar
  12. Durand F, Chausson F, Regnault M (1999) Increases in tissue free amino acid levels in response to prolonged emersion in marine crabs an ammonia-detoxifying process efficient in the intertidal Carcinus maenas but not in the subtidal Necora puber. J Exp Biol 202:2191–2202PubMedGoogle Scholar
  13. Greenaway P (1991) Nitrogenous excretion in aquatic and terrestrial Crustacea. Mem Queensland Mus 31:215–227Google Scholar
  14. Harris RR, Andrews MB (1985) Total NPS pool and ammonia net efflux rate changes in Carcinus maenas during acclimation to low environmental salinity. Comp Biochem Physiol A 82:301–308CrossRefGoogle Scholar
  15. Harrison JF (1995) Nitrogen metabolism and excretion in locusts. In: Walsh PJ, Wright P (eds) Nitrogen metabolism and excretion, chap 8. CRC Press, Boca Raton, pp 119–131Google Scholar
  16. Hartenstein R (1968) Nitrogen metabolism in the terrestrial isopod Oniscus asellus. Am Zool 8:507–519PubMedGoogle Scholar
  17. Holdich DM, Mayes KR (1976) Blood volume and total water content of the woodlouse, Oniscus asellus, in conditions of hydration and desiccation. J Insect Physiol 27:547–553CrossRefGoogle Scholar
  18. Khademi S, O’Connell J, REmis J, Robles-Colmenares Y, Miercke LJW, Stroud RM (2004) Mechanism of ammonia transport by Amt/MEP/Rh: structure of AmtB at 1/.35 Å. Science 305:1587–1594CrossRefPubMedGoogle Scholar
  19. King FD, Cucci TL, Bidigare RR (1985) A pathway of nitrogen metabolism in marine decapod crabs. Comp Biochem Physiol 80B:401–403CrossRefGoogle Scholar
  20. Kirby PK, Harbaugh RD (1974) Diurnal patterns of ammonia release in marine and terrestrial isopods. Comp Biochem Physiol 47A:1313–1322CrossRefGoogle Scholar
  21. Kleinschuster SJ, Morris JE (1972) Glutamine synthetase, an enzyme characteristic of vertebrate systems in invertebrate tissues. Experientia 38(10):1157–1158Google Scholar
  22. Kormanik GA, Cameron JN (1981) Ammonia excretion in animals that breathe water: a review. Mar Biol Lett 2:11–23Google Scholar
  23. Lund P (1986) L-glutamine and L-glutamate: UV-method with glutaminase and glutamate dehydrogenase. In: Bergmeyer HU (ed) Methods of enzymatic analysis, vol 8. VCH Verlagsgesellschaft, Weinheim, pp 357–363Google Scholar
  24. Marini AM, Soussi-Boudekou S, Vissers S, Andre B (1997) A family of ammonium transporters in Saccharomyces cerevisiae. Mol Cell Biol 17:4282–4293PubMedGoogle Scholar
  25. Mondzac A, Ehrlich GE, Seegmiller JE (1965) An enzymatic determination of ammonia in biological fluids. J Lab Clin Med 66:526–533PubMedGoogle Scholar
  26. Needham J (1938) Contributions of chemical physiology to the problems of reversal in evolution. Biol Rev 13:225–251Google Scholar
  27. Nelson DL, Lehninger AL, Cox MM (2000) Lehninger principles of biochemistry, 3rd edn. Worth Publishing, New YorkGoogle Scholar
  28. O’Donnell MJ, Wright JC (1995) Nitrogen excretion in terrestrial crustaceans. In: Walsh PJ, Wright P (eds) Nitrogen metabolism and excretion, chap 7. CRC Press, Boca Raton, pp 105–118Google Scholar
  29. Paris OH (1963) The ecology of Armadillidium vulgare in California grassland: food enemies and weather. Ecol Monogr 23:1–22Google Scholar
  30. Regnault M (1992) Effects of air exposure on nitrogen metabolism in the crab Cancer pagurus. J Exp Zool 264:372–380PubMedGoogle Scholar
  31. Schmidt ASC, Uglow RF (1997) Haemolymph constituent levels and ammonia efflux rates of Nephrops norvegicus during emersion. Mar Biol 127:403–410CrossRefGoogle Scholar
  32. Sreenivasula RP, Bhagyalakshmi A (1994) Changes in oxidative metabolism in selected tissues of the crab (Scylla serrata) in response to cadmium toxicity. Ecotoxicol Environ Safety 29:255–264PubMedGoogle Scholar
  33. 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 205:2765–2775PubMedGoogle Scholar
  34. Wieser W (1972a) Oxygen consumption and ammonia excretion in Ligia beaudiniana M.-E. Comp Biochem Physiol 43A:869–876CrossRefGoogle Scholar
  35. Wieser W (1972b) A glutaminase in the body wall of terrestrial isopods. Nature 239:288–290Google Scholar
  36. Wieser W, Schweizer G (1970) A re-examination of the excretion of nitrogen by terrestrial isopods. J Exp Biol 52:267–274Google Scholar
  37. Wieser W, Schweizer G (1972) Der Gehalt an Ammoniak und Freien Aminosuren sowie die Eigenschaften einer Glutaminase bei Porcellio scaber (Isopoda). J Comp Physiol B 81:73–88Google Scholar
  38. Wieser W, Schweizer G, Hartenstein R (1969) Patterns in the release of ammonia by terrestrial isopods. Oecologia 3:390–400CrossRefGoogle Scholar
  39. Wright PA (1995) Nitrogen excretion: three end products, many physiological roles. J Exp Biol 198:273–281PubMedGoogle Scholar
  40. Wright JC, Machin J (1990) Water vapour absorption in terrestrial isopods. J Exp Biol 154:13–30Google Scholar
  41. Wright JC, Machin J (1993a) Energy-dependent water vapour absorption (WVA) in the pleoventral cavity of terrestrial isopods (Crustacea, Isopoda, Oniscidea): evidence for pressure cycling as a supplement to the colligative uptake mechanism. Physiol Zool 66:193–215Google Scholar
  42. Wright JC, Machin J (1993b) Atmospheric water vapour absorption and the water budget of terrestrial isopods. Biol Bull 184:243–253Google Scholar
  43. Wright JC, O’Donnell MJ (1993) Total ammonia concentration and pH of haemolymph, pleon fluid and maxillary urine in Porcellio scaber Latreille (Isopoda, Oniscidea): relationship to ambient humidity and water vapour uptake. J Exp Biol 176:233–246Google Scholar
  44. Wright JC, O’Donnell MJ, Reichert J (1994) Effects of ammonia loading on Porcellio scaber: glutamine and glutamate synthesis, ammonia excretion and toxicity. J Exp Biol 188:143–157PubMedGoogle Scholar
  45. Wright JC, Caveney S, O’Donnell MJ, Reichert J (1996) Changes in tissue amino acid levels in response to ammonia-stress in the terrestrial isopod Porcellio scaber Latr. J Exp Zool 274:265–274Google Scholar
  46. Wright JC, O’Donnell MJ, Sazgar S (1997) Haemolymph osmoregulation and the fate of sodium and chloride during dehydration in terrestrial isopods. J Insect Physiol 45:795–807CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2004

Authors and Affiliations

  1. 1.Department of BiologyPomona CollegeClaremontUSA

Personalised recommendations