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Journal of Comparative Physiology B

, Volume 177, Issue 8, pp 917–926 | Cite as

Osmotic and metabolic responses to dehydration and urea-loading in a dormant, terrestrially hibernating frog

  • Timothy J. Muir
  • Jon P. Costanzo
  • Richard E. LeeJr
Original Paper

Abstract

Physiological responses to dehydration in amphibians are reasonably well documented, although little work has addressed this problem in hibernating animals. We investigated osmotic and metabolic responses to experimental manipulation of hydration state in the wood frog (Rana sylvatica), a terrestrial hibernator that encounters low environmental water potential during autumn and winter. In winter-conditioned frogs, plasma osmolality varied inversely with body water content (range 69–79%, fresh mass) primarily due to increases in sodium and chloride concentrations, as well as accumulation of glucose and urea. Decreased hydration was accompanied by a marked reduction in the resting rate of oxygen consumption, which was inversely correlated with plasma osmolality and urea concentration. In a separate experiment, resting rates of oxygen consumption in fully hydrated frogs receiving injections of saline or saline containing urea did not differ initially; however, upon dehydration, metabolic rates decreased sooner in the urea-loaded frogs than in control frogs. Our findings suggest an important role for urea, acting in concert with dehydration, in the metabolic regulation and energy conservation of hibernating R. sylvatica.

Keywords

Metabolism Urea Dehydration Hibernation Rana sylvatica 

References

  1. Arad Z (2001) Desiccation and rehydration in land snails—a test for distinct set points in Theba pisana. Isr J Zool 47:41–53Google Scholar
  2. Baldwin RF, Calhoun AJK, DeMaynader PG (2006) Conservation planning for amphibian species with complex habitat requirements: a case study using movements and habitat selection of the wood frog Rana sylvatica. J Herpetol 40:442–453CrossRefGoogle Scholar
  3. Balinsky JB (1981) Adaptation of nitrogen metabolism to hypertonic environment in Amphibia. J Exp Zool 215:335–350CrossRefGoogle Scholar
  4. Chew SF, Chan NKY, Loong AM, Hiong KC, Tam WL, Ip YK (2004) Nitrogen metabolism in the African lungfish (Protopterus dolloi) aestivating in a mucus cocoon on land. J Exp Biol 207:777–786PubMedCrossRefGoogle Scholar
  5. Churchill TA, Storey KB (1993) Dehydration tolerance in wood frogs: a new perspective on development of amphibian freeze tolerance. Am J Physiol 265:R1324–R1332PubMedGoogle Scholar
  6. Costanzo JP, Lee RE (2005) Cryoprotection by urea in a terrestrially hibernating frog. J Exp Biol 208:4079–4089PubMedCrossRefGoogle Scholar
  7. Costanzo JP, Lee RE, Lortz PH (1993) Physiological responses of freeze-tolerant and -intolerant frogs: clues to evolution of anuran freeze tolerance. Am J Physiol 265:R721–R725PubMedGoogle Scholar
  8. Cowan KJ, Storey KB (2002) Urea and KCl have different effects on enzyme activities in liver and muscle of estivating versus nonestivating species. Biochem Cell Biol 80:745–755PubMedCrossRefGoogle Scholar
  9. Edwards JR, Jenkins JL, Swanson DL (2004) Seasonal effects of dehydration on glucose mobilization in freeze-tolerant chorus frogs (Pseudacris triseriata) and freeze-intolerant toads (Bufo woodhousii and B. cognatus). J Exp Zool 301A:521–531CrossRefGoogle Scholar
  10. Flanigan JE, Withers PC, Guppy M (1991) In vitro metabolic depression of tissues from the aestivating frog Neobatrachus pelobatoides. J Exp Biol 161:273–283Google Scholar
  11. Fuery CJ, Attwood PV, Withers PC, Yancey PH, Baldwin J, Guppy M (1997) Effects of urea on M4-lactate dehydrogenase from elasmobranchs and urea-accumulating Australian desert frogs. Comp Biochem Physiol B 117:143–150PubMedCrossRefGoogle Scholar
  12. Garcia-Romeu F, Masoni A, Isaia J (1981) Active urea transport through isolated skins of frog and toad. Am J Physiol 241:114–123Google Scholar
  13. Gatten REJ (1987) Activity metabolism of anuran amphibians: tolerance to dehydration. Physiol Zool 60:576–585Google Scholar
  14. Gil N, Katz U (1996) Oxygen consumption, heart rate and respiratory movements are maintained almost unchanged in toads (Bufo viridis) on soil without access to free water. J Arid Environ 33:237–245CrossRefGoogle Scholar
  15. Grundy JE, Storey KB (1994) Urea and salt effects on enzymes from estivating and non-estivating amphibians. Mol Cell Biochem 131:9–17PubMedCrossRefGoogle Scholar
  16. Hand SC, Somero GN (1982) Urea and methylamine effects on rabbit muscle phosphofructokinase. J Biol Chem 257:734–741PubMedGoogle Scholar
  17. Hillman SS (1978a) The roles of oxygen delivery and electrolyte levels in the dehydrational death of Xenopus laevis. J Comp Physiol 128:169–175Google Scholar
  18. Hillman SS (1978b) Some effects of dehydration on internal distributions of water and solutes in Xenopus laevis. Comp Biochem Physiol 61:303–307CrossRefGoogle Scholar
  19. Hillman SS (1987) Dehydrational effects on cardiovascular and metabolic capacity in two amphibians. Physiol Zool 60:608–613Google Scholar
  20. Hochachka PW, Somero GN (2002) Biochemical adaptation. Oxford University Press, New YorkGoogle Scholar
  21. Jørgensen CB (1997a) 200 years of amphibian water economy: from Robert Townson to the present. Biol Rev 72:153–237PubMedCrossRefGoogle Scholar
  22. Jørgensen CB (1997b) Urea and amphibian water economy. Comp Biochem Physiol A 117:161–170CrossRefGoogle Scholar
  23. Kaji DM, Lim J, Shilkoff W, Zaidi W (1998) Urea inhibits the Na–K pump in human erythrocytes. J Membr Biol 165:125–131PubMedCrossRefGoogle Scholar
  24. Katz U, Hoffman J (1990) Changing plasma osmolality—a strategy of adaptation in anuran amphibia to water scarcity under burrowing conditions. In: Hanke W (eds) Biology and physiology of amphibians. Gutav Fischer Verlag, New York, pp 350–356Google Scholar
  25. Kennett R, Christian K (1994) Metabolic depression in estivating long-neck turtles (Chelodina rugosa). Physiol Zool 67:1087–1102Google Scholar
  26. Layne JR Jr, Lee RE (1987) Freeze tolerance and the dynamics of ice formation in wood frogs (Rana sylvatica) from southern Ohio. Can J Zool 65:2062–2065CrossRefGoogle Scholar
  27. Layne JR, Rice ME (2003) Postfreeze locomotion performance in wood frogs (Rana sylvatica) and spring peepers (Pseudacris crucifer). Can J Zool 81:2061–2065CrossRefGoogle Scholar
  28. Loong AM, Hiong KC, Lee SML, Wong WP, Chew SF, Ip YK (2005) Ornithine-urea cycle and urea synthesis in African lungfishes, Protopterus aethiopicus and Protopterus annectens, exposed to terrestrial conditions for six days. J Exp Zool 303A:354–365CrossRefGoogle Scholar
  29. McDonald MD, Smith CP, Walsh PJ (2006) The physiology and evolution of urea transport in fishes. J Membr Biol 212:93–107PubMedCrossRefGoogle Scholar
  30. Pinder AW, Storey KB, Ultsch GR (1992) Estivation and hibernation. In: Feder ME, Burggren WW (eds) Environmental physiology of the amphibians. The University of Chicago Press, Chicago, pp 250–274Google Scholar
  31. Preest MR, Brust DG, Wygoda ML (1992) Cutaneous water loss and the effects of temperature and hydration state on aerobic metabolism of canyon treefrogs, Hyla arenicolor. Herpetologica 48:210–219Google Scholar
  32. Rees BB, Hand SC (1993) Biochemical correlates of estivation tolerance in the mountainsnail Oreohelix (Pulmonata: Oreohelicidae). Biol Bull 184:230–242CrossRefGoogle Scholar
  33. Regosin JV, Windmiller BS, Reed JM (2003) Terrestrial habitat use and winter densities of the wood frog (Rana sylvatica). J Herpetol 37:390–394CrossRefGoogle Scholar
  34. Schmid WD (1965) Some aspects of the water economy of nine species of amphibians. Ecology 46:261–269CrossRefGoogle Scholar
  35. Secor SM (2005) Physiological responses to feeding, fasting and estivation for anurans. J Exp Biol 208:2595–2608PubMedCrossRefGoogle Scholar
  36. Shoemaker VH (1964) The effects of dehydration on electrolyte concentrations in a toad, Bufo marinus. Comp Biochem Physiol 13:261–271PubMedCrossRefGoogle Scholar
  37. Shoemaker VH, Hillman SS, Hillyard SD, Jackson DC, McClanahan LL, Withers PC, Wygoda ML (1992) Exchange of water, ions, and respiratory gases in terrestrial amphibians. In: Feder ME, Burggren WW (eds) Environmental physiology of the amphibians. The University of Chicago Press, Chicago, pp 125–150Google Scholar
  38. Shpun S, Hoffman J, Katz U (1992) Anuran Amphibia which are not acclimable to high salt, tolerate high plasma urea. Comp Biochem Physiol A 103:473–477CrossRefGoogle Scholar
  39. Somero GN (1986) Protons, osmolytes, and fitness of internal milieu for protein function. Am J Physiol 251:R197–R213PubMedGoogle Scholar
  40. Spaans EJA, Baker JM (1996) The soil freezing characteristic: its measurement and similarity to the soil moisture characteristic. Soil Sci Soc Am J 60:13–19CrossRefGoogle Scholar
  41. Spotila JR, O’Connor MP, Bakken GS (1992) Biophysics of heat and mass transfer. In: Feder ME, Burggren WW (eds) Evironmental physiology of the amphibians. The University of Chicago Press, Chicago, pp 59–80Google Scholar
  42. Vleck D (1987) Measurement of O2 consumption, CO2 production, and water vapor production in a closed system. J Appl Physiol 62:2103–2106PubMedCrossRefGoogle Scholar
  43. Williams JB, Lee RE (2005) Plant senescence cues entry into diapause in the gall fly Eurosta solidaginis: resulting metabolic depression is critical for water conservation. J Exp Biol 208:4437–4444PubMedCrossRefGoogle Scholar
  44. Withers PC, Guppy M (1996) Do Australian desert frogs co-accumulate counteracting solutes with urea during aestivation? J Exp Biol 199:1809–1816PubMedGoogle Scholar
  45. Wray S, Wilkie DR (1995) The relationship between plasma urea levels and some muscle trimethylamine levels in Xenopus laevis: a 31P and 14N Nuclear magnetic resonance study. J Exp Biol 198:373–378PubMedGoogle Scholar
  46. Wright PA (1995) Nitrogen excretion: three end products, many physiological roles. J Exp Biol 198:273–281PubMedGoogle Scholar
  47. Yancey PH, Burg MB (1990) Counteracting effects of urea and betaine on colony-forming efficiency of mammalian cells in culture. Am J Physiol 258:R198–R204PubMedGoogle Scholar
  48. Yancey PH, Clark ME, Hand SC, Bowlus RD, Somero GN (1982) Living with water stress: evolution of osmolyte systems. Science 217:1214–1222PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2007

Authors and Affiliations

  • Timothy J. Muir
    • 1
  • Jon P. Costanzo
    • 1
  • Richard E. LeeJr
    • 1
  1. 1.Department of ZoologyMiami UniversityOxfordUSA

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