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Oecologia

, Volume 185, Issue 4, pp 561–571 | Cite as

Water availability and environmental temperature correlate with geographic variation in water balance in common lizards

  • Andréaz DupouéEmail author
  • Alexis Rutschmann
  • Jean François Le Galliard
  • Donald B. Miles
  • Jean Clobert
  • Dale F. DeNardo
  • George A. BruschIV
  • Sandrine Meylan
Physiological ecology - original research

Abstract

Water conservation strategies are well documented in species living in water-limited environments, but physiological adaptations to water availability in temperate climate environments are still relatively overlooked. Yet, temperate species are facing more frequent and intense droughts as a result of climate change. Here, we examined variation in field hydration state (plasma osmolality) and standardized evaporative water loss rate (SEWL) of adult male and pregnant female common lizards (Zootoca vivipara) from 13 natural populations with contrasting air temperature, air humidity, and access to water. We found different patterns of geographic variation between sexes. Overall, males were more dehydrated (i.e. higher osmolality) than pregnant females, which likely comes from differences in field behaviour and water intake since the rate of SEWL was similar between sexes. Plasma osmolality and SEWL rate were positively correlated with environmental temperature in males, while plasma osmolality in pregnant females did not correlate with environmental conditions, reproductive stage or reproductive effort. The SEWL rate was significantly lower in populations without access to free standing water, suggesting that lizards can adapt or adjust physiology to cope with habitat dryness. Environmental humidity did not explain variation in water balance. We suggest that geographic variation in water balance physiology and behaviour should be taken account to better understand species range limits and sensitivity to climate change.

Keywords

Ectotherm Osmolality Pregnancy Temperature Water loss 

Notes

Acknowledgements

We thank Pauline Blaimont, Pauline Dufour, Laurène Duhalde, Amélie Faure, Julia Rense, and Qiang Wu for their help with fieldwork. We also thank Clotilde Biard for lending us some of the loggers. We are grateful to the ‘Office Nationale des Forêts’, the ‘Parc National des Cévennes’, and the regions Auvergne, Rhône Alpes and Languedoc Roussillon for allowing us to sample lizards. This study was funded by the Centre National de la Recherche Scientifique (CNRS) the Agence Nationale de la Recherche (ANR-13-JSV7-0011-01 to SM) and the National Science Foundation (NSF-EF1241848 to DBM).

Author contribution statement

AD, AR, JFLG, DBM, JC, and SM conceived the ideas and designed methodology; AD, AR, JFLG, DBM, JC, and SM captured lizards; AD and AR collected water loss data; AD, GAB, and DD collected osmolality data; AD analysed the data; AD and AR led the writing of the manuscript. All authors contributed critically to the drafts and gave final approval for publication.

Compliance with ethical standards

Conflict of interest

The authors declare no competing or financial interests.

Supplementary material

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Supplementary material 1 (DOCX 18 kb)
442_2017_3973_MOESM2_ESM.docx (18 kb)
Supplementary material 2 (DOCX 17 kb)
442_2017_3973_MOESM3_ESM.docx (29 kb)
Supplementary material 3 (DOCX 29 kb)
442_2017_3973_MOESM4_ESM.docx (17 kb)
Supplementary material 4 (DOCX 17 kb)

References

  1. Angilletta MJ, Cooper BS, Schuler MS, Boyles JG (2010) The evolution of thermal physiology in endotherms. Front Biosci 26:861–881. doi: 10.1093/intimm/dxu021 Google Scholar
  2. Belasen A, Brock K, Li B et al (2016) Fine with heat, problems with water: microclimate alters water loss in a thermally adapted insular lizard. Oikos. doi: 10.1111/oik.03712 Google Scholar
  3. Bouwstra JA, Honeywell-Nguyen PL, Gooris GS, Ponec M (2003) Structure of the skin barrier and its modulation by vesicular formulations. Prog Lipid Res 42:1–36. doi: 10.1016/S0163-7827(02)00028-0 CrossRefPubMedGoogle Scholar
  4. Champagne AM, Munoz-Garcia A, Shtayyeh T et al (2012) Lipid composition of the stratum corneum and cutaneous water loss in birds along an aridity gradient. J Exp Biol 215:4299–4307. doi: 10.1242/jeb.077016 CrossRefPubMedGoogle Scholar
  5. Cheung KL, Lafayette RA (2013) Renal physiology of pregnancy. Adv Chronic Kidney Dis 20:209–214. doi: 10.1053/j.ackd.2013.01.012 CrossRefPubMedPubMedCentralGoogle Scholar
  6. Cooke SJ, Sack L, Franklin CE et al (2013) What is conservation physiology? Perspectives on an increasingly integrated and essential science. Conserv Physiol 1:1–23. doi: 10.1093/conphys/cot001 CrossRefGoogle Scholar
  7. Cox CL, Cox RM (2015) Evolutionary shifts in habitat aridity predict evaporative water loss across squamate reptiles. Evolution (NY) 69:2507–2516. doi: 10.1111/evo.12742 CrossRefGoogle Scholar
  8. Cryan PM, Wolf BO (2003) Sex differences in the thermoregulation and evaporative water loss of a heterothermic bat, Lasiurus cinereus, during its spring migration. J Exp Biol 206:3381–3390. doi: 10.1242/jeb.00574 CrossRefPubMedGoogle Scholar
  9. Dauphin-Villemant C, Xavier F (1986) Adrenal activity in the females Lacerta vivipara Jacquin: possible involvement in the success of gestation. In: Assemacher I, Boissin J (eds) Endocrine regulation as adaptive mechanism to environment. CNRS, Paris, pp 241–250Google Scholar
  10. Davis JR, DeNardo DF (2009) Water supplementation affects the behavioral and physiological ecology of gila monsters (Heloderma suspectum) in the sonoran desert. Physiol Biochem Zool 82:739–748. doi: 10.1086/605933 CrossRefPubMedGoogle Scholar
  11. DeNardo DF, Zubal TE, Hoffman TCM (2004) Cloacal evaporative cooling: a previously undescribed means of increasing evaporative water loss at higher temperatures in a desert ectotherm, the Gila monster Heloderma suspectum. J Exp Biol 207:945–953. doi: 10.1242/jeb.00861 CrossRefPubMedGoogle Scholar
  12. Deutsch CA, Tewksbury JJ, Huey RB et al (2008) Impacts of climate warming on terrestrial ectotherms across latitude. Proc Natl Acad Sci U S A 105:6668–6672CrossRefPubMedPubMedCentralGoogle Scholar
  13. Du W (2004) Water exchange of flexible-shelled eggs and its effect on hatchling traits in the Chinese skink, Eumeces chinensis. J Comp Physiol B Biochem Syst Environ Physiol 174:489–493. doi: 10.1007/s00360-004-0435-3 CrossRefGoogle Scholar
  14. Dunkin RC, Wilson D, Way N et al (2013) Climate influences thermal balance and water use in African and Asian elephants: physiology can predict drivers of elephant distribution. J Exp Biol 216:2939–2952. doi: 10.1242/jeb.080218 CrossRefPubMedGoogle Scholar
  15. Dupoué A, Lourdais O (2014) Relative reproductive effort drives metabolic changes and maternal emaciation during pregnancy in a viviparous snake. J Zool 293:49–56. doi: 10.1111/jzo.12116 CrossRefGoogle Scholar
  16. Dupoué A, Brischoux F, Angelier F et al (2015a) Intergenerational trade-off for water may induce a mother–offspring conflict in favour of embryos in a viviparous snake. Funct Ecol 29:414–422. doi: 10.1111/1365-2435.12349 CrossRefGoogle Scholar
  17. Dupoué A, Stahlschmidt ZR, Michaud B, Lourdais O (2015b) Physiological state influences evaporative water loss and microclimate preference in the snake Vipera aspis. Physiol Behav 144:82–89. doi: 10.1016/j.physbeh.2015.02.042 CrossRefPubMedGoogle Scholar
  18. Foley C, Pettorelli N, Foley L (2008) Severe drought and calf survival in elephants. Biol Lett 4:541–544. doi: 10.1098/rsbl.2008.0370 CrossRefPubMedPubMedCentralGoogle Scholar
  19. González-Suárez M, Mugabo M, Decencière B et al (2011) Disentangling the effects of predator body size and prey density on prey consumption in a lizard. Funct Ecol 25:158–165. doi: 10.1111/j.1365-2435.2010.01776.x CrossRefGoogle Scholar
  20. Guillon M, Guiller G, DeNardo DF, Lourdais O (2014) Microclimate preferences correlate with contrasted evaporative water loss in parapatric vipers at their contact zone. Can J Zool 92:81–86CrossRefGoogle Scholar
  21. Hetem RS, Strauss WM, Fick LG et al (2010) Variation in the daily rhythm of body temperature of free-living Arabian oryx (Oryx leucoryx): does water limitation drive heterothermy? J Comp Physiol B Biochem Syst Environ Physiol 180:1111–1119. doi: 10.1007/s00360-010-0480-z CrossRefGoogle Scholar
  22. Kattan GH, Lillywhite HB (1989) Humidity acclimation and skin permeability in the lizard Anolis carolinensis. Physiol Zool 62:593–606CrossRefGoogle Scholar
  23. Kearney M, Shine R, Porter WP (2009) The potential for behavioral thermoregulation to buffer “cold-blooded” animals against climate warming. Proc Natl Acad Sci U S A 106:3835–3840. doi: 10.1073/pnas.0808913106 CrossRefPubMedPubMedCentralGoogle Scholar
  24. Kennett R, Christian KA (1994) Metabolic depression in estivating long-neck turtles (Chelodina rugosa). Physiol Zool 67:1087–1102CrossRefGoogle Scholar
  25. Köhler A, Sadowska J, Olszewska J et al (2011) Staying warm or moist? Operative temperature and thermal preferences of common frogs (Rana temporaria) and effects on locomotion. Herpetol J 21:17–26Google Scholar
  26. Le Galliard J-F, Le Bris M, Clobert J (2003) Timing of locomotor impairment and shift in thermal preferences during gravidity in a viviparous lizard. Funct Ecol 17:877–885CrossRefGoogle Scholar
  27. Lillywhite HB (2006) Water relations of tetrapod integument. J Exp Biol 209:202–226. doi: 10.1242/jeb.02007 CrossRefPubMedGoogle Scholar
  28. Lorenzon P, Clobert J, Oppliger A, John-Alder H (1999) Effect of water constraint on growth rate, activity and body temperature of yearling common lizard (Lacerta vivipara). Oecologia 118:423–430CrossRefPubMedGoogle Scholar
  29. Lorenzon P, Clobert J, Massot M (2001) The contribution of phenotypic plasticity to adaptation in Lacerta vivipara. Evolution (NY) 55:392–404. doi:10.1554/0014-3820(2001)055[0392:TCOPPT]2.0.CO;2Google Scholar
  30. Lorioux S, Lisse H, Lourdais O (2013) Dedicated mothers: predation risk and physical burden do not alter thermoregulatory behaviour of pregnant vipers. Anim Behav 86:401–408. doi: 10.1016/j.anbehav.2013.05.031 CrossRefGoogle Scholar
  31. Lourdais O, Lorioux S, Dupoué A et al (2015) Embryonic water uptake during pregnancy is stage- and fecundity-dependent in the snake Vipera aspis. Comp Biochem Physiol Part A Mol Integr Physiol 189:102–106. doi: 10.1016/j.cbpa.2015.07.019 CrossRefGoogle Scholar
  32. Marquis O, Massot M, Le Galliard JF (2008) Intergenerational effects of climate generate cohort variation in lizard reproductive performance. Ecology 89:2575–2583. doi: 10.1890/07-1211.1 CrossRefPubMedGoogle Scholar
  33. Mautz WJ (1982) Patterns of evaporative water loss. In: Gans C, Pough FH (eds) Biology of the Reptilia. Academic Press, London, pp 443–481Google Scholar
  34. Mazerolle MJ (2016) AICcmodavg: Model selection and multimodel inference based on (Q)AIC(c)Google Scholar
  35. McKechnie AE, Wolf BO (2010) Climate change increases the likelihood of catastrophic avian mortality events during extreme heat waves. Biol Lett 6:253–256. doi: 10.1098/rsbl.2009.0702 CrossRefPubMedGoogle Scholar
  36. Meylan S, Dufty AM, Clobert J (2003) The effect of transdermal corticosterone application on plasma corticosterone levels in pregnant Lacerta vivipara. Comp Biochem Physiol Part A Mol Integr Physiol 134:497–503CrossRefGoogle Scholar
  37. Miles DB, Sinervo B, Frankino WA (2000) Reproductive burden, locomotor performance, and the cost of reproduction in free ranging lizards. Evolution (NY) 54:1386–1395. doi:10.1554/0014-3820(2000)054[1386:Rblpat]2.0.Co;2Google Scholar
  38. Moeller KT, Butler MW, DeNardo DF (2013) The effect of hydration state and energy balance on innate immunity of a desert reptile. Front Zool 10:23–33. doi: 10.1186/1742-9994-10-23 CrossRefPubMedPubMedCentralGoogle Scholar
  39. Moen DS, Winne CT, Reed RN (2005) Habitat-mediated shifts and plasticity in the evaporative water loss rates of two congeneric pit vipers (Squamata, Viperidae, Agkistrodon). Evol Ecol Res 7:759–766Google Scholar
  40. Muir TJ, Costanzo JP, Lee RE (2007) Osmotic and metabolic responses to dehydration and urea-loading in a dormant, terrestrially hibernating frog. J Comp Physiol B 177:917–926. doi: 10.1007/s00360-007-0190-3 CrossRefPubMedGoogle Scholar
  41. Peterman WE, Semlitsch RD (2014) Spatial variation in water loss predicts terrestrial salamander distribution and population dynamics. Oecologia 176:357–369CrossRefPubMedGoogle Scholar
  42. Peterson CC (2002) Temporal, population, and sexual variation in hematocrit of free-living desert tortoises: correlational tests of causal hypotheses. Can J Zool 80:461–470. doi: 10.1139/Z02-021 CrossRefGoogle Scholar
  43. Pilorge T, Xavier F, Barbault R (1983) Variations in litter size and reproductive effort within and between some populations of Lacerta vivipara. Ecography (Cop) 6:381–382CrossRefGoogle Scholar
  44. Pinheiro J, Bates D, DebRoy S et al (2016) nlme: Linear and nonlinear mixed effects modelsGoogle Scholar
  45. Rezende EL, Diniz-Filho JAF (2012) Phylogenetic analyses: comparing species to infer adaptations and physiological mechanisms. Compr Physiol 2:639–674. doi: 10.1002/cphy.c100079 PubMedGoogle Scholar
  46. Rozen-Rechels D, van Beest FM, Richard E et al (2015) Density-dependent, central-place foraging in a grazing herbivore: competition and tradeoffs in time allocation near water. Oikos 124:1142–1150. doi: 10.1111/oik.02207 CrossRefGoogle Scholar
  47. Rutschmann A, Miles DB, Le Galliard JF et al (2016) Climate and habitat interact to shape the thermal reaction norms of breeding phenology across lizard populations. J Anim Ecol 85:457–466. doi: 10.1111/1365-2656.12473 CrossRefPubMedGoogle Scholar
  48. Schultz TJ, Webb JK, Christian KA (2008) The physiological cost of pregnancy in a tropical viviparous snake. Copeia 2008:637–642. doi: 10.1643/CP-06-182 CrossRefGoogle Scholar
  49. Secor SM, Stein ED, Diamond J (1994) Rapid upregulation of snake intestine in response to feeding: a new model of intestinal adaptation. Am J Physiol 266:G695–G705PubMedGoogle Scholar
  50. Shine R (2006) Is increased maternal basking an adaptation or a pre-adaptation to viviparity in lizards? J Exp Zool Part A Comp Exp Biol 305A:524–535CrossRefGoogle Scholar
  51. Somero GN (2011) Comparative physiology: a “crystal ball” for predicting consequences of global change. Am J Physiol Regul Integr Comp Physiol 301:R1–R14. doi: 10.1152/ajpregu.00719.2010 CrossRefPubMedGoogle Scholar
  52. Speakman JR, Ergon T, Cavanagh R et al (2003) Resting and daily energy expenditures of free-living field voles are positively correlated but reflect extrinsic rather than intrinsic effects. Proc Natl Acad Sci USA 100:14057–14062CrossRefPubMedPubMedCentralGoogle Scholar
  53. Stachenfeld NS, Splenser AE, Calzone WL et al (2001) Sex differences in osmotic regulation of AVP and renal sodium handling. J Appl Physiol 91:1893–1901PubMedGoogle Scholar
  54. Taylor BE, Scott DE, Gibbons JW (2006) Catastrophic reproductive failure, terrestrial survival, and persistence of the marbled salamander. Conserv Biol 20:792–801. doi: 10.1111/j.1523-1739.2005.00321.x CrossRefPubMedGoogle Scholar
  55. Tieleman BI, Williams JB, Buschur ME (2002) Physiological adjustments to arid and mesic environments in larks (Alaudidae). Physiol Biochem Zool 75:305–313. doi: 10.1086/341998 CrossRefPubMedGoogle Scholar
  56. Tieleman BI, Williams JB, Bloomer P (2003) Adaptation of metabolism and evaporative water loss along an aridity gradient. Proc R Soc B Biol Sci 270:207–214. doi: 10.1098/rspb.2002.2205 CrossRefGoogle Scholar
  57. Tingley R, Greenlees MJ, Shine R (2012) Hydric balance and locomotor performance of an anuran (Rhinella marina) invading the Australian arid zone. Oikos 121:1959–1965. doi: 10.1111/j.1600-0706.2012.20422.x CrossRefGoogle Scholar
  58. Todgham AE, Stillman JH (2013) Physiological responses to shifts in multiple environmental stressors: relevance in a changing world. Integr Comp Biol 53:539–544. doi: 10.1093/icb/ict086 CrossRefPubMedGoogle Scholar
  59. Van Damme R, Bauwens D, Verheyen RF (1986) Selected body temperatures in the lizard Lacerta vivipara: variation within and between populations. J Therm Biol 11:219–222CrossRefGoogle Scholar
  60. Van Sant MJ, Oufiero CE, Muñoz-Garcia A et al (2012) A phylogenetic approach to total evaporative water loss in mammals. Physiol Biochem Zool 85:526–532. doi: 10.1086/667579 CrossRefPubMedGoogle Scholar
  61. Webber MM, Gibbs AG, Rodríguez-Robles JA (2015) Hot and not-so-hot females: reproductive state and thermal preferences of female Arizona Bark Scorpions (Centruroides sculpturatus). J Evol Biol 28:368–375. doi: 10.1111/jeb.12569 CrossRefPubMedGoogle Scholar
  62. Webster MD, Campbell GS, King JR (1985) Cutaneous resistance to water-vapor diffusion in pigeons and the role of the plumage. Physiol Zool 58:58–70CrossRefGoogle Scholar
  63. Weldon CW, Daniels SR, Clusella-Trullas S, Chown SL (2013) Metabolic and water loss rates of two cryptic species in the African velvet worm genus Opisthopatus (Onychophora). J Comp Physiol B Biochem Syst Environ Physiol 183:323–332. doi: 10.1007/s00360-012-0715-2 CrossRefGoogle Scholar
  64. Whitehead FJ, Couper RTL, Moore L et al (1996) Dehydration deaths in infants and young children. Am J Forensic Med Pathol 17:73–78CrossRefPubMedGoogle Scholar
  65. Wikelski M, Cooke SJ (2006) Conservation physiology. Trends Ecol Evol 21:38–46. doi: 10.1016/j.tree.2005.10.018 CrossRefPubMedGoogle Scholar
  66. Williams JB, Muñoz-Garcia A, Ostrowski S, Tieleman BI (2004) A phylogenetic analysis of basal metabolism, total evaporative water loss, and life-history among foxes from desert and mesic regions. J Comp Physiol B Biochem Syst Environ Physiol 174:29–39. doi: 10.1007/s00360-003-0386-0 CrossRefGoogle Scholar
  67. Williams JB, Muñoz-garcia A, Champagne A (2012) Climate change and cutaneous water loss of birds. J Exp Biol 215:1053–1060. doi: 10.1242/jeb.054395 CrossRefPubMedGoogle Scholar
  68. Woods HA, Smith JN (2010) Universal model for water costs of gas exchange by animals and plants. Proc Natl Acad Sci U S A 107:8469–8474. doi: 10.1073/pnas.0905185107 CrossRefPubMedPubMedCentralGoogle Scholar
  69. Wright CD, Jackson ML, DeNardo DF (2013) Meal consumption is ineffective at maintaining or correcting water balance in a desert lizard, Heloderma suspectum. J Exp Biol 216:1439–1447. doi: 10.1242/jeb.080895 CrossRefPubMedGoogle Scholar
  70. Zylstra ER, Steidl RJ, Jones CA, Averill-Murray RC (2013) Spatial and temporal variation in survival of a rare reptile: a 22-year study of Sonoran desert tortoises. Oecologia 173:107–116. doi: 10.1007/s00442-012-2464-z CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany 2017

Authors and Affiliations

  • Andréaz Dupoué
    • 1
    Email author
  • Alexis Rutschmann
    • 2
  • Jean François Le Galliard
    • 1
    • 3
  • Donald B. Miles
    • 4
  • Jean Clobert
    • 2
  • Dale F. DeNardo
    • 5
  • George A. BruschIV
    • 5
  • Sandrine Meylan
    • 1
    • 6
  1. 1.CNRS UPMC, UMR 7618, iEES Paris, Université Pierre et Marie CurieParisFrance
  2. 2.Station d’Ecologie Théorique et Expérimentale du CNRS à Moulis, UMR 5321Saint GironsFrance
  3. 3.Département de biologieEcole normale supérieure, PSL Research University, CNRS, UMS 3194, Centre de recherche en écologie expérimentale et prédictive (CEREEP-Ecotron IleDeFrance)Saint-Pierre-lès-NemoursFrance
  4. 4.Department of Biological SciencesOhio UniversityAthensUSA
  5. 5.School of Life SciencesArizona State UniversityTempeUSA
  6. 6.ESPE de Paris, Université Sorbonne Paris IVParisFrance

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