Skip to main content
Log in

Variation in stress and innate immunity in the tree lizard (Urosaurus ornatus) across an urban–rural gradient

  • Original Article
  • Published:
Journal of Comparative Physiology B Aims and scope Submit manuscript

Abstract

The urban environment presents new and different challenges to wildlife, but also potential opportunities depending on the species. As urban encroachment onto native habitats continues, understanding the impact of this expansion on native species is vital to conservation. A key physiological indicator of environmental disturbance is the vertebrate stress response, involving increases in circulating glucocorticoids (i.e. corticosterone), which exert influence on numerous physiological parameters including energy storage, reproduction, and immunity. We examined how urbanization in Phoenix, Arizona influences corticosterone levels, blood parasitism, and innate immunity in populations of tree lizards (Urosaurus ornatus) to determine whether urbanization may be detrimental or beneficial to this species. Both baseline and stress-induced corticosterone concentrations were significantly lower in urban lizards relative to the rural ones, however, the magnitude of the increase in corticosterone with stress did not differ across populations. Urban lizards also had a lower ratio of heterophils to lymphocytes, but elevated overall leukocyte count, as compared to lizards from the natural site. Urban and rural lizards did not differ in their prevalence of the blood parasite, Plasmodium mexicanum. Taken together, these results suggest that urban tree lizards may have suppressed overall corticosterone concentrations possibly from down-regulation as a result of frequent exposure to stressors, or increased access to urban resources. Also, urban lizards may have bolstered immunocompetence possibly from increased immune challenges, such as wounding, in the urban environment, or from greater energetic reserves being available as a result of access to urban resources.

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

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Aguirre AA, Balazs GH, Spraker TR, Gross TS (1995) Adrenal and hematological responses to stress in juvenile green turtles (Chelonia mydas) with and without fibropapillomas. Physiol Zool 68:831–854

    Google Scholar 

  • Anderies JM, Katti M, Shochat E (2007) Living in the city: Resource availability, predation, and bird population dynamics in urban areas. J Theor Biol 247:36–49

    Article  PubMed  Google Scholar 

  • Astheimer LB, Buttemer WA, Wingfield JC (1995) Seasonal and acute changes in adrenocortical responsiveness in an arctic-breeding bird. Horm Behav 29:442–457

    Article  PubMed  CAS  Google Scholar 

  • Baker PJ, Bentley AJ, Ansell RJ, Harris S (2005) Impact of predation by domestic cats Felis catus in an urban area. Mamm Rev 35:302–312

    Article  Google Scholar 

  • Bautista LM, Garcia JT, Calmaestra RG, Palacin C, Martin CA, Morales MB, Bonal R, Vinuela J (2004) Effect of weekend road traffic on the use of space by raptors. Conserv Bio 18:726–732

    Article  Google Scholar 

  • Beck BB, Engen CW, Gelfand PW (1973) Behavior and activity cycles of Gambels quail and raptorial birds at a Sonoran-Desert waterhole. Condor 75:466–470

    Article  Google Scholar 

  • Bennett GF (1970) Simple techniques for making avian blood smears. Can J Zool 48:585

    Article  Google Scholar 

  • Bonier F, Martin PR, Sheldon KS, Jensen JP, Foltz SL, Wingfield JC (2007a) Sex- specific consequences of life in the city. Behav Ecol 18:121–129

    Article  Google Scholar 

  • Bonier F, Martin PR, Wingfield JC (2007b) Urban birds have broader environmental tolerance. Biol Lett 3:670–673

    Article  PubMed  Google Scholar 

  • Boonstra R (2004) Coping with changing northern environments: The role of the stress axis in birds and mammals. Integr Comp Bio 44:95–108

    Article  Google Scholar 

  • Boonstra R, McColl CJ, Karels TJ (2001) Reproduction at all costs: The adaptive stress response of male arctic ground squirrels. Ecology 82:1930–1946

    Article  Google Scholar 

  • Braman SK, Latimer JG, Oetting RD, McQueen RD, Eckberg TB, Prinster M (2000) Management strategy, shade, and landscape composition effects on urban landscape plant quality and arthropod abundance. J Econ Entomol 93:1464–1472

    Article  PubMed  CAS  Google Scholar 

  • Burger J, Bowman R, Woolfenden GE, Gochfeld M (2004) Metal and metalloid concentrations in the eggs of threatened Florida scrub-jays in suburban habitat from south-central Florida. Sci Total Environ 328:185–193

    Article  PubMed  CAS  Google Scholar 

  • Bush AO, Lafferty KD, Lotz JM, Shostak AW (1997) Parasitology meets ecology on its own terms: Margolis et al. revisited. J Parasitol 83:575–583

    Article  PubMed  CAS  Google Scholar 

  • Campbell TW (1996) Clinical pathology. In: Mader DR (ed) Reptile medicine and surgery. WB Saunders Co., PA, pp 248–257

    Google Scholar 

  • Cartledge CA, Gartrell B, Jones SM (2005) Adrenal and white cell count responses to chronic stress in gestating and postpartum females of the viviparous skink Egernia whitii (Scincidae). Comp Biochem Physiol A 141:100–107

    Article  CAS  Google Scholar 

  • Cyr NE, Earle K, Tam C, Romero LM (2007) The effect of chronic psychological stress on corticosterone, plasma metabolites, and immune responsiveness in European starlings. Gen Comp Endocrinol 154:59–66

    Article  PubMed  CAS  Google Scholar 

  • Dhabhar FS, McEwen BS (1999) Enhancing versus suppressive effects of stress hormones on skin immune function. Proc Nat Acad Sci USA 96:1059–1064

    Article  PubMed  CAS  Google Scholar 

  • Dunlap KD, Schall JJ (1995) Hormonal alterations and reproductive inhibition in male fence lizards (Sceloporus occidentalis) infected with the malarial parasite plasmodium-mexicanum. Physiol Zool 68:608–621

    CAS  Google Scholar 

  • Eens M, Pinxten R, Verheyen RF, Blust R, Bervoets L (1999) Great and blue tits as indicators of heavy metal contamination in terrestrial ecosystems. Ecotoxicol Environ Saf 44:81–85

    Article  PubMed  CAS  Google Scholar 

  • Fearn S, Robinson B, Sambono J, Shine R (2001) Pythons in the pergola: The ecology of ‘nuisance’ carpet pythons (Morelia spilota) from suburban habitats in south - eastern Queensland. Wildl Res 28:573–579

    Article  Google Scholar 

  • Fernandez-Juricic E (2002) Can human disturbance promote nestedness? A case study with breeding birds in urban habitat fragments. Oecologia 131:269–278

    Article  Google Scholar 

  • Ficetola GF, Sacchi R, Scali S, Gentilli A, De Bernardi F, Galeotti P (2007) Vertebrates respond differently to human disturbance: Implications for the use of a focal species approach. Acta Oecol Int J Ecol 31:109–118

    Article  Google Scholar 

  • Fokidis HB, Greiner EC, Deviche P (2008) Interspecific variation in avian blood parasites and haematology associated with urbanization in a desert habitat. J Avian Bio 39:300–310

    Article  Google Scholar 

  • Fokidis HB, Orchinik M, Deviche P (in review) Patterns of total and free corticosterone secretion in birds associated with urbanization in a desert city. Gen Comp Endocrinol

  • French SS, Moore MC (2008) Immune function varies with reproductive stage and context in female and male tree lizards, Urosaurus ornatus. Gen Comp Endocrinol 155:148–156

    Article  PubMed  CAS  Google Scholar 

  • French SS, Matt KS, Moore MC (2006) The effects of stress on wound healing in male tree lizards (Urosaurus ornatus). Gen Comp Endocrinol 145:128–132

    Article  PubMed  CAS  Google Scholar 

  • French SS, DeNardo DF, Moore MC (2007a) Trade-offs between the reproductive and immune systems: Facultative responses to resources or obligate responses to reproduction? Am Nat 170:79–89

    Article  PubMed  Google Scholar 

  • French SS, Johnston GIH, Moore MC (2007b) Immune activity suppresses reproduction in food-limited female tree lizards Urosaurus ornatus. Funct Ecol 21:1115–1122

    Article  Google Scholar 

  • French SS, McLemore R, Vernon B, Johnston GIH, Moore MC (2007c) Corticosterone modulation of reproductive and immune systems trade-offs in female tree lizards: Long-term corticosterone manipulations via injectable gelling material. J Exp Biol 210:2859–2865

    Article  PubMed  CAS  Google Scholar 

  • Garamszegi LZ, Erritzoe J, Moller AP (2007) Feeding innovations and parasitism in birds. Biol J Linn Soc 90:441–455

    Article  Google Scholar 

  • Gering E, Atkinson CT (2004) A rapid method for counting nucleated erythrocytes on stained blood smears by digital image analysis. J Parasitol 90:879–881

    Article  PubMed  Google Scholar 

  • Germaine SS, Wakeling BF (2001) Lizard species distributions and habitat occupation along an urban gradient in Tucson, Arizona, USA. Biol Conserv 97:229–237

    Article  Google Scholar 

  • Gillies C, Clout M (2003) The prey of domestic cats (Felis catus) in two suburbs of Auckland City, New Zealand. J Zool 259:309–315

    Article  Google Scholar 

  • Giuliano WM, Lutz RS, Patino R (1995) Physiological-responses of northern bobwhite (Colinus virginianus) to chronic water-deprivation. Physiol Zool 68:262–276

    Google Scholar 

  • Godfrey RD, Fedynich AM, Pence DB (1987) Quantification of hematozoa in blood smears. J Wildl Dis 23:558–565

    PubMed  Google Scholar 

  • Gross WB, Siegel PB (1986) Effects of initial and 2nd periods of fasting on heterophil lymphocyte ratios and body-weight. Avian Dis 30:345–346

    Article  PubMed  CAS  Google Scholar 

  • Hanley KA, Stamps JA (2002) Does corticosterone mediate bidirectional interactions between social behaviour and blood parasites in the juvenile black iguana, Ctenosaura similis? Anim Behav 63:311–322

    Article  Google Scholar 

  • Harmon BG (1998) Avian heterophils in inflammation and disease resistance. Poult Sci 77:972–977

    PubMed  CAS  Google Scholar 

  • Hostetler M (1999) Scale, birds, and human decisions: A potential for integrative research in urban ecosystems. Landsc Urban Plan 45:15–19

    Article  Google Scholar 

  • Hostetler M, Knowles-Yanez K (2003) Land use, scale, and bird distributions in the phoenix metropolitan area. Landsc Urban Plan 62:55–68

    Article  Google Scholar 

  • Jessop TS, Hamann M, Limpus CJ (2004) Body condition and physiological changes in male green turtles during breeding. Mar Ecol Prog Ser 276:281–288

    Article  Google Scholar 

  • Jokimaki J, Kaisanlahti-Jokimaki ML, Sorace A, Fernandez-Juricic E, Rodriguez Prieto I, Jimenez MD (2005) Evaluation of the “safe nesting zone” hypothesis across an urban gradient: a multi-scale study. Ecography 28:59–70

    Article  Google Scholar 

  • Koenig J, Shine R, Shea G (2002) The dangers of life in the city: Patterns of activity, injury and mortality in suburban lizards (Tiliqua scincoides). J Herpetol 36:62–68

    Google Scholar 

  • Landys MM, Ramenofsky M, Wingfield JC (2006) Actions of glucocorticoids at a seasonal baseline as compared to stress-related levels in the regulation of periodic life processes. Gen Comp Endocrinol 148:132–149

    Article  PubMed  CAS  Google Scholar 

  • Marquardt WC, Demaree RS, Grieve RB (2000) Parasitology and vector biology. Academic Press, SD

    Google Scholar 

  • McLean MA, Angilletta MJ, Williams KS (2005) If you can’t stand the heat, stay out of the city: Thermal reaction norms of chitinolytic fungi in an urban heat island. J Therm Biol 30:384–391

    Article  Google Scholar 

  • Moore MC (1986) Elevated testosterone levels during nonbreeding-season territoriality in a fall-breeding lizard, Sceloporus jarrovi. J Comp Physiol A 158:159–163

    Article  PubMed  CAS  Google Scholar 

  • Moore IT, Jessop TS (2003) Stress, reproduction, and adrenocortical modulation in amphibians and reptiles. Horm Behav 43:39–47

    Article  PubMed  CAS  Google Scholar 

  • Moore IT, Mason RT (2001) Behavioral and hormonal responses to corticosterone in the male red-sided garter snake, Thamnophis sirtalis parietalis. Physiol Behav 72:669–674

    Article  PubMed  CAS  Google Scholar 

  • Moore MC, Thompson CW, Marler CA (1991) Reciprocal changes in corticosterone and testosterone levels following acute and chronic handling stress in the tree lizard, Urosaurus ornatus. Gen Comp Endocrinol 81:217–226

    Article  PubMed  CAS  Google Scholar 

  • Moore MC, Hews DK, Knapp R (1998) Hormonal control and evolution of alternative male phenotypes: Generalizations of models for sexual differentiation. Am Zool 38:133–151

    CAS  Google Scholar 

  • Morici LA, Elsey RM, Lance VA (1997) Effects of long-term corticosterone implants on growth and immune function in juvenile alligators, Alligator mississippiensis. J Exp Zool 279:156–162

    Article  PubMed  CAS  Google Scholar 

  • Munoz FJ, Galvan A, Lerma M, De la Fuente M (2000) Seasonal changes in peripheral blood leukocyte functions of the turtle Mauremys caspica and their relationship with corticosterone, 17-beta-estradiol and testosterone serum levels. Vet Immunol Immunopathol 77:27–42

    Article  PubMed  CAS  Google Scholar 

  • Parris KM, Hazell DL (2005) Biotic effects of climate change in urban environments: The case of the grey-headed flying-fox (Pteropus poliocephalus) in Melbourne, Australia. Biol Conserv 124:267–276

    Article  Google Scholar 

  • Partecke J, Schwabl I, Gwinner E (2006) Stress and the city: Urbanization and its effects on the stress physiology in European Blackbirds. Ecology 87:1945–1952

    Article  PubMed  Google Scholar 

  • Reed RN, Shine R (2002) Lying in wait for extinction: Ecological correlates of conservation status among Australian elapid snakes. Conserv Bio 16:451–46

    Article  Google Scholar 

  • Rich EL, Romero LM (2005) Exposure to chronic stress downregulates corticosterone responses to acute stressors. Am J Physiol Regul Integr Comp Physiol 288:R1628–1636

    PubMed  CAS  Google Scholar 

  • Rodriguez AB, Marchena JM, Harvey S, Barriga C, Lea RW (2001) Immobilization stress and daily variations of melatonin and corticosterone in the serum of ring dove (Streptopelia risoria). Biog Amines 16:185–197

    CAS  Google Scholar 

  • Romero LM, Reed JM (2008) Repeatability of baseline corticosterone concentrations. Gen Comp Endocrinol 156:27–33

    Article  PubMed  CAS  Google Scholar 

  • Romero LM, Remage-Healey L (2000) Daily and seasonal variation in response to stress in captive starlings (Sturnus vulgaris): Corticosterone. Gen Comp Endocrinol 119:52–59

    Article  PubMed  CAS  Google Scholar 

  • Romero LM, Meister CJ, Cyr NE, Kenagy GJ, Wingfield JC (2008) Seasonal glucocorticoid responses to capture in wild free-living mammals. Am J Physiol Regul Integr Comp Physiol 294:R614–R622

    PubMed  CAS  Google Scholar 

  • Saad AH, Elridi R (1988) Endogenous corticosteroids mediate seasonal cyclic changes in immunity of lizards. Immunobiology 177:390–403

    PubMed  CAS  Google Scholar 

  • Sapolsky RM, Romero LM, Munck AU (2000) How do glucocorticoids influence stress responses? Integrating permissive, suppressive, stimulatory, and preparative actions. Endocr Rev 21:55–89

    Article  PubMed  CAS  Google Scholar 

  • Schall JJ, Smith TC (2006) Detection of a malaria parasite (Plasmodium mexicanum) in ectoparasites (mites and ticks), and possible significance for transmission. J Parasitol 92:413–415

    Article  PubMed  CAS  Google Scholar 

  • Schoech SJ, Bowman R, Reynolds SJ (2004) Corticosterone, nutrition, and timing of reproduction in Florida Scrub-Jays. Horm Behav 46:121–121

    Article  CAS  Google Scholar 

  • Shochat E, Warren PS, Faeth SH, McIntyre NE, Hope D (2006) From patterns to emerging processes in mechanistic urban ecology. Trends Ecol Evol 21:186–191

    Article  PubMed  Google Scholar 

  • Sorace A (2002) High density of bird and pest species in urban habitats and the role of predator abundance. Ornis Fenn 79:60–71

    Google Scholar 

  • Thompson CW, Moore MC (1992) Behavioral and hormonal correlates of alternative reproductive strategies in a polygynous lizard—tests of the relative plasticity and challenge hypotheses. Horm Behav 26:568–585

    Article  PubMed  CAS  Google Scholar 

  • Vleck M (1984) Reproductive season and water-stress in a Sonoran Desert bird—the Curve-Billed Thrasher. Am Zool 24:A5–A5

    Google Scholar 

  • Vleck CM, Vertalino N, Vleck D, Bucher TL (2000) Stress, corticosterone, and heterophil to lymphocyte ratios in free-living Adelie Penguins. Condor 102:392–400

    Article  Google Scholar 

  • Wada M, Shimizu T (2004) Seasonal changes in adrenocortical responses to acute stress in polygynous male bush warblers (Cettia diphone). Gen Comp Endocrinol 135:193–200

    Article  PubMed  CAS  Google Scholar 

  • Walberg J (2001) White blood cell counting techniques in birds. Semin Avian Exotic Pet Med 10:72–76

    Article  Google Scholar 

  • Wang G, Richardson MI, Moore IT, Soma KK, Li DM, Lei FM, Wingfield JC (2006) Seasonal regulation of adrenocortical response to stress in two species of snowfinches on the Tibet plateau. Integr Comp Bio 46:E151–E151

    Article  Google Scholar 

  • Wilson BS, Wingfield JC (1992) Correlation between female reproductive condition and plasma-corticosterone in the lizard Uta stansburiana. Copeia 691–697

  • Wingfield JC, Maney DL, Breuner CW, Jacobs JD, Lynn S, Ramenofsky M, Richardson RD (1998) Ecological bases of hormone-behavior interactions: The “emergency life history stage”. Am Zool 38:191–206

    CAS  Google Scholar 

  • Woodley SK, Moore MC (2002) Plasma corticosterone response to an acute stressor varies according to reproductive condition in female tree lizards (Urosaurus ornatus). Gen Comp Endocrinol 128:143–148

    Article  PubMed  CAS  Google Scholar 

  • Woods M, McDonald RA, Harris S (2003) Predation of wildlife by domestic cats Felis catus in Great Britain. Mamm Rev 33:174–188

    Article  Google Scholar 

Download references

Acknowledgments

We would like to thank Nataliya Emmert for help with field work, Pierre Deviche for use of his light microscope, and Jon Davis for use of his backyard and alleyway. We would also like to thank PRG at ASU for critical feedback on this article.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Susannah S. French.

Additional information

Communicated by H.V. Carey.

Rights and permissions

Reprints and permissions

About this article

Cite this article

French, S.S., Fokidis, H.B. & Moore, M.C. Variation in stress and innate immunity in the tree lizard (Urosaurus ornatus) across an urban–rural gradient. J Comp Physiol B 178, 997–1005 (2008). https://doi.org/10.1007/s00360-008-0290-8

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00360-008-0290-8

Keywords

Navigation