Skip to main content
Log in

Integration of autonomic and local mechanisms in regulating cardiovascular responses to heating and cooling in a reptile (Crocodylus porosus)

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

Abstract

Reptiles change heart rate and blood flow patterns in response to heating and cooling, thereby decreasing the behavioural cost of thermoregulation. We tested the hypothesis that locally produced vasoactive substances, nitric oxide and prostaglandins, mediate the cardiovascular response of reptiles to heat. Heart rate and blood pressure were measured in eight crocodiles (Crocodylus porosus) during heating and cooling and while sequentially inhibiting nitric-oxide synthase and cyclooxygenase enzymes. Heart rate and blood pressure were significantly higher during heating than during cooling in all treatments. Power spectral density of heart rate and blood pressure increased significantly during heating and cooling compared to the preceding period of thermal equilibrium. Spectral density of heart rate in the high frequency band (0.19–0.70 Hz) was significantly greater during cooling in the saline treatment compared to when nitric-oxide synthase and cyclooxygenase enzymes were inhibited. Cross spectral analysis showed that changes in blood pressure preceded heart rate changes at low frequencies (<0.1 Hz) only. We conclude that the autonomic nervous system controls heart rate independently from blood pressure at higher frequencies while blood pressure changes determine heart rate at lower frequencies. Nitric oxide and prostaglandins do not control the characteristic heart rate hysteresis response to heat in C. porosus, although nitric oxide was important in buffering blood pressure against changes in heart rate during cooling, and inhibition caused a compensatory decrease in parasympathetic stimulation of the heart.

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
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

Abbreviations

BP :

blood pressure

COX :

cyclooxygenase

fH :

heart rate

NO :

nitric oxide

L-NAME :

N ω -nitro-l-arginine methyl ester

SNP :

sodium nitroprusside

References

  • Akselrod S, Gordon D, Ubel FA, Barger AC, Cohen RJ (1981) Power spectrum analysis of heart rate fluctuation: a quantitative probe of beat-to-beat cardiovascular control. Science 213:220–222

    CAS  PubMed  Google Scholar 

  • Altimiras J (1999) Understanding autonomic sympathovagal balance from short-term heart rate variations. Are we analyzing noise? Comp Biochem Physiol 124A: 447–460

    CAS  Google Scholar 

  • Altimiras J, Franklin CE, Axelsson M (1998) Relationship between blood pressure and heart rate in the saltwater crocodile Crocodylus porosus. J Exp Biol 201:2235–2242

    PubMed  Google Scholar 

  • Bartholomew GA (1982) Physiological control of body temperature. In: Gans C, Pough FH (eds) Biology of the Reptilia, vol 12. Academic Press, New York, pp 167–212

  • Bartholomew GA, Tucker VA (1963) Control of changes in body temperature, metabolism, and circulation by the agamid lizard, Amphibolurus barbatus. Physiol Zool 36:199–218

    Google Scholar 

  • Berger RD, Saul JP, Cohen RJ (1989) Transfer function analysis of autonomic regulation I. canine atrial rate response. Am J Physiol 256: H142-H152

    CAS  PubMed  Google Scholar 

  • Cerutti C, Barres C, Paultre C (1994) Baroreflex modulation of blood pressure and heart rate variabilities in rats: assessment by spectral analysis. Am J Physiol 266: H1993-H2000

    CAS  PubMed  Google Scholar 

  • Chatfield C (1987) The analysis of time series: an introduction, 3rd edn. Chapman and Hall, London

    Google Scholar 

  • Cohen MA, Taylor JA (2002) Short-term cardiovascular oscillations in man: measuring and modelling the physiologies. J Physiol (Lond) 542:669–683

    Google Scholar 

  • Cooper KE (2002) Molecular biology of thermoregulation. Some historical perspectives on thermoregulation. J Appl Physiol 92:1717–1724

    CAS  PubMed  Google Scholar 

  • Crossley DA, Hicks JW, Altimiras J (2003) Ontogeny of baroreflex control in the American alligator Alligator mississippiensis. J Exp Biol 206:2895–2902

    Article  PubMed  Google Scholar 

  • De Vera L, Gonzales J (1997) Power spectral analysis of short-term RR interval and arterial blood pressure oscillations in lizard (Gallotia galloti): effects of parasympathetic blockade. Comp Biochem Physiol 118A: 671–678

    Google Scholar 

  • De Vera L., Gonzales, J (1999) Power spectral analysis of short-term RR interval and blood pressure oscillations in the lizard, Gallotia galloti: effects of sympathetic blockade. J Exp Zool 283:113–120

    Article  PubMed  Google Scholar 

  • di Rienzo M, Parati G, Castiglione P, Omboni S, Ferrari AU, Ramirez AJ, Pedotti A, Mancia G (1991) Role of sinoaortic afferents in modulating BP and pulse-interval spectral characteristics in unanesthetized cats. Am J Physiol 261: H1811-H1818

    PubMed  Google Scholar 

  • Dzialowski EM, O’Connor MP (2001) Physiological control of warming and cooling during simulated shuttling and basking in lizards. Physiol Biochem Zool 74:679–693

    Article  CAS  PubMed  Google Scholar 

  • Ehmke H, Just A (2003) The orexins: linking circulatory control with behavior. Am J Physiol 285: R519-R521

    Google Scholar 

  • Franklin CE, Seebacher F (2003) The effect of heat transfer mode on heart rate responses and hysteresis during heating and cooling in the estuarine crocodile, Crocodylus porosus. J Exp Biol 206:1143–1151

    Article  PubMed  Google Scholar 

  • Grigg GC, Alchin J (1976) The role of the cardiovascular system in thermoregulation of Crocodylus johnstoni. Physiol Zool 49:24–36

    Google Scholar 

  • Grigg GC, Drane CR, Courtice GP (1979) Time constants of heating and cooling in the eastern water dragon, Physignathus lesueruii, and some generalizations about heating and cooling in reptiles. J Therm Biol 4:95–103

    Article  Google Scholar 

  • Henderson LA, Keay KA, Bandler R (2000) Caudal midline medulla mediates behaviourally-coupled but not baroreceptor-mediated vasodepression. Neuroscience 98:779–792

    Google Scholar 

  • Kurata Y, Hisatome I, Imanishi S, Shibamoto T (2002) Dynamical description of sinoatrial node pacemaking: improved mathematical model for primary pacemaker cell. Am J Physiol 283, H2074-H2101

    Google Scholar 

  • Lafranchi PA, Somers VK (2002) Arterial baroreflex function and cardiovascular variability: interactions and implications. Am J Physiol 283: R815–R826

    Google Scholar 

  • Li P-L, Chao Y-M, Chan SHH, Chan JYH (2001) Potentiation of baroreceptor reflex response by heat shock protein 70 in nucleus tractus solitarii confers cardiovascular protection during heat stroke. Circulation 103:2114–2119

    CAS  PubMed  Google Scholar 

  • Morgareidge KR, White FN (1972) Cutaneous vascular changes during heating and cooling in the Galapagos marine iguana. Nature 223:587–591

    Google Scholar 

  • Morris JL, Nilsson S (1994) The circulatory system. In: Nilsson S, Holmgren S (eds) Comparative physiology and evolution of the autonomic nervous system. Harwood Academic Publishers, Switzerland, pp 193–256

  • O’Connor MP (1999) Physiological and ecological implications of a simple model of heating and cooling in reptiles. J Therm Biol 24:113–136

    Article  Google Scholar 

  • Overgaard J, Stecyk JAW, Farrell AP, Wang T (2002) Adrenergic control of the cardiovascular system in the turtle Trachemys scripta. J Exp Biol 205:3335–3345

    CAS  PubMed  Google Scholar 

  • Rademacher DJ, Patel S, Hopp FA, Dean C, Hillard CJ, Seagard JL (2003) Microinjection of a cannabinoid receptor antagonist into the NTS increases baroreflex duration in dogs. Am J Physiol 284:H1570–H1576

    CAS  Google Scholar 

  • Rainsford KD (2001) The ever-emerging anti-inflammatories. Have there been any real advances? J Physiol (Paris) 95:11–19

    Google Scholar 

  • Rimoldi O, Pierini S, Ferrari A., Cerutti S, Pagani M, Malliani A (1990) Analysis of short-term oscillations of R-R and arterial pressure in conscious dogs. Am J Physiol 258:H967-H976

    CAS  PubMed  Google Scholar 

  • Robbe HWJ, Mulder LJM, Rűddel H, Langewitz WA, Veldman JBP, Mulder G (1987) Assessment of baroreceptor reflex sensitivity by means of spectral analysis. Hypertension 10:538–543

    CAS  PubMed  Google Scholar 

  • Robertson S, Smith EN (1979) Thermal indications of cutaneous blood flow in the American alligator. Comp Biochem Physiol 62A: 569–572

    Article  Google Scholar 

  • Salvemini D (1997) Regulation of cyclooxygenase enzymes by NO. Cell Mol Life Sci 53:576–582

    Article  CAS  PubMed  Google Scholar 

  • Scholz H (2003) Prostaglandins. Am J Physiol 285:R512-R514

    Google Scholar 

  • Seebacher F (2000) Heat transfer in a microvascular network: the effect of heart rate on heating and cooling in reptiles (Pogona barbata and Varanus varius). J Theor Biol 203:97–109

    Article  CAS  PubMed  Google Scholar 

  • Seebacher F, Franklin CE (2001) Control of heart rate during thermoregulation in the heliothermic lizard, Pogona barbata: importance of cholinergic and adrenergic mechanisms. J Exp Biol 204:4361–4366

    CAS  PubMed  Google Scholar 

  • Seebacher F, Franklin CE (2003) Prostaglandins are important in thermoregulation of a lizard (Pogona vitticeps). Proc R Soc Lond B (Suppl) 270:S50–S53

    Google Scholar 

  • Shaul PW (2002) Regulation of endothelial NO synthase: location, location, location. Annu Rev Physiol 64:749–774

    Article  CAS  PubMed  Google Scholar 

  • Sils IV, Szlyk-Modrow PC, Tartarini KA, Matthew CB, Francesconi RP (2002) Effect of NO synthase inhibition on regional blood flow during hyperthermia. J Therm Biol 26:1–7

    Article  Google Scholar 

  • Smith EN, Robertson S, Davies DG (1978) Cutaneous blood flow during heating and cooling in the American alligator. Am J Physiol 235:R160–R167

    CAS  PubMed  Google Scholar 

  • Solomonson LP, Flam BR, Pendleton LC, Goodwin BL, Eichler DC (2003) The caveolar NO synthase/arginine regeneration system for NO production in endothelial cells. J Exp Biol 206:2083–2087

    Article  CAS  PubMed  Google Scholar 

  • Stewart J (1996). Calculus. Brooks/Cole Publishing, Pacific Grove, California, pp 569–572

  • Tosini G, Bertolucci C, Foà A. (2001) The circadian system of reptiles: a multioscillatory and multiphotoreceptive system. Physiol Behav 72:461–471

    Article  CAS  PubMed  Google Scholar 

  • Viana F, de la Pena E, Belmonte C (2002) Specificity of cold thermotransduction is determined by differential ionic channel expression. Nat Neurosci 5:254–260

    Article  CAS  PubMed  Google Scholar 

  • Viswanath V, Story GM, Peier AM, Petrus MJ, Lee VM, Hwang SW, Patapoutian A, Jegla T (2003) Opposite thermosensor in fruitfly and mouse. Nature 423:822–823

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Frank Seebacher.

Additional information

Communicated by I.D. Hume

Rights and permissions

Reprints and permissions

About this article

Cite this article

Seebacher, F., Franklin, C.E. Integration of autonomic and local mechanisms in regulating cardiovascular responses to heating and cooling in a reptile (Crocodylus porosus). J Comp Physiol B 174, 577–585 (2004). https://doi.org/10.1007/s00360-004-0446-0

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00360-004-0446-0

Keywords

Navigation