Skip to main content
Log in

Hemodynamics of tonic immobility in the American alligator (Alligator mississippiensis) identified through Doppler ultrasonography

  • Original paper
  • Published:
Journal of Comparative Physiology A Aims and scope Submit manuscript

Abstract

American alligators (Alligator mississippiensis) held inverted exhibit tonic immobility, combining unresponsiveness with flaccid paralysis. We hypothesize that inverting the alligator causes a gravitationally promoted increase in right aortic blood flowing through the foramen of Panizza, with a concurrent decrease in blood flow through the primary carotid, and thereby of cerebral perfusion. Inverting the alligator results in displacement of the liver, post-pulmonary septum, and the heart. EKG analysis revealed a significant decrease in heart rate following inversion; this decrease was maintained for approximately 45 s after inversion which is in general agreement with the total duration of tonic immobility in alligators (49 s). Doppler ultrasonography revealed that following inversion of the alligator, there was a reversal in direction of blood flow through the foramen of Panizza, and this blood flow had a significant increase in velocity (compared to the foraminal flow in the prone alligator). There was an associated significant decrease in the velocity of blood flow through the primary carotid artery once the alligator was held in the supine position. Tonic immobility in the alligator appears to be a form of vasovagal syncope which arises, in part, from the unique features of the crocodilian 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
Fig. 7
Fig. 8
Fig. 9
Fig. 10
Fig. 11

Similar content being viewed by others

References

  • Alboni P, Alboni M (2017) Typical vasovagal syncope as a “defense mechanism” for the heart by contrasting sympathetic overactivity. Clin Auton Res 27:253–261

    Article  Google Scholar 

  • Alboni P, Alboni M, Bertorelle G (2008) The origin of vasovagal syncope: To protect the heart or to escape predation? Clin Auton Res 18:170–178

    Article  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Axelsson M, Franklin C (2001) The calibre of the foramen of Panizza in Crocodylus porosus is variable and under adrenergic control. J Comp Physiol B 171:341–346

    Article  CAS  Google Scholar 

  • Axelsson M, Holm S, Nilsson S (1989) Flow dynamics of the crocodilian heart. Am J Physiol 256:R875–R879

    CAS  PubMed  Google Scholar 

  • Axelsson M, Franklin C, Lofman C, Nilsson S, Grigg G (1996) Dynamic anatomical study of cardiac shunting in crocodiles using high-resolution angioscopy. J Exp Biol 199:359–365

    CAS  PubMed  Google Scholar 

  • Axelsson M, Franklin C, Fritsche G, Grigg G, Nilsson S (1997) The sub-pulmonary conus and the arterial anastomosis as important sites of cardiovascular regulation in the crocodile Crocodylus porosus. J Exp Biol 200:807–814

    CAS  PubMed  Google Scholar 

  • Berger P (1987) The reptilian baroreceptor and its role in cardiovascular control. Am Zool 27:111–120

    Article  Google Scholar 

  • Caro T (2014) Antipredator deception in terrestrial vertebrates. Curr Zool 60:16–25

    Article  Google Scholar 

  • Claessens L (2009) A cineradiographic study of lung ventilation in Alligator mississippiensis. J Exp Zool A 311:563–585

    Article  Google Scholar 

  • Clerici C, Veneroni L (2012) The impossible escape: Studies on the tonic immobility in animals from a comparative psychology perspective. Novinka Science, New York

    Google Scholar 

  • Colman N, Nahm K, Ganzeboom K, Shen W, Reitsma J, Linzer M, Wieling W, Kaufmann H (2004) Epidemiology of reflex syncope. Clin Auton Res 14(1):9–17

    Article  Google Scholar 

  • Cook A, Tran V-H, Spicer D, Rob JM, Sridharan S, Taylor A, Anderson R, Jensen B (2017) Sequential segmental analysis of the crocodilian heart. J Anat 231:484–499

    Article  Google Scholar 

  • Crawford FT (1977) Induction and duration of tonic immobility. Psychol Rec 1:89–107

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Da Silva L, Menescal-de-Oliveira L (2007) Role of opioidergic and GABAergic neurotransmission of the nucleus raphe magnus in the modulation of tonic immobility in guinea pigs. Brain Res Bull 72:25–31

    Article  Google Scholar 

  • Dan D, Hoag J, Ellenbogen K, Wood M, Eckberg D, Gilligan D (2002) Cerebral blood flow velocity declines before arterial pressure in patients with orthostatic vasovagal presyncope. J Am Coll Cardiol 39:1039–1045

    Article  Google Scholar 

  • De Oliveira L, Hoffman A, Menescal-de-Oliveira L (1997) Participation of the medial and anterior hypothalamus in the modulation of tonic immobility in guinea pigs. Physiol Behav 62:1171–1178

    Article  Google Scholar 

  • Farmer CG, Uriona T, Olsen D, Steenblik M, Sanders K (2008) The right-to-left shunt in crocodilians serves digestion. Physiol Biochem Zool 81:125–137

    Article  CAS  Google Scholar 

  • Findsen A, Crossley D, Wang T (2018) Feeding alters blood flow patterns in the American alligator (Alligator mississippiensis). Comp Biochem Phys A 215:1–5

    Article  CAS  Google Scholar 

  • Franklin C, Axelsson M (1994) The intrinsic properties of an in situ perfused crocodile heart. J Exp Biol 186:269–288

    CAS  PubMed  Google Scholar 

  • Franklin C, Axelsson M (2000) Physiology: an actively controlled heart valve. Nature 406:847–848

    Article  CAS  Google Scholar 

  • Gallup G (1973) Simulated predation and tonic immobility in Anolis carolinensis. Copeia 1973:623–624

    Article  Google Scholar 

  • Gallup G (1974) Animal hypnosis: factual status of a fictional concept. Psychol Bull 81:836–853

    Article  Google Scholar 

  • Gallup G (1977) Tonic immobility: the role of fear and predation. Psychol Rec 27:41–61

    Article  Google Scholar 

  • Gans C, Clark B (1976) Studies on ventilation of Caiman crocodilus (Crocodilia: Reptilia). Resp Physiol 26:285–301

    Article  CAS  Google Scholar 

  • Gaskell W, Gadow H (1884) On the anatomy of the cardiac nerves in certain cold-blooded vertebrates. J Physiol 5:362–372

    Article  Google Scholar 

  • Gaunt A, Gans C (1969) Diving bradycardia and withdrawal bradycardia in Caiman crocodilus. Nature 223:207–208

    Article  CAS  Google Scholar 

  • Gehlbach F (1970) Death-feigning and erratic behaviour in leptotyphlopid, colubrid, and elapid snakes. Herpetologica 26:24–34

    Google Scholar 

  • Greene HW (1988) Antipredator mechanisms in reptiles. In: Gans C, Huey RB (eds) Biology of the Reptilia, vol 16. Alan R. Liss, New York, pp 1–152

    Google Scholar 

  • Hagensen M, Abe A, Wang T (2010) Baroreflex control of heart rate in the broad-nosed caiman (Caiman latirostris) is temperature dependent. Comp Biochem Phys A 156:458–462

    Article  Google Scholar 

  • Hatton D, Lanthorn T, Webster D, Meyer M (1978) Baroreceptor involvement in the immobility reflex. Behav Biol 22:122–127

    Article  CAS  Google Scholar 

  • Hatton D, Webster D, Lanthorn T, Meyer M (1979) Evidence for baroreceptor involvement in the immobility reflex in the rabbit: blood pressure changes during induction and termination. Behav Neural Biol 26:89–96

    Article  CAS  Google Scholar 

  • Hermosillo A, Jordan J, Vallejo M, Kostine A, Marquez M, Cardenas M (2006) Cerebrovasular blood flow during the near syncopal phase of head-up tilt test: a comparative study in different types of neurally mediated syncope. Europace 8:199–203

    Article  Google Scholar 

  • Hoagland H (1928a) The mechanism of tonic immobility in vertebrates. J Gen Physiol 1:426–447

    Google Scholar 

  • Hoagland H (1928b) On the mechanism of tonic immobility. J Gen Physiol 11:715–741

    Article  CAS  Google Scholar 

  • Huggins S, Hoff H, Pena R (1969) Heart and respiratory rates in crocodilian reptiles under conditions of minimal stimulation. Physiol Zool 42:320–333

    Article  Google Scholar 

  • Jones D, Shelton G (1993) The physiology of the alligator heart: left aortic flow patterns and right-to-left shunts. J Exp Biol 176:247–269

    Google Scholar 

  • Klemm W (1971) Neurophysiologic studies of the immobility reflex (“animal hypnosis”). In: Ehrenprels S, Solnitzky O (eds) Neurosciences Research, vol 4. Academic Press, New York, pp 165–212

    Chapter  Google Scholar 

  • Klemm W (1976) Identity of sensory and motor systems that are critical to the immobility reflex (‘animal hypnosis’). J Neurosci Res 2:57–69

    Article  CAS  Google Scholar 

  • Kunin RA (1967) Electroencephalograph studies in animal hypnosis. Am J Clin Hypn 9:256–261

    Article  CAS  Google Scholar 

  • Leys C, Ley C, Klein O, Bernard P, Licata L (2013) Detecting outliers: do not use standard deviation around the mean, use absolute deviation around the mean. J Exp Soc Pyschol 49:764–766

    Article  Google Scholar 

  • Lillywhite H (1993) Orthostatic intolerance of viperid snakes. Physiol Zool 66:1000–1014

    Article  Google Scholar 

  • Lillywhite HB, Albert J, Sheehy C, Seymour RS (2012) Gravity and the evolution of cardiopulmonary morphology in snakes. Comp Biochem Physiol A 161:230–242

    Article  CAS  Google Scholar 

  • McBride D, Reis C, Frank E, Klebe D, Zhang J, Applegate IIR, Tang J (2016) An experimental model of vasovagal syncope induces cerebral hypoperfusion and fainting-like behavior in awake rats. PLOS One 11:e0163280. https://doi.org/10.1371/journal.pone.0163280

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Munns S, Owerkowics T, Andrewartha S, Frappell P (2012) The accessory role of the diaphragmaticus muscle in lung ventilation in the estuariane crocodile Crocodylus porosus. J Exp Biol 215:845–852

    Article  Google Scholar 

  • Nifong J, Silliman B (2013) Impacts of a large-bodied, apex predator (Alligator mississippiensis Daudin 1801) on salt marsh food webs. J Exp Mar Biol Ecol 440:185–191

    Article  Google Scholar 

  • O’Brien T, Dunlap W (1975) Tonic immobility in the blue crab (Callinectes sapidus, Rathbun): Its relation to threat of predation. J Comp Physiol Psych 89:86–94

    Article  Google Scholar 

  • Ouchi Y, Okada H, Yoshikawa E, Futatsubashi M, Nobezawa S (2001) Absolute changes in regional cerebral blood flow in association with upright posture in humans: an orthostatic PET study. J Nucl Med 42:707–712

    CAS  PubMed  Google Scholar 

  • Pham-Gia T, Hung T (2001) The mean and median absolute deviations. Math Comput Model 34:921–936

    Article  Google Scholar 

  • Prestrude A, Crawford F (1970) Tonic immobility in the lizard, Iguana iguana. Anim Behav 18:391–395

    Article  Google Scholar 

  • Reese AM (1914) The vascular system of the Florida alligator. Proc Acad Nat Sci Phila 66:413–425

    Google Scholar 

  • Sleeper B (1996) Alligators: Beneath the blackwater. Northwood Press, Wisconsin

    Google Scholar 

  • Smith E, Allison R, Crowder E (1974) Bradycardia in a free ranging alligator. Copeia 1974:770–772

    Article  Google Scholar 

  • Sung R, Du Z, Yu C, Yam M, Fok T (2000) Cerebral blood flow during vasovagal syncope induced by active standing or head up tilt. Arch Dis Child 82:154–158

    Article  CAS  Google Scholar 

  • Syme DA, Gamperl K, Jones DR (2002) Delayed depolarization of the cog-wheel valve and pulmonary-to-systemic shunting in alligators. J Exp Biol 205:1843–1851

    PubMed  Google Scholar 

  • van der Merwe NJ, Kotze S (1993) The topography of the thoracic and abdominal organs of the Nile crocodile (Crocodylus niloticus). Onderstepoort J Vet Res 60:219–222

    PubMed  Google Scholar 

  • Webster D, Lanthorn T, Hatton D, Meyer M (1978) Baroreceptor involvement in the immobility reflex of the frog: Evidence for a cross-species mechanism. Physiol Psychol 6:396–398

    Article  Google Scholar 

  • Webster D, Lanthorn T, Meyer M (1979) Immobility responses in Anolis carolinensis. Physiol Psychol 7:451–453

    Article  Google Scholar 

  • Weinheimer C, Pendergast D, Spotila J, Wilson D, Standora E (1982) Peripheral circulation in Alligator mississippiensis: effects of diving, fear, movement, investigator activities, and temperature. J Comp Physiol 148:57–63

    Article  Google Scholar 

  • White C, Seymour R (2014) The role of gravity in the evolution of mammalian blood pressure. Evolution 68:901–908

    Article  Google Scholar 

  • Wieling W, Thijs R, van Dijk N, Wilde A, Benditt D, Gert van Dijk J (2009) Symptoms and signs of syncope: a review of the link between physiology and clinical clues. Brain 132:2630–2642

    Article  Google Scholar 

  • Young BA, Street S, Wassersug R (1994) Anatomical and gravitational influences on cardiac displacement in snakes (Lepidosauria, Serpentes). Zoomorphology 114:169–175

    Article  CAS  Google Scholar 

  • Young BA, Wassersug R, Pinder A (1997) Gravitational gradients and blood flow patterns in specialized arboreal (Ahaetulla nasuta) and terrestrial (Crotalus adamanteus) snakes. J Comp Physiol B 167:481–493

    Article  CAS  Google Scholar 

Download references

Acknowledgements

The authors wish to thank Dr. Ruth Elsey and the Louisiana Department of Wildlife and Fisheries for their cooperation, and Dr. P. Kondrashov for his continued support. All procedures performed in studies involving animals were in accordance with the ethical standards of the institution or practice at which the studies were conducted.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Bruce A. Young.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Young, B.A., Adams, J., Segal, S. et al. Hemodynamics of tonic immobility in the American alligator (Alligator mississippiensis) identified through Doppler ultrasonography. J Comp Physiol A 204, 953–964 (2018). https://doi.org/10.1007/s00359-018-1293-x

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00359-018-1293-x

Keywords

Navigation