Journal of Comparative Physiology A

, Volume 204, Issue 11, pp 953–964 | Cite as

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

  • Bruce A. YoungEmail author
  • James Adams
  • Solomon Segal
  • Tatyana Kondrashova
Original paper


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.


Perfusion Blood flow Crocodilian Posture Carotid 



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.


  1. Alboni P, Alboni M (2017) Typical vasovagal syncope as a “defense mechanism” for the heart by contrasting sympathetic overactivity. Clin Auton Res 27:253–261CrossRefGoogle Scholar
  2. Alboni P, Alboni M, Bertorelle G (2008) The origin of vasovagal syncope: To protect the heart or to escape predation? Clin Auton Res 18:170–178CrossRefGoogle Scholar
  3. Altimiras J, Franklin C, Axelsson M (1998) Relationships between blood pressure and heart rate in the saltwater crocodile Crocodylus porosus. J Exp Biol 201:2235–2242PubMedGoogle Scholar
  4. 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 171:341–346CrossRefGoogle Scholar
  5. Axelsson M, Holm S, Nilsson S (1989) Flow dynamics of the crocodilian heart. Am J Physiol 256:R875–R879PubMedGoogle Scholar
  6. 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 199:359–365PubMedGoogle Scholar
  7. 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 200:807–814PubMedGoogle Scholar
  8. Berger P (1987) The reptilian baroreceptor and its role in cardiovascular control. Am Zool 27:111–120CrossRefGoogle Scholar
  9. Caro T (2014) Antipredator deception in terrestrial vertebrates. Curr Zool 60:16–25CrossRefGoogle Scholar
  10. Claessens L (2009) A cineradiographic study of lung ventilation in Alligator mississippiensis. J Exp Zool A 311:563–585CrossRefGoogle Scholar
  11. Clerici C, Veneroni L (2012) The impossible escape: Studies on the tonic immobility in animals from a comparative psychology perspective. Novinka Science, New YorkGoogle Scholar
  12. 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):9–17CrossRefGoogle Scholar
  13. 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 231:484–499CrossRefGoogle Scholar
  14. Crawford FT (1977) Induction and duration of tonic immobility. Psychol Rec 1:89–107CrossRefGoogle Scholar
  15. Crossley D, Hicks J, Altimiras J (2003) Ontogeny of baroreflex control in the American alligator Alligator mississippiensis. J Exp Biol 206:2895–2902CrossRefGoogle Scholar
  16. 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 72:25–31CrossRefGoogle Scholar
  17. 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 39:1039–1045CrossRefGoogle Scholar
  18. 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 62:1171–1178CrossRefGoogle Scholar
  19. Farmer CG, Uriona T, Olsen D, Steenblik M, Sanders K (2008) The right-to-left shunt in crocodilians serves digestion. Physiol Biochem Zool 81:125–137CrossRefGoogle Scholar
  20. Findsen A, Crossley D, Wang T (2018) Feeding alters blood flow patterns in the American alligator (Alligator mississippiensis). Comp Biochem Phys A 215:1–5CrossRefGoogle Scholar
  21. Franklin C, Axelsson M (1994) The intrinsic properties of an in situ perfused crocodile heart. J Exp Biol 186:269–288PubMedGoogle Scholar
  22. Franklin C, Axelsson M (2000) Physiology: an actively controlled heart valve. Nature 406:847–848CrossRefGoogle Scholar
  23. Gallup G (1973) Simulated predation and tonic immobility in Anolis carolinensis. Copeia 1973:623–624CrossRefGoogle Scholar
  24. Gallup G (1974) Animal hypnosis: factual status of a fictional concept. Psychol Bull 81:836–853CrossRefGoogle Scholar
  25. Gallup G (1977) Tonic immobility: the role of fear and predation. Psychol Rec 27:41–61CrossRefGoogle Scholar
  26. Gans C, Clark B (1976) Studies on ventilation of Caiman crocodilus (Crocodilia: Reptilia). Resp Physiol 26:285–301CrossRefGoogle Scholar
  27. Gaskell W, Gadow H (1884) On the anatomy of the cardiac nerves in certain cold-blooded vertebrates. J Physiol 5:362–372CrossRefGoogle Scholar
  28. Gaunt A, Gans C (1969) Diving bradycardia and withdrawal bradycardia in Caiman crocodilus. Nature 223:207–208CrossRefGoogle Scholar
  29. Gehlbach F (1970) Death-feigning and erratic behaviour in leptotyphlopid, colubrid, and elapid snakes. Herpetologica 26:24–34Google Scholar
  30. 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 1–152Google Scholar
  31. 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 156:458–462CrossRefGoogle Scholar
  32. Hatton D, Lanthorn T, Webster D, Meyer M (1978) Baroreceptor involvement in the immobility reflex. Behav Biol 22:122–127CrossRefGoogle Scholar
  33. 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 26:89–96CrossRefGoogle Scholar
  34. 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 8:199–203CrossRefGoogle Scholar
  35. Hoagland H (1928a) The mechanism of tonic immobility in vertebrates. J Gen Physiol 1:426–447Google Scholar
  36. Hoagland H (1928b) On the mechanism of tonic immobility. J Gen Physiol 11:715–741CrossRefGoogle Scholar
  37. Huggins S, Hoff H, Pena R (1969) Heart and respiratory rates in crocodilian reptiles under conditions of minimal stimulation. Physiol Zool 42:320–333CrossRefGoogle Scholar
  38. Jones D, Shelton G (1993) The physiology of the alligator heart: left aortic flow patterns and right-to-left shunts. J Exp Biol 176:247–269Google Scholar
  39. 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 165–212CrossRefGoogle Scholar
  40. Klemm W (1976) Identity of sensory and motor systems that are critical to the immobility reflex (‘animal hypnosis’). J Neurosci Res 2:57–69CrossRefGoogle Scholar
  41. Kunin RA (1967) Electroencephalograph studies in animal hypnosis. Am J Clin Hypn 9:256–261CrossRefGoogle Scholar
  42. 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 49:764–766CrossRefGoogle Scholar
  43. Lillywhite H (1993) Orthostatic intolerance of viperid snakes. Physiol Zool 66:1000–1014CrossRefGoogle Scholar
  44. Lillywhite HB, Albert J, Sheehy C, Seymour RS (2012) Gravity and the evolution of cardiopulmonary morphology in snakes. Comp Biochem Physiol A 161:230–242CrossRefGoogle Scholar
  45. 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. CrossRefPubMedPubMedCentralGoogle Scholar
  46. 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 215:845–852CrossRefGoogle Scholar
  47. 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 440:185–191CrossRefGoogle Scholar
  48. 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 89:86–94CrossRefGoogle Scholar
  49. 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 42:707–712PubMedGoogle Scholar
  50. Pham-Gia T, Hung T (2001) The mean and median absolute deviations. Math Comput Model 34:921–936CrossRefGoogle Scholar
  51. Prestrude A, Crawford F (1970) Tonic immobility in the lizard, Iguana iguana. Anim Behav 18:391–395CrossRefGoogle Scholar
  52. Reese AM (1914) The vascular system of the Florida alligator. Proc Acad Nat Sci Phila 66:413–425Google Scholar
  53. Sleeper B (1996) Alligators: Beneath the blackwater. Northwood Press, WisconsinGoogle Scholar
  54. Smith E, Allison R, Crowder E (1974) Bradycardia in a free ranging alligator. Copeia 1974:770–772CrossRefGoogle Scholar
  55. 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 82:154–158CrossRefGoogle Scholar
  56. Syme DA, Gamperl K, Jones DR (2002) Delayed depolarization of the cog-wheel valve and pulmonary-to-systemic shunting in alligators. J Exp Biol 205:1843–1851PubMedGoogle Scholar
  57. 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 60:219–222PubMedGoogle Scholar
  58. 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 6:396–398CrossRefGoogle Scholar
  59. Webster D, Lanthorn T, Meyer M (1979) Immobility responses in Anolis carolinensis. Physiol Psychol 7:451–453CrossRefGoogle Scholar
  60. 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 148:57–63CrossRefGoogle Scholar
  61. White C, Seymour R (2014) The role of gravity in the evolution of mammalian blood pressure. Evolution 68:901–908CrossRefGoogle Scholar
  62. 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 132:2630–2642CrossRefGoogle Scholar
  63. Young BA, Street S, Wassersug R (1994) Anatomical and gravitational influences on cardiac displacement in snakes (Lepidosauria, Serpentes). Zoomorphology 114:169–175CrossRefGoogle Scholar
  64. 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 167:481–493CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of Anatomy, Kirksville College of Osteopathic MedicineA.T. Still UniversityKirksvilleUSA
  2. 2.Department of Family Medicine, Preventitive Medicine, and Community HealthKirksville College of Osteopathic Medicine, A.T. Still UniversityKirksvilleUSA

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