Summary
Despite the very considerable difficulties presented by the basic molluscan anatomy and the possession of a blood pigment with an oxygen carrying capacity that never exceeds 4.5 vols%, the cephalopod circulatory system contrives to deliver oxygen at a rate fully comparable with that of an active fish. This is achieved by adding accessory pumps to push blood through the gills, by a multiplicity of pulsatile veins and by raising the systemic blood pressure considerably above the levels found in other molluscs. Detailed control of blood distribution is a necessity in a system where the peripheral resistences may be expected to change dramatically when the animal starts to move and large parts of the central nervous system are apparently dedicated to this task. In this account we have reviewed blood pressure and flow at rest and in exercise. We have further examined the evidence which indicates how the animals modulate the cardiac output, drawing attention to the very different response found in cephalopods and the higher vertebrates.
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References
Alexandrowicz, J.S., A pulsating ganglion in the Octopoda. Proc. R. Soc. B.157 (1963) 562–573.
Alexandrowicz, J.S., The neurosecretory system of the vena cava in Cephalopoda. I.Eledone cirrhosa. J. mar. biol. Ass. U.K.44 (1964) 111–132.
Alexandrowicz, J. S., The neurosecretory system of the vena cava in Cephalopoda. II.Sepia officinalis andOctopus vulgaris. J. mar. biol. Ass. U.K.45 (1965) 209–228.
Barber, V.C., and Graziadei, P., The fine structure of cephalopod blood vessels. III. Vessel innervation. Z. Zellforsch. mikrosk. Anat. (1967) 162–174.
Bourne, G.B., Blood pressure in the squid,Loligo pealei. Comp. Biochem. Physiol.72A (1982) 23–27.
Bourne, G.B., Redmond, J.R., and Johansen, K.,Nautilus pompilius; branchial circulation enhanced by an auxiliary pumping mechanism. Experientia33 (1977) 1453.
Bourne, G.B., Redmond, J.R., and Johansen, K., Some aspects of haemodynamics inNautilus pompilius. J. exp. Zool.205 (1978) 63–70.
Boyle, P.R., and Knobloch, D., On growth of the octopusEledone cirrhosa. J. mar. biol. Ass. U.K.62 (1982) 277–296.
Brett, J.R., The relation of size to rate of oxygen consumption and sustained swimming speed of Sockeye salmon (Oncorhynchus nerka). J. Fish. Res. Bd Can.22 (1965) 1491–1501.
Browning, J., The density and dimensions of exchange vessels inOctopus pallidus. J. Zool. Lond.196 (1965) 569–579.
Driedzic, W.R., Contractile performance of cephalopod hearts under anoxic conditions. J. exp. Biol.117 (1985) 471–474.
Foti, L., Genoino, I.T., and Agnisolo, G.,In vitro cardiac performance inOctopus vulgaris (Lam). Comp. Biochem. Physiol.82C (1909) 483–488.
Fredericq, H., and Bacq, Z.M., Analyse quantitative des effects cardiaques de la stimulation du nerf vicéral des céphalopodes. Archs int. Physiol.49 (1939) 490–496.
Fry, H. J. B., The influence of the visceral nerves on the heart of cephalopods. J. Physiol. Lond.39 (1909) 184–206.
Gosline, J.M., and Shadwick, R.E., The biomechanics of the arteries ofNautilus, Nototodarus andSepia. Pacific Science36 (1982) 283–296.
Gosline, J.M., and Shadwick, R.E., The role of elastic energy storage mechanisms in swimming: an analysis of muscle elasticity in escape jetting by the squidLoligo opalescens. Can. J. Zool.61 (1983) 1421–1431.
Gray, E. G., Electron microscopy of the glio-vascular organisation of the brain ofOctopus. Phil. Trans. R. Soc. B255 (1969) 13–32.
Hill, R.B., and Welsh, J.H., Heart circulation and blood cells, in: Physiology of the Mollusca, vol. 2, pp. 126–174. Eds K. M. Wilbur and C. M. Yonge. Academic Press, New York 1966.
Houlihan, D.F., Duthie, G., Smith, P.J., Wells, M.J., and Wells, J., Ventilation and circulation during exercise inOctopus vulgaris. J. comp. Physiol. B156 (1986) 683–689.
Houlihan, D.F., Innes, A.J., Wells, M.J., and Wells, J., Oxygen consumption and blood gases ofOctopus vulgaris in hypoxic conditions. J. comp. Physiol.148 (1982) 35–40.
Johansen, K., Cardiac output in the large cephalopodO. dofleini. J. exp. Biol.42 (1965) 475–480.
Johansen, K., Brix, O., and Lykkeboe, G., Blood gas transport in the cephalopod,Sepia officinalis. J. exp. Biol.99 (1982) 331–338.
Johansen, K., and Martin, A.W., Circulation in the cephalopod,Octopus dofleini, Comp. Biochem. Physiol.5 (1962) 161–176.
Jones, H.D., The circulatory systems of gastropods and bivalves, in: The Mollusca, vol. 5 (II), pp. 189–238. Eds A.S.M. Saleuddin and K.M. Wilbur, Academic Press, New York 1983.
Kier, W.A., The functional morphology of the musculature of squid (Loliginidae) arms and tentacles. J. Morph.172 (1982) 179–192.
Koch, U.T., and Koester, J., Time sharing of heart power: Cardiovascular adaptations to food-arousal inAplysia. J. comp. Physiol.149 (1982) 31–42.
Kruta, V., Effects de l'excitation des nerfs viscéraux sur l'activité cardiaque chez les céphalopodes. C.r. séanc. Soc. Biol.122 (1936) 582–585.
Kuwasawa, K., Effects of ACh and IJPs on the av valve and ventricle ofDolabella auricularia. Am. Zool.19 (1979) 129–143.
Maginnis, L.A., and Wells, M.J., The oxygen consumption ofOctopus cyanea. J. exp. Biol.51 (1969) 607–613.
Martin, A.W., and Aldrich, F.A., Comparison of hearts and branchial heart appendages in some Cephalopods. Can. J. Zool.48 (1970) 751–756.
Mislin, H., Nachweis einer reflektorischen Regulation des peripheren Kreislaufs der Cephalopoden. Experientia6 (1950) 467–468.
Mislin, H., and Kauffmann, M., Der aktive Gefässpuls in der Arm-Schirmhaut der Cephalopoden. Revue suisse Zool.55 (1948) 267–271.
O'Dor, R.K., Respiratory metabolism and swimming performance of the squid,Lologo opalescens. Can. J. Fish. aquat. Sci.39 (1982) 580–587.
O'Dor, R.K., and Wells, M.J., Circulation time, blood reserves and extracellular space in a cephalopod. J. exp. Biol.11 (1984) 461–464.
Ranson, W.B., On the cardiac rhythm of invertebrates. J. Physiol.5 (1884) 262–341.
Read, K.R.H., Molluscan haemoglobin and myoglobin, in: Physiology of Mollusca, chap. 6, vol. 2, pp. 209–232. Eds K. M. Wilbur and C. M. Yonge. Academic Press, New York 1966.
Santer, R.M., Greer Walker, M.G., Emerson, L., and Witthames, P.R., On the morphology of the heart ventricle in marine teleost fish (Teleostei) Comp. Biochem. Physiol.76A (1983) 453–457.
Shadwick, R.E., and Gosline, J.M., Elastic arteries in invertebrates: mechanics of the octopus aorta. Science213 (1981) 759–761.
Shadwick, R.E., and Gosline, J.M., Physical and chemical properties of rubber-like elastic fibres from the octopus aorta. J. exp. Biol.114 (1985a) 239–257.
Shadwick, R.E., and Gosline, J.M., Mechanical properties of the octopus aorta. J. exp. Biol.114 (1985b) 259–284.
Shadwick, R.E., Gosline, J.M., and Milsom, W.K., Arterial haemodynamics in the cephalopod mollusc,Octopus dofleini. J. exp. Biol. (1987) in press.
Skramlik, E. von, Über den Kreislauf bei den Weichtieren. Ergbn. Biol.18 (1941) 88–286.
Smith, L.S., The role of venous peristalsis in the arm circulation ofOctopus dofleini. Comp. Biochem. Physiol.7 (1962) 269–275,.
Smith, P.J.S., Studies on the circulatory organs of the octopus,Eledone cirrhosa (Lam.). Ph. D. Thesis, University of Aberdeen, Scotland 1979.
Smith, P.J.S., The role of venous pressure in regulation of output from the heart of the octopus,Eledone cirrhosa (Lam.). J. exp. Biol.93 (1981a) 243–255.
Smith, P.J.S., The octopod ventricular cardiogram. Comp. Biochem. Physiol.70A (1981b) 103–105.
Smith, P.J.S., The contribution of the branchial heart to the accessory branchial pump in the Octopoda. J. exp. Biol.98 (1982) 229–237.
Smith, P.J.S., Molluscan circulation: Haemodynamics and the heart, in: Circulation, Respiration and Metabolism, pp. 344–355. Ed. R. Gilles, Springer-Verlag, Berlin-Heidelberg 1985a.
Smith, P.J.S., Cardiac performance in response to loading pressures for two molluscan species,Busycon canaliculatum (L.) (Gastropoda) andMercenaria mercenaria (L.) (Bivalvia). J. exp. Biol.119 (1985b) 301–320.
Smith, P.J.S., Cardiac output in the Mollusca: Scope and regulation. Experientia (1987) submitted.
Smith, P.J.S., and Boyle, P.R., The cardiac innervation ofEledone cirrhosa (Lamarck) (Mollusca: Cephalopoda). Phil. Trans R. Soc. (Lond.)B300 (1983) 493–511.
Smith, P.J.S., Duthie, G.G., Wells, M.J., and Houlihan, D.F., Continuous recording of arterial blood PO2 inOctopus vulgaris during progressive hypoxia and movement. J. exp. Biol.117 (1985) 475–479.
Smith, P.J.S., and Hill, R.B., Cardiac performance in response to loading pressures and perfusion with 5-hydroxytryptamine in the isolated heart ofBusycon canaliculatum (Gastropoda, Prosobranchia). J. exp. Biol.123 (1986) 243–253.
Smith, P.J.S., and Hill, R.B. Modulation of output from an isolated gastropod heart: Effects of acetylcholine and FMRFamide. J. exp. Biol. (1987) in press.
Ward, D.V., and Wainwright, S.A., Locomotory aspects of squid mantle structure. J. Zool.167 (1972) 437–449.
Webber, D.M., and O'Dor, R.K., Respiration and swimming performance of short-finned squid (Illex illecebrosus). NAFO Sci. coun. Stud.9 (1985) 133–138.
Wells, M.J., The heartbeat ofOctopus vulgaris. J. exp. Biol.78 (1979) 87–104.
Wells, M.J., Nervous control of the heartbeat inOctopus. J. exp. Biol.85 (1980) 111–128.
Wells, M.J., Circulation in cephalopods, in: The Mollusca, vol. 5, pp. 239–290. Eds K.M. Wilbur and A.S.M., Saleuddin. Academic Press, New York 1983a.
Wells, M.J., Hormones and the circulation inOctopus, in: Molluscan Neuro-Endocrinology, pp. 221–228. Eds J. Lever and H.H. Boer. North Holland, Amsterdam 1983b.
Wells, M.J., Duthie, G.G. Houlihan, D.F., Smith, P.J.S., and Wells, J., Blood flow and pressure changes in exercising octopuses. J. exp. Biol. (1987) in press.
Wells, M.J., and Mangold, K., The effects of extracts from neurosecretory cells in the anterior vena cava and pharyngo-ophthalmic vein upon the hearts of intact free-moving octopuses. J. exp. Biol.84 (1980) 319–334.
Wells, M.J., O'Dor, R.K., Mangold, K., and Wells, J., Diurnal changes in activity and metabolic rate inOctopus vulgaris. Mar. Behav. Physiol.9 (1983a) 275–287.
Wells, M.J., O'Dor, R.K., Mangold, K., and Wells, J., Oxygen consumption in movement byOctopus. Mar. Behav. Physiol.9 (1983b) 289–303.
Wells, M.J., O'Dor, R.K., Mangold, K., and Wells, J., Feeding and metabolic rate inOctopus. Mar. Behav. Physiol.9 (1983c) 305–317.
Wells, M.J., and Smith, P.J.S., The ventilation cycle inOctopus. J. exp. Biol.116 (1985) 375–383.
Wells, M.J., and Wells, J., The circulatory response to acute hypoxia inOctopus. J. exp. Biol.104 (1983) 59–71.
Wells, M.J., and Wells, J., Ventilation frequencies and stroke volumes in acute hypoxia inOctopus. J. exp. Biol.118 (1986a) 445–448.
Wells, M.J., and Wells, J., Blood flow in acute hypoxia in an cephalopod. J. exp. Biol.122 (1986b) 345–353.
Young, J.Z., The anatomy of the brain ofOctopus. Clarendon Press, Oxford 1971.
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Wells, M.J., Smith, P.J.S. The performance of the octopus circulatory system: A triumph of engineering over design. Experientia 43, 487–499 (1987). https://doi.org/10.1007/BF02143577
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DOI: https://doi.org/10.1007/BF02143577