Skip to main content Accessibility help
×
Home
Hostname: page-component-55b6f6c457-b6fb2 Total loading time: 0.304 Render date: 2021-09-25T04:34:38.137Z Has data issue: true Feature Flags: { "shouldUseShareProductTool": true, "shouldUseHypothesis": true, "isUnsiloEnabled": true, "metricsAbstractViews": false, "figures": true, "newCiteModal": false, "newCitedByModal": true, "newEcommerce": true, "newUsageEvents": true }

Article contents

Did lungs and the intracardiac shunt evolve to oxygenate the heart in vertebrates?

Published online by Cambridge University Press:  08 February 2016

Colleen Farmer*
Affiliation:
Brown University, Providence, Rhode Island

Abstract

Traditional wisdom of the evolution of lungs in fishes is that lungs arose when gill ventilation was hindered by an aquatic habitat that was low in oxygen. This scenario has been buttressed primarily by a proposed correlation between extant air-breathing fishes and hypoxic habitats, as well as by the fact that early vertebrate fossils were found in sediments believed to indicate a semi-arid environment. There are problems with this scenario, yet it retains a dominant influence on how the evolution of aerial respiration is viewed. This paper presents a new hypothesis for lung evolution that is more consistent with the fossil record and physiology of extant animals than the traditional scenario; I propose that lungs evolved to supply the heart with oxygen. The primitive vertebrate heart was spongy in architecture and devoid of coronary support, obtaining oxygen from luminal blood. By supplying oxygen to this tissue, lungs may have been important in ancient fishes for sustaining activity, regardless of environment. Furthermore, this function for lungs may have influenced cardiovascular adaptations of tetrapods because their divided cardiovascular system isolates the right side of the heart from pulmonary oxygen. I propose that three innovations compensate for this isolation: In extant amphibians oxygen-rich blood from cutaneous and buccal respiration enters the right side of the heart; in chelonians and lepidosaurs the intracardiac shunt washes oxygen-rich blood into the right side of the heart; in mammals, birds, and perhaps in crocodilians, support of the heart by coronary vasculature eliminates this problem.

Type
Articles
Copyright
Copyright © The Paleontological Society 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Barrell, J. 1916. Influence of Silurian–Devonian climates on the rise of airbreathing vertebrates. Geological Society of America Bulletin 27:387436.CrossRefGoogle Scholar
Bates, D. W., and Vinsonhaler, R. 1957. The use of louvers as a means of guiding fish at the Tracy, California, pumping plant. Transactions of the American Fisheries Society for 1956 86:3857.CrossRefGoogle Scholar
Beamish, F. W. H. 1966. Muscular fatigue and mortality in haddock, Melanogrammus aeglefinus, caught by otter trawl. Journal of the Fisheries Resource Board of Canada 23:15071521.CrossRefGoogle Scholar
Becker, G. C. 1983. Fishes of Wisconsin. University of Wisconsin, Madison.Google Scholar
Bennett, A. F. 1978. Activity metabolism of the lower vertebrates. Annual Review of Physiology 400:447469.CrossRefGoogle Scholar
Black, E. C. 1955. Blood levels of hemoglobin and lactic acid in some freshwater fishes following exercise. Journal of the Fisheries Resource Board of Canada 12:917929.CrossRefGoogle Scholar
Black, E. C. 1957a. Alterations in the blood level of lactic acid in certain salmonoid fishes following muscular activity. I. Kamloops trout, Salmo gairdneri. Journal of the Fisheries Resource Board of Canada 14:117134.CrossRefGoogle Scholar
Black, E. C. 1957b. Alterations in the blood level of lactic acid in certain salmonoid fishes following muscular activity. II. Lake trout, Salvelinus namaycush. Journal of the Fisheries Resource Board of Canada 14:645649.CrossRefGoogle Scholar
Black, E. C. 1957c. Alterations in the blood level of lactic acid in certain salmonoid fishes following muscular activity. III. Sockeye salmon, Oncorhynchus nerka. Journal of the Fisheries Resource Board of Canada 14:807814.CrossRefGoogle Scholar
Black, E. C. 1958. Hyperactivity as a lethal factor in fish. Journal of the Fisheries Resource Board of Canada 15:573586.CrossRefGoogle Scholar
Black, E. C., Robertson Connor, A., Lam, K., and Chiu, W. 1962. Changes in glycogen, pyruvate and lactate in rainbow trout (Salmo gairdneri) during and following muscular activity. Journal of the Fisheries Resource Board of Canada 19:409436.CrossRefGoogle Scholar
Boucot, A., and Janis, C. 1983. Environment of the early Paleozoic vertebrates. Palaeogeography, Palaeoclimatology, Palaeoecology 41:251287.CrossRefGoogle Scholar
Brady, A. J., and Dubkin, C. 1964. Coronary circulation in the turtle ventricle. Biochemical Physiology 13:119128.Google ScholarPubMed
Brainerd, E. L. 1994. The evolution of lung-gill bimodal breathing and the homology of vertebrate respiratory pumps. American Zoologists 34:289299.CrossRefGoogle Scholar
Bray, A. A. 1985. The evolution of the terrestrial vertebrates: environmental and physiological considerations. Philosophical Transactions of the Royal Society of London B 309:289322.CrossRefGoogle ScholarPubMed
Breisch, E. A., White, F., Jones, H. M., and Laurs, R. M. 1983. Ultrastructural morphometry of the myocardium of Thunnus alalunga. Cell and Tissue Research 233:427438.CrossRefGoogle ScholarPubMed
Burggren, W., and Randall, D. 1978. Oxygen uptake and transport during hypoxic exposure in the sturgeon Acipenser transmontanus. Respiration Physiology 34:171183.CrossRefGoogle ScholarPubMed
Coates, M. I., and Clack, J. A. 1995. Romer's gap: tetrapod origins and terrestriality. Bulletin du Museum national d'Histoire naturelle 4e séries 17:373388.Google Scholar
Daeschler, E. B., and Shubin, N. H. 1995. Tetrapod origins. Paleobiology 21:404409.CrossRefGoogle Scholar
Davie, P. S., and Farrell, A. P. 1991. The coronary and luminal circulations of the myocardium of fishes. Canadian Journal of Zoology 69:19932001.CrossRefGoogle Scholar
Denison, R. H. 1951. Late Devonian fresh-water fishes from the western United States. Fieldiana (Geology) 11:221261.Google Scholar
Denison, R. H. 1956. A review of the habitat of the earliest vertebrates. Fieldiana (Geology) 11:361457.Google Scholar
Denison, R. H. 1968. Early Devonian lungfishes from Wyoming, Utah and Idaho. Fieldiana (Geology) 17:353413.Google Scholar
Driedzic, W. R., and Gesser, H. 1994. Energy metabolism and contractility in ectothermic vertebrate hearts: hypoxia, acidosis, and low temperature. Physiological Reviews 74:221258.CrossRefGoogle ScholarPubMed
Emery, S. H., Mangano, C., and Randazzo, V. 1985. Ventricle morphology in pelagic elasmobranch fishes. Comparative Biochemistry and Physiology A82: 635–543.Google Scholar
Farmer, C. G., and Jackson, D. C. 1995. The importance of lung ventilation during activity in Amia calva. American Zoologist 35:62A.Google Scholar
Farrell, A. P. 1984. A review of cardiac performance in the teleost heart: intrinsic and humoral regulation. Canadian Journal of Zoology 62:523536.CrossRefGoogle Scholar
Farrell, A. P., and Jones, D. R. 1992. The heart. In Hoar, W. S., Randall, D. J., and Farrell, A. P., eds. Fish Physiology 12(A):188Academic Press, San Diego.Google Scholar
Farrell, A. P., Small, S., and Graham, M. S. 1989. Effect of heart rate and hypoxia on the performance of a perfused trout heart. Canadian Journal of Zoology 67:274280.CrossRefGoogle Scholar
Foxon, G. E. H. 1950. A description of the coronary arteries in dipnoan fishes and some remarks on their importance from the evolutionary standpoint. Journal of Anatomy, London 84:121131.Google ScholarPubMed
Foxon, G. E. H. 1955. Problems of the double circulation in vertebrates. Biological Reviews 30:196228.CrossRefGoogle Scholar
Fricke, H., Hissmann, K., Schauer, J., Reinicke, O., Kasang, L., and Plante, R. 1991. Habitat and population size of the coelacanth Latimeria chalumnae at Grand Comoro. Environmental Biology of Fishes 32:287300.CrossRefGoogle Scholar
Gans, C. 1970. Respiration in early tetrapods—the frog is a red herring. Evolution 24:723734.CrossRefGoogle ScholarPubMed
Gans, C. 1989. Stages in the origin of vertebrates: analysis by means of scenarios. Biological Reviews 64:221268.CrossRefGoogle ScholarPubMed
Gesser, H. 1985. Effects of hypoxia and acidosis on fish heart performance. Pp. 402410In Gilles, R., ed. Respiration and metabolism: current comparative approaches. Springer, Berlin.CrossRefGoogle Scholar
Gesser, H., and Poupa, O. 1983. Acidosis and cardiac muscle contractility: comparative aspects. Comparative Biochemistry and Physiology 76A:559566.CrossRefGoogle Scholar
Gesser, H., Andresen, P., Brams, P., and Sund-Laursen, J. 1982. Inotropic effects of adrenaline on the anoxic or hypercapnic myocardium of rainbow trout and eel. Journal of Comparative Physiology 147:123128.CrossRefGoogle Scholar
Goodyear, P. C. 1967. Feeding habits of three species of gars, Lepisosteus, along the Mississippi gulf coast. Transactions of the American Fisheries Society 96:297300.CrossRefGoogle Scholar
Graham, J. B. 1976. Respiratory adaptations of marine air-breathing fishes. Pp. 165187In Hughes, G. M., ed. Respiration of amphibious vertebrates. Academic Press, London.Google Scholar
Graham, J. B. 1994. An evolutionary perspective for bimodal respiration: a biological synthesis of fish air breathing. American Zoologist 34:229237.CrossRefGoogle Scholar
Graham, M. S., and Farrell, A. P. 1990. Myocardial oxygen consumption in trout acclimated to 5° and 15°C. Physiological Zoology 63:536554.CrossRefGoogle Scholar
Grant, R. T., and Regnier, M. 1926. The comparative anatomy of the cardiac coronary vessels. Heart 13:285317.Google Scholar
Grigg, G. 1965. Studies on the Queensland lungfish, Neoceratodus Forsteri (Krefft) III. Aerial respiration in relation to habits. Australian Journal of Zoology 13:413421.CrossRefGoogle Scholar
Gunther, A. 1871a. Description of Ceratodus, a genus of Ganoid fishes, recently discovered in rivers of Queensland, Australia. Philosophical Transactions of the Royal Society of London 161:511571.CrossRefGoogle Scholar
Gunther, A. 1871b. The new Ganoid fish from Queensland (Ceratodus). Nature 1871:406408.Google Scholar
Hicks, J. W. 1993. Mechanism of intracardiac shunting in reptiles. Pp. 249259In Scheid, P., ed. Respiration in health and disease. G. Fischer Verlag, Stuttgart.Google Scholar
Hicks, J. W. 1994. Adrenergic and cholinergic regulation of intracardiac shunting. Physiological Zoology 67:13251346.CrossRefGoogle Scholar
Hicks, J. W. 1995. Cardiac shunting in reptiles: mechanisms, regulation and physiological function. In Gans, C. and Gaunt, A. S., eds. The biology of the Reptilia. Morphology, Vol. G, The visceral organs. Society for the Study of Amphibians and Reptiles, Ithaca, N.Y.Google Scholar
Hicks, J. W., and Wood, S. C. 1989. Oxygen homeostasis in lower vertebrates: the impact of external and internal hypoxia. Pp. 311341In Wood, S. C., ed. Comparative pulmonary physiology. Marcel Dekker, New York.Google Scholar
Hochachka, P. W., Guppy, M., Guderley, H., Storey, K. B., and Hulbert, W. C. 1978. Metabolic biochemistry of water- vs. air-breathing in osteoglossids: heart enzymes and ultrastructure. Canadian Journal of Zoology 56:759768.CrossRefGoogle Scholar
Jackson, D. C., Shi, H., Singer, J. H., Hamm, P. H., and Lawler, R. G. 1995. Effects of input pressure on in vitro turtle heart during anoxia and acidosis: a 31P-NMR study. American Journal of Physiology 268 (Regulatory Integrative Comparative Physiology 37):R683R689.Google ScholarPubMed
Johansen, K. 1970. Air breathing in fishes. Pp. 361411In Hoar, W. S. and Randall, D. J., eds. Fish physiology, Vol. 4. Academic Press, New York.Google Scholar
Johansen, K. 1985. A Phylogenetic overview of cardiovascular shunts. Pp. 1732In Johansen, K. and Burggren, W., eds. Alfred Benzon Symposium 21: Cardiovascular shunts; phylogenetic, ontogenetic and clinical aspects. Munksgaard, Copenhagen.Google Scholar
Johansen, K., and Burggren, W. 1980. Cardiovascular function in the lower vertebrates. Pp. 61117In Bourne, G. H., ed. Hearts and heart-like organs. Academic Press, New York.Google Scholar
Johansen, K., and Hanson, D. 1968. Functional anatomy of the hearts of lungfishes and amphibians. American Zoologist 8:191210.CrossRefGoogle ScholarPubMed
Johansen, K., and Lenfant, C. 1967. Respiratory function in the South American lungfish, Lepidosiren paradoxa (Fitz). Journal of Experimental Biology 46: 205–18.Google Scholar
Johansen, K., Lenfant, C., and Grigg, G. C. 1967. Respiratory control in the lungfish, Neoceratodus forsteri (Krefft). Comparative Biochemistry and Physiology 20:835845.CrossRefGoogle Scholar
Johansen, K., Lenfant, C., and Hanson, D. 1968. Cardiovascular dynamics in the lungfishes. Zeitschrift für vergleichende Physiologie 59:157186.Google Scholar
Johansen, K., Hanson, D., and Lenfant, C. 1970. Respiration in a primitive air breather, Amia calva. Respiration Physiology 9:162174.CrossRefGoogle Scholar
Jones, D. R., and Randall, D. J. 1978. The respiratory and circulatory systems during exercise. In Hoar, W. S. and Randall, D. J., eds. Fish Physiology 7:425501. Academic Press, New York.Google Scholar
Kiceniuk, J. W., and Jones, D. R. 1977. The oxygen transport system in trout (Salmo gairdneri) during sustained exercise. Journal of Experimental Biology 69:247260.Google Scholar
Kohmoto, T., Argenziano, M., Yamamoto, N., Vliet, K. A., Gu, A., DeRosa, C. M., Fisher, P., Spotnitz, H. M., Burkhoff, D., and Smith, C. R. 1997. Assessment of transmyocardial perfusion in alligator hearts. Circulation 95:15851591.CrossRefGoogle ScholarPubMed
Kramer, D. L., Lindsey, C. C., Moodie, G. E. E., and Stevens, E. D. 1978. The fishes and the aquatic environment of the central Amazon basin, with particular reference to respiratory patterns. Canadian Journal of Zoology 56:717729.CrossRefGoogle Scholar
Krefft, G. 1870. Description of a gigantic amphibian allied to genus Lepidosiren, from Wide Bay district, Queensland. Proceedings of the Zoological Society of London 1870:221224.Google Scholar
Krosniunas, E. H., and Hicks, J. W. 1994. Cardiovascular correlates of behavior in the turtle. The Physiologist 37(5):A-95[Abstract.]Google Scholar
Lenfant, C., and Johansen, K. 1968. Respiration in the African lungfish Protopterus aethiopicus: I. Respiratory properties of blood and normal patterns of breathing and gas exchange. Journal of Experimental Biology 49:437452.Google ScholarPubMed
Liem, K. F. 1988. Form and function of lungs: The evolution of air breathing mechanisms. American Zoologist 28:739759.CrossRefGoogle Scholar
MacKinnon, M. R., and Heatwole, H. 1981. Comparative cardiac anatomy of the reptilia. IV. The coronary arterial circulation. Journal of Morphology 170:127.CrossRefGoogle ScholarPubMed
Magid, A. M. A. 1966. Breathing and function in the spiracles in Polypterus senegalus. Animal Behavior 14:530533.CrossRefGoogle ScholarPubMed
Maisey, J. G. 1996. Discovering fossil fishes. H. Holt, New York.Google Scholar
Mallatt, J. 1985. Reconstructing the life cycle and the feeding of ancestral vertebrates. Pp. 5968In Foreman, R. E., Gorbman, A., Dodd, J. M., and Olsson, R., eds. Evolutionary biology of primitive fishes. Plenum, New York.CrossRefGoogle Scholar
Martin, D., Grably, S., Royer, F., Benchetrit, G., Rossi, A., Tota, B., Marciano, V., Farina, F. and Zummo, G. 1987. Metabolic alterations induced by hypoxia in the tortoise heart, comparison between spongy and compact myocardium. Comparative Biochemistry and Physiology 86A:319323.CrossRefGoogle Scholar
Matthew, W. D. 1915. Climate and evolution. Annals of the New York Academy of Sciences 24:171318.CrossRefGoogle Scholar
Millot, J., Anthony, J. and Robineau, J. 1978. Anatomie de Latimeria chalumnae, Vol. 3. Centre nationale de la Recherche scientifique, Paris.Google Scholar
Morris, C. 1892. The origin of lungs, a chapter in evolution. American Naturalist 26:975986.CrossRefGoogle Scholar
Navaratnam, V. 1980. Anatomy of the mammalian heart. Pp. 349374In Bourne, G. H., ed. Hearts and heart-like organs. Academic Press, New York.Google Scholar
Nelson, J. S. 1984. Fishes of the world. Wiley, New York.Google Scholar
Packard, G. C. 1974. The evolution of air-breathing in Paleozoic gnathostome fishes. Evolution 28:320325.CrossRefGoogle ScholarPubMed
Parker, R. R., and Black, E. C. 1959. Muscular fatigue and mortality in troll-caught chinook salmon (Oncorhynchus tshawytscha). Journal of the Fisheries Resource Board of Canada 16:95106.CrossRefGoogle Scholar
Paulik, G. J., and De Lacy, A. C. 1957. Swimming abilities of upstream migrant silver salmon, sockeye salmon and steelhead at several water velocities. Technical Report 44:140. School of Fisheries, University of Washington, Seattle.Google Scholar
Poupa, O., and Lindström, L. 1983. Comparative and scaling aspects of heart and body weights with reference to blood supply of cardiac fibers. Comparative biochemistry and physiology 76A:412421.Google Scholar
Rahn, H., Rahn, K. B., Howell, B. J., Gans, C., and Tenney, S. M. 1971. Air-breathing of the garfish (Lepisosteus osseus). Respiration Physiology 11:285307.CrossRefGoogle Scholar
Randall, D., Burggren, W., Farrell, A., and Haswell, M. S. 1981. The evolution of air breathing in vertebrates. Cambridge University Press, New York.CrossRefGoogle Scholar
Reighard, J. 1903. The natural history of Amia calva linnaeus. Pp. 59109In Mark Anniversary Volume. H. Holt, New York.Google Scholar
Roberts, T. R. 1972. Ecology of fishes in the Amazon and Congo basins. Bulletin of the Museum of Comparative Zoology 143:117157.Google Scholar
Robertson, J. I. 1913. The development of the heart and vascular system of Lepidosiren paradoxa. Quarterly Journal of Microscopical Science 59:53132.Google Scholar
Saksena, V. P. 1963. Effects of temperature, light, feeding and activity on the rate of aerial breathing in gar (Lepisosteus). Dissertation Abstracts 24(6):2628. . University of Oklahoma, Norman.Google Scholar
Sanchez-Quintana, D., and Hurle, J. M. 1987. Ventricular myocardial architecture in marine fishes. Anatomical Record 217:263273.CrossRefGoogle ScholarPubMed
Santer, R. M., and Greer Walker, M. 1980. Morphological studies on the ventricle of teleost and elasmobranch hearts. Journal of Zoology, London 190:259272.CrossRefGoogle Scholar
Schrenkeisen, R. 1963. Field book of fresh-water fishes of North America. Putnam, New York.Google Scholar
Secondat, M. 1950. Influence de l'exercice musculaire sur la capacité pour l'oxygène du sang de la carpe (Cyprinus carpio L.). Comptes rendus. Académies des Sciences 230:17871788.Google Scholar
Secondat, M., and Diaz, D. 1942. Recherches sur la lactacidémie chez le poisson d'eau douce. Académies des Sciences 215:7173.Google Scholar
Shelton, G. 1985. Functional and cardiovascular shunts in the amphibia. Pp. 100116In Johansen, K. and Burggren, W., eds. Alfred Benzon Symposium 21: Cardiovascular shunts; phylogenetic, ontogenetic and clinical aspects. Munksgaard, Copenhagen.Google Scholar
Shelton, G., and Burggren, W. 1976. Cardiovascular dynamics of the Chelonia during apnea and lung ventilation. Journal of Experimental Biology 64:323343.Google ScholarPubMed
Shipman, B. 1989. Patterns of ventilation and acid-base recovery following exhausting activity in the air-breathing fish Lepisosteus oculatus. . University of Texas, Arlington.Google Scholar
Shlaifer, A., and Breder, C. M. 1940. Social and respiratory behavior of small tarpon. Zoologica 25:493512.Google Scholar
Sidell, B. D., Driedzic, W. R., Stowe, D. B., and Johnston, I. A. 1987. Biochemical correlations of power development and metabolic fuel preferenda in fish hearts. Physiological Zoology 60:221232.CrossRefGoogle Scholar
Sturkie, P. D. 1986. Avian physiology, 4th ed.Springer, New York.CrossRefGoogle Scholar
Thomson, K. S. 1969a. The biology of the lobe-finned fishes. Biological Reviews 44:91154.CrossRefGoogle Scholar
Thomson, K. S. 1969b. The environment and distribution of Paleozoic sarcopterygian fishes. American Journal of Science 267:457464.CrossRefGoogle Scholar
Thomson, K. S. 1980. The ecology of Devonian lobe-finned fishes. Pp. 187–122 In Panchen, A. L., ed. The terrestrial environment and the origin of land vertebrates. Academic Press, New York.Google Scholar
Tota, B., and Gattuso, A. 1996. Heart ventricle pumps in teleosts and elasmobranchs: a morphodynamic approach. Journal of Experimental Zoology 275:162171.3.0.CO;2-B>CrossRefGoogle Scholar
Tota, B., Cimini, V., Salvatore, G., and Zummo, G. 1983. Comparative study of the ventricular myocardium of elasmobranch and teleost fishes. American Journal of Anatomy 167:1532.CrossRefGoogle ScholarPubMed
Turner, J. D., and Driedzic, W. R. 1980. Mechanical and metabolic response of the perfused isolated fish heart to anoxia and acidosis. Canadian Journal of Zoology 58:886889.CrossRefGoogle Scholar
Turner, J. D., Wood, C. M., and Hobe, H. 1983. Physiological consequences of severe exercise in the inactive benthic flathead sole Hippoglossoides elassodon: a comparison with the active pelagic rainbow trout Salmo gairdneri. Journal of Experimental Biology 104:269288.Google Scholar
Ultsch, G. R. 1996. Gas exchange, hypercarbia and acid-base balance, paleoecology, and the evolutionary transition from water-breathing to air-breathing among vertebrates. Palaeogeography, Palaeoclimatology, Palaeoecology 123:127.CrossRefGoogle Scholar
Vorobyeva, E. 1975. Some peculiarities in evolution of the rhipidistian fishes. In Lehman, J. P., ed. Problèmes actuels de paleontologie. Colloques Internationaux. Centre national de la Recherche scientifique 218:223230.Google Scholar
Walker, W. F., and Liem, K. F. 1994. Functional anatomy of the vertebrates: an evolutionary perspective. Saunders College, Fort Worth, Tex.Google Scholar
Wasser, J. S., Meinertz, E. A., Chang, S. Y., Lawler, R. G., and Jackson, D. C. 1992. Metabolic and cardiodynamic responses of isolated turtle hearts to ischemia and reperfusion. American Journal of Physiology 262:R437R443.Google ScholarPubMed
West, N. H., Butler, P. J., and Bevan, R. M. 1992. Pulmonary blood flow at rest and during swimming in the green turtle, Chelonia mydas. Physiological Zoology 65:287310.CrossRefGoogle Scholar
Wood, C. M., Turner, J. D., and Graham, M. S. 1983. Why do fish die after severe exercise? Journal of Fish Biology 22:189201.CrossRefGoogle Scholar
45
Cited by

Send article to Kindle

To send this article to your Kindle, first ensure no-reply@cambridge.org is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about sending to your Kindle. Find out more about sending to your Kindle.

Note you can select to send to either the @free.kindle.com or @kindle.com variations. ‘@free.kindle.com’ emails are free but can only be sent to your device when it is connected to wi-fi. ‘@kindle.com’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

Find out more about the Kindle Personal Document Service.

Did lungs and the intracardiac shunt evolve to oxygenate the heart in vertebrates?
Available formats
×

Send article to Dropbox

To send this article to your Dropbox account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Dropbox.

Did lungs and the intracardiac shunt evolve to oxygenate the heart in vertebrates?
Available formats
×

Send article to Google Drive

To send this article to your Google Drive account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Google Drive.

Did lungs and the intracardiac shunt evolve to oxygenate the heart in vertebrates?
Available formats
×
×

Reply to: Submit a response

Please enter your response.

Your details

Please enter a valid email address.

Conflicting interests

Do you have any conflicting interests? *