Skip to main content

The dipnoan buccal pump reconstructed in 3D and implications for air breathing in Devonian lungfishes

  • A. M. Clement (a1), J. A. Long (a2), P. Tafforeau (a3) and P. E. Ahlberg (a1)

Lungfishes are known for, and indeed take their name from, their bimodal respiratory abilities. All three extant genera can use their lungs to extract oxygen from the atmosphere, although their reliance upon this capability differs among taxa. Lungs are considered primitive for the Osteichthyes, however the distinctive buccal pump mode of air gulping exhibited by extant lungfishes appears to be a specialization. It is associated with a number of derived skeletal characters (cranial ribs, long parasphenoid stalk, midline gap between palatal tooth plates) that first appeared during the Devonian. These have been described individually, but in no Devonian lungfish has their three-dimensional (3D) spatial relationship been reconstructed and analyzed. Here we present the 3D morphology of Rhinodipterus, a Mid-Late Devonian lungfish from Australia and Europe, based on synchrotron tomography and conventional microtomography scans.

Unlike less crownward contemporaneous lungfishes such as Griphognathus and Chirodipterus, Rhinodipterus has a full set of skeletal buccal pump components that can be directly compared to those of extant lungfishes, suggesting that it made more extensive use of air breathing than other Gogo or Bergisch Gladbach genera. This is interesting in relation to the environmental context as Gogo and Bergisch Gladbach are both marine, contrasting with the frequently hypoxic tropical to subtropical fresh water environments inhabited by modern lungfishes. The evolution of buccal pump-supported lung ventilation was evidently not necessarily associated with a transition to non-marine habitats.

Hide All
Ahlberg, P. E. 1991. A re-examination of sarcopterygian interrelationships, with special reference to Porolepiformes. Zoological Journal of the Linnean Society 103:241287.
Bartsch, P. 1997. Aspects of craniogenesis and evolutionary biology in polypteriform fishes. Netherlands Journal of Zoology 47:365381.
Bemis, W. E. 1986. Feeding systems of living Dipnoi: Anatomy and Function. Journal of Morphology Supplement 1:249275.
Berner, R. A. 2006. GEOCARBSULF: A combined model for Phanerozoic atmospheric O2 and CO2 Geochimica et Cosmochimica Acta 70:56535664.
Berner, R. A. 2009. Phanerozoic atmospheric oxygen: new results using the geocarbsulf model. American Journal of Science 309:603606.
Bishop, I. R., and Foxon, G. E.. 1968. The mechanism of breathing in the South American lungfish, Lepidospiren paradoxa; a radiological study. Journal of Zoology 154:263271.
Brainerd, E. L. 1994. The Evolution of Lung-Gill Bimodal Breathing and the Homology of Vertebrate Respiratory Pumps. American Zoologist 34:289299.
Burggren, W. W., and Johansen, K.. 1986. Circulation and respiration in lungfishes (Dipnoi). Journal of Morphology Supplement 1:217236.
Campbell, K. S. W., and Barwick, R. E.. 1988. Geological and palaeontological information and phylogenetic hypotheses. Geological Magazine 125:207227.
Campbell, K. S. W., and Barwick, R. E.. 1990. Paleozoic dipnoan phylogeny: functional complexes and evolution without parsimony. Paleobiology 16:143169.
Campbell, K. S. W., and Barwick, R. E.. 2000. The braincase, mandible and dental structures of the Early Devonian lungfish Dipnorhynchus kurikae from Wee Jasper, New South Wales. Records of the Australian Museum 52:103128.
Clack, J. A. 2007. Devonian climate change, breathing, and the origin of the tetrapod stem group. Integrative and Comparative Biology 47:510523.
Clement, A. M. 2012. A new species of long-snouted lungfish from the Late Devonian of Australia, and its functional and biogeographical implications. Palaeontology 55:5171.
Clement, A. M., and Ahlberg, P. E.. 2014. The first virtual cranial endocast of a lungfish (Sarcopterygii: Dipnoi). PloS One 9:e113898. doi:10.1371/journal.pone.0113898.
Clement, A. M., and Long, J. A.. 2010. Air-breathing adaptation in a marine Devonian lungfish. Biology Letters 6:509512.
Cloutier, R. 1996. Dipnoi (Akinetia: Sarcopterygii). Pp. 198226in H. P. Schultze, and R. Cloutier, eds. Devonian Fishes and Plants of Miguasha. Quebec, Canada Verlag Dr Friedrich Pfeil, Munich.
Coolidge, E., Hedrick, M. S., and Milsom, W. K.. 2007. Ventilory Systems. Fish Physiology. Elsevier.
Criswell, K. E. 2015. The comparative osteology and phylogenetic relationships of African and South American lungfishes (Sarcopterygii: Dipnoi). Zoological Journal of the Linnean Society 174:801858.
Dahl, T. W., Hammarlund, E. U., Anbar, A. D., Bond, D. P. G., Gill, B. C., Gordon, G. W., Knoll, A. H., Nielsen, A. T., Schovsbo, N. H., and Canfield, D. E.. 2010. Devonian rise in atmospheric oxygen correlated to the radiations of terrestrial plants and large predatory fish. Proceeding of the National Academy of Sciences USA 107:1791117915.
Friedman, M. 2007. The interrelationships of Devonian lungfishes (Sarcopterygii: Dipnoi) as inferred from neurocranial evidence and new data from the genus Soederberghia Lehman, 1959. Zoological Journal of the Linnean Society 151:115171.
Friedman, M. 2010. Postcranial evolution in early lungfishes (Dipnoi: Sarcopterygii): new insights from Soederberghia groenlandica. Pp. 299324in D. K. Elliott, J. G. Maisey, X. Yu, and D. Miao, eds. Morphology, Phylogeny and Paleobiogeography of Fossil Fishes. Verlag Dr. Friedrich Pfeil, Munich.
Friedman, M., and Coates, M. I.. 2005. A newly recognized fossil coelacanth highlights the early morphological diversification of the clade. Proceedings of the Royal Society B 273:245250.
Geiger, S. P., Torres, J. J., and Crabtree, R. E.. 2000. Air breathing and gill ventilation frequencies in juvenile tarpon, Megalops atlanticus: responses to changes in dissolved oxygen, temperature, hydrogen sulfide, and pH. Environmental Biology of Fishes 59:181190.
Goodrich, E. S. 1958. Studies on the structure and development of vertebrates. Dover Publications, New York.
Graham, J. B. 1997. Air-breathing Fishes: Evolution, Diversity and Adaptation. Academic Press, California.
Graham, J. B., Rosenblatt, R. H., and Gans, C.. 1978. Vertebrate air breathing arose in fresh waters and not in the ocean Evolution 32:459463.
Graham, J. B., Wegner, N. C., Miller, L. A., Jew, C. J., Chin Lai, N., Berquist, R. M., Frank, L. R., and Long, J. A.. 2014. Spiracular air breathing in polypterid fishes and its implications for aerial respiration in stem tetrapods. Nature Communications 5:3022. doi:10.1038/ncomms4022.
Grigg, G. C. 1965. Studies on the Queensland Lungfish, Neoceratodus forsteri (Krefft). 3. Aerial respiration in relation to habits. Australian Journal of Zoology 13:413422.
Gross, W. 1956. Über Crossopterygier und Dipnoer aus dem baltischen Oberdevon im Zusammenhang einer vergleichenden Untersuchung des Porenkanalsystems paläozoischer Agnathen und Fische. Almqvist and Wiksell, Stockholm.
Huxley, T. H. 1880. On the applications of the laws of evolution to the arrangement of the Vertebrata and more particularly of the Mammalia. Proceedings of the Zoological Society of London 1888:649662.
Jessen, H. 1973. Weitere fischreste aus dem Oberen Plattenkalk der Bergisch-Gladbach—Paffrather mulde (Oberdevon, Rheinesches Schiefergebirge). Palaeontogr Abt A Palaeozool-Stratigr 143:159187.
Johansen, K., Lenfant, C., and Grigg, G. C.. 1967. Respiratory control in the lungfish Neoceratodus forsteri (Krefft). Comparative Biochemistry and Physiology 20:835854.
Kardong, K. V. 2006. Vertebrates: Comparative Anatomy, Function, Evolution. McGraw Hill, New York.
Krupina, N. I. 1995. New species of Rhinodipterus (Dipnoi) from the Upper Devonian of north western Russia. Geobios 28(Suppl. 2): 269274.
Liem, K. F. 1988. Form and function of lungs: the evolution of air breathing mechanisms. American Zoologist 28:739759.
Long, J. A. 1993. Cranial ribs in Devonian lungfishes and the origin of dipnoan air-breathing. Memoirs of the Association of Australasian Palaeontologists 15:199209.
Long, J. A. 2010. New holodontid lungfishes from the Late Devonian Gogo Formation of Western Australia. Pp. 275298in D. K. Elliott, J. G. Maisey, X. Yu, and D. Miao, eds. Fossil fishes and related Biota: Morphology, Phylogeny and Paleobiogeography. D. Verlag Pfeil, München.
Long, J. A., and Clement, A. M.. 2009. The postcranial anatomy of two Middle Devonian lungfishes (Osteichthyes, Dipnoi) from Mt. Howitt, Victoria, Australia. Memoirs of Museum Victoria 66:189202.
Longo, S., Riccio, M., and McCune, A. R.. 2013. Homology of Lungs and Gas Bladders: Insights from Arterial Vasculature. Journal of Morphology 274:687703.
McMahon, B. E. 1969. A functional analysis of the aquatic and aerial respiratory movements of an African lungfish, Protopterus aethiopicus. Journal of Experimental Biology 51:407430.
Melendez, I., Grice, K., Trinajstic, K., Ladjavardi, M., Greenwood, P., and Thompson, K.. 2013. Biomarkers reveal the role of photic zone euxinia in exceptional fossil preservation: An organic geochemical perspective. Geology 41:123126.
Miles, R. S. 1977. Dipnoan (lungfish) skulls and the relationships of the group: a study based on new species from the Devonian of Australia. Zoological Journal of the Linnean Society 61:1328.
Millot, J., and Anthony, J.. 1958. Anatomie de Latimeria chalumnae, I - Squelette, Muscles, et Formation de Soutiens. CNRS, Paris 3:122.
Müller, J. 1844. Uber den Bau und die Grenzen der Ganoiden, and uber das naturliche System der Fische. Abhandlungen der Koniglichen Akademie der Wissenschaften zu Berlin. 1844:117216.
Niedźwiedzki, G., Szrek, P., Narkiewicz, K., Narkiewicz, M., and Ahlberg, P. E.. 2010. Tetrapod trackways from the early Middle Devonian period of Poland. Nature 463:4348.
Ørvig, T. 1961. New finds of acanthodians, arthrodires, crossopterygians, ganoids and dipnoans in the upper Middle Devonian calcareous flags (Oberer Plattenkalk) of the Bergisch Gladbach-Paffrath trough. Palaontologische Zeitschrift 35:1027.
Pardo, J. D., Huttenlocker, A. K., and Small, B. J.. 2014. An exceptionally preserved transitional lungfish from the Lower Permian of Nebraska, USA, and the origin of modern lungfishes. PloS One 9:e108542. doi:10.1371/journal.pone.0108542.
Perry, S. F., Wilson, R. J. A., Straus, C., Harris, M. B., and Remmers, J. E.. 2001. Which came first, the lung or the breath? Comparative Biochemistry and Physiology Part A 129:3747.
Playford, P. E. 1980. Devonian ‘great barrier reef’ of Canning Basin, Western Australia. Bulletin of the American Association of Petroleum Geologists 64:814840.
Playford, P. E., Hocking, M. R., and Cockbain, A. E.. 2009. Devonian reef complexes of the Canning Basin, Western Australia. Geological Survey of Western Australia 145:444.
Qiao, T., and Zhu, M.. 2009. A new tooth-plated lungfish from the Middle Devonian of Yunnan, China, and its phylogenetic relationships. Acta Zoologica 90(Suppl. 1):236252.
Romer, A. S. 1955. Herpetichthyes, Amphibioidei, Choanichthyes or Sarcopterygii? Nature 176:126127.
Ronquist, F., Teslenko, M., van der Mark, P., Ayres, D. L., Darling, A., Höhna, S., Larget, B., Liu, L., Suchard, M. A., and Huelsenbeck, J. P.. 2012. MrBayes 3.2: Efficient Bayesian Phylogenetic Inference and Model Choice Across a Large Model Space. Software for Systematics and Evolution 61:539542.
Sakellariou, A., Sawkins, T. J., Limaye, A., and Senden, T. J.. 2004. X-ray tomography for mesoscale physics. Physica A-statistical mechanics and its applications 339:152158.
Sanchez, S., Fernandez, V., Pierce, S. E., and Tafforeau, P.. 2013. Homogenization of sample absorption for the imaging of large and dense fossils with synchrotron microtomography. Nat Protoc 8:17081717.
Schultze, H.-P. 1975. Das axialskelett der Dipnoer aus dem Overdevon von Bergisch-Gladbach (westdeutschland). Colloques int. Cent. natn. Res. scient. 218:149159.
Swofford, D. L. 2001. PAUP* Phylogenetic Analysis Using Parsimony (*and Other Methods). Version 4. Sinauer Associates, Sunderland, Massachusetts.
Thomson, K. S. 1969. The biology of the lobe-finned fishes. Biological Reviews 44:91154.
White, E. 1962. A dipnoan from the Assise de Mazy of Hingeon. Bulletin Institut Royal des Sciences Naturelles de Belgique 38:18.
Recommend this journal

Email your librarian or administrator to recommend adding this journal to your organisation's collection.

  • ISSN: 0094-8373
  • EISSN: 1938-5331
  • URL: /core/journals/paleobiology
Please enter your name
Please enter a valid email address
Who would you like to send this to? *