Thanks to visit codestin.com
Credit goes to link.springer.com

Skip to main content
Springer Nature Link
Log in

Physiological Evidence Indicates Lungfish as a Sister Group to the Land Vertebrates

  • Chapter
  • First Online:
Cardio-Respiratory Control in Vertebrates

  • 1230 Accesses

  • 3 Citations

Abstract

Abstract Current research tends to support that lungfish (Dipnoi) and land vertebrates (Tetrapoda) form a sister group, which has stimulated an interest in these animals. The extant lungfish include: Protopterus, the African lungfish (four species) and the South American lungfish (Lepidosiren paradoxa) (one species). The African and South American lungfish have well-developed lung and reduced gills, while the Australian lungfish (Neoceratodus forsteri) is highly dependent on the gill ventilation, and its lung is one of the simplest among vertebrates. Lungfish and land vertebrates share many features of respiratory control. Lepidosiren (and probably Protopterus possess central cerebral CO2 and H+ receptors, which regulate acid–base by increases or decreases in pulmonary ventilation. This regulatory pattern is also valid for land vertebrates, including human beings. By contrast, teleost fish lack central CO2/H+-receptors, which suggests that the lung and the central chemoreceptors evolved together. In this context, any very specific features are common to lungfish and land vertebrates, and these include the Hering–Breuer reflex and the presence of very specific stretch receptors.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution

Subscribe and save

Springer+
from £29.99 /Month
  • Starting from 10 chapters or articles per month
  • Access and download chapters and articles from more than 300k books and 2,500 journals
  • Cancel anytime
View plans

Buy Now

Chapter
GBP 19.95
Price includes VAT (United Kingdom)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
GBP 143.50
Price includes VAT (United Kingdom)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
GBP 179.99
Price includes VAT (United Kingdom)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
GBP 179.99
Price includes VAT (United Kingdom)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Similar content being viewed by others

Explore related subjects

Discover the latest articles, books and news in related subjects, suggested using machine learning.

References

  • Abe AS (1995) Estivation in South American amphibians and reptiles. Brazilian Journal of Medical and Biological Research 28:1241-1247

    PubMed  CAS  Google Scholar 

  • Amin-Naves J, Giusti H, Glass ML (2004) Effects of acute temperature changes on aerial and aquatic gas exchange, pulmonary ventilation and blood gas status in the South American lungfish, Lepidosiren paradoxa. Comparative Biochemistry and Physiology A 138:133-139

    Article  CAS  Google Scholar 

  • Amin-Naves J, Sanchez AP, Bassi M, Giusti H, Rantin FT, Glass ML (2007a) Blood gases of the South American lungfish Lepidosiren paradoxa: a comparison to other air-breathing fish and to amphibians. In: Fernandes MN, Rantin FT, Glass ML, Kapoor BG (eds) Fish Respiration and Environment. Science, Enfield, NH, USA, pp 243-252

    Chapter  Google Scholar 

  • Amin-Naves J, Giusti H, Hoffman A, Glass ML (2007b) Components to the acid-base related ventilatory drives in the South American lungfish Lepidosiren paradoxa. Respiratory Physiology and Neurobiology 155(1):35-40

    Article  CAS  Google Scholar 

  • Amin-Naves J, Giusti H, Hoffman A, Glass ML (2007c) Central ventilatory control in the South American lungfish, Lepidosiren paradoxa: contributions of pH and CO2. Journal of Comparative Physiology B 177:529-534

    Article  CAS  Google Scholar 

  • Andrade DV, Simone PB, Toledo LF, Abe AS (2004) Seasonal changes in blood oxygen transport and acid-base status in the tegu lizard, T upinambis merianae. Respiratory Physiology and Neurobiology 140:197-208

    Article  PubMed  CAS  Google Scholar 

  • Bassi M, Klein W, Fernandes MN, Perry SF, Glass ML (2005) Pulmonary oxygen diffusing capacity of the South American lungfish Lepidosiren paradoxa: physiological values by the Bohr integration method. Physiological and Biochemical Zoology 78(4):560-569

    Article  PubMed  CAS  Google Scholar 

  • Bernard DG, Li A, Nattie EE (1996) Evidence for central chemoreceptors in the midline raphe. Journal of Applied Physiology 80(1):108-115

    PubMed  CAS  Google Scholar 

  • Bohr C (1909) Über die spezifische Tätigkeit der Lungen bei der respiratorischen Gasaufnahme und ihr Verhalten zu der durch die Alveolenwand stattfindende Gasdiffusion. Skandinavisches Archiv für Physiologie 22:221-280

    Google Scholar 

  • Branco LGS, Glass ML (1995) Ventilatory responses to carboxihaemoglobinaemia and hypoxic hypoxia in Bufo paracnemis. Jounal of Experimental Biology 198 (6):1417-1421

    CAS  Google Scholar 

  • Branco LG, Wood SC (1993) Effect of temperature on central chemical control of ventilation in the alligator Alligator mississippiensis. Jounal of Experimental Biology 179:261-272

    CAS  Google Scholar 

  • Branco LGS, Glass ML, Wang T, Hoffmann A (1993) Temperature and central chemoreceptor drive to ventilation in toad (Bufo paracnemis). Respiration Physiology 93:337-346

    Article  PubMed  CAS  Google Scholar 

  • Brinkmann H, Denk A, Zitzle J, Joss JMP, Meyer A (2004) Complete mitochondrial genome sequence of the South American and the Australian lungfish: testing of the phylogenetic performance of mitochondrial data sets for phylogenetic problems in tetrapod relationships. Journal of Molecular Evolution 59:834-848

    Article  PubMed  CAS  Google Scholar 

  • Burleson ML, Milsom WK (1995a) Cardio-ventilatory control in rainbow trout: I. Pharmacology of branchial oxygen-sensitive chemoreceptors. Respiration Physiology 100:231-238

    Article  CAS  Google Scholar 

  • Burleson ML, Milsom WK (1995b) Cardio-ventilatory control in rainbow trout: II. Reflex effects of exogenous neurochemicals. Respiration physiology 101:289-299

    Article  CAS  Google Scholar 

  • Carroll RL (1988) Vertebrate Palaeontology and Evolution, 1st edn. Freeman and Company, New York

    Google Scholar 

  • Claiborne JB Jr, Heisler N (1986) Acid-base regulation and ion transfers in the carp (Cyprinus carpio): pH compensation during graded long- and short-term environmental hypercapnia, and the effect of bicarbonate infusion. Journal of Experimental Biology 126:41-61

    PubMed  CAS  Google Scholar 

  • Crawford EC Jr, Gatz RN, Magnussen H, Perry SF, Piiper J (1976) Lung volumes, pulmonary blood flow, and carbon monoxide diffusing capacity of turtles. Journal of Comparative Physiology 107:169-178

    Google Scholar 

  • Daniels CB, Orgeig S (2003) Pulmonary surfactant: the key to evolution. New Physiological Science 18:151-159

    CAS  Google Scholar 

  • Dejours P (1981) Principles of Comparative Respiratory Physiology, 2nd edn. Elsevier, Amsterdam

    Google Scholar 

  • DeLaney RG, Lahiri S, Fishman AP (1974) Aestivation of the African lungfish Proptopterus aethiopicus: cardiovascular and pulmonary function. Journal of Experimental Physiology 6:111-128

    Google Scholar 

  • DeLaney RG, Lahiri S, Hamilton R, Fishman AP (1977) Acid-base balance and plasma composition in the aestivating lungfish (Protopterus). American Journal of Physiology 232(1):R10-R17

    PubMed  CAS  Google Scholar 

  • Delaney RG, Laurent P, Galante R, Pack AI, Fishman AP (1983) Pulmonary mecanoreceptors in the dipnoi lungfish Protopterus and Lepidosiren. American Journal of Physiology 244:R418-R428

    PubMed  CAS  Google Scholar 

  • Fitziger LJ (1837) Vorläufiger Bericht über eine höchst interessante Entdeckung Dr. Natterers in Brasilien. Isis 1837:379-380

    Google Scholar 

  • Foxon GEH, Bishop IR (1968) The mechanism of breathing in the in the South American lungfish (Lepidosiren paradoxa); radiological study. Journal of Zoology (London) 154:26-272

    Google Scholar 

  • Fritsche R, Axelsson M, Franklin CE, Grigg GC, Holmgren S, Nilsson S (1993) Physiology 142B:509-514

    Google Scholar 

  • Gilmour KM, Euverman, Esbaugh RM, Kenney AJ, Chew LSF, Ip YK, Perry SF (2007) Mechanisms of acid-base regulation in the African lungfish Protopterus annectens. Jounal of Experimental Biology 210:1944-1959

    Article  CAS  Google Scholar 

  • Glass, ML, Johansen K (1982) Pulmonary oxygen capacity of lizard Tupinambis teguixin. Journal of Experimental Zoology 219:385-388

    Article  Google Scholar 

  • Glass ML, Burggren WW, Johansen K (1981a) Pulmonary diffusing capacity of the bullfrog (Rana catesbeiana). Acta Physiologica Scandinavica 113:485-490

    Article  CAS  Google Scholar 

  • Glass ML, Johansen K, Abe AS (1981b) Pulmonary diffusing capacity in reptiles (relations to temperature and O2-uptake). Journal of Comparative Physiology 142B:509-514

    Google Scholar 

  • Glass ML, Fernandes MS, Soncini R, Glass H, Wasser JS (1997) Effects of dry season dormancy on oxygen uptake, heart rate, and blood pressures in the toad Bufo paracnemis. Journal of Experimental Zoology 279:330-336

    Article  PubMed  CAS  Google Scholar 

  • Greenwood PH (1986) The natural history of African lungfishes. Journal of Morphological Supplement 1:163-179

    Google Scholar 

  • Guyenet PG, Stornette RL, Baylis DA, Mulkey DK (2005) Retropezoid nucleus: a litmus test for the identification of central respiratory and cardiovascular responses to hypoxia in the Australian lungfish. Respiration Physiology 94:173-187

    Google Scholar 

  • Harada Y, Wang YZ, Kuno M. (1985) Central chemosensitivity to H+ and CO2 in respiratory center in vitro. Brain Research 333(2):336-339

    Article  PubMed  CAS  Google Scholar 

  • Heisler N (1984) Acid-base regulation in fishes. In: Hoar WS, Randall DJ (eds) Physiology, vol. XA. Academic, Orlando, pp 315-401

    Google Scholar 

  • Heisler N, Forcht, Ultsch GR, Anderson JF (1982) Acid-base regulation to environmental hypercapnia in two aquatic salamanders, Siren lacertina and Amphiuma means. Respiration Physiology 49:141-158

    Article  PubMed  CAS  Google Scholar 

  • Hlastala MP, Berger AJ (1996) Physiology of Respiration. Oxford University Press, New York

    Google Scholar 

  • Johansen K, Lenfant C (1967) Respiratory function in the South American lungfish, Lepidosiren paradoxa. Journal of Experimental Biology 46:305-218

    Google Scholar 

  • Johansen K, Lenfant C (1968) Respiration in the African Lungfish Protopterus aethiopicus : II Control of breathing. Journal of Experimental Biology49453-468

    CAS  Google Scholar 

  • Johansen K, Lenfant C Grigg GC (1967) respiratory control in the lungfish Neoceratodus forsteri Krefft).Comparative Biochemistry20:835-854

    Google Scholar 

  • Joss J, Johanson Z, (2007) Is Palaeospondylus gunni a fossil larval lungfish? Insights from Neoceratodus forsteri development. Journal of experimental zoology. Part B. Molecular and Developmental Evolution 308B:163-171

    Article  Google Scholar 

  • Kind PK, Grigg GC, Booth DT (2002) Physiological responses to prolonged aquatic hypoxia in the Queensland lungfish. Neoceratodus forsteri.Respiratory Physiology and Neurology132:179-190

    Article  Google Scholar 

  • Lahiri S, Szidon JP, Fishman AP (1970) Potential respiratory and circulatory adjustments to hypoxia in the African lungfish. Federation Proceedings 29(No2):1141-1148

    PubMed  CAS  Google Scholar 

  • Lenfant C, Johansen K, Grigg GC (1966/1967) Respiratory proporties of blood and pattern of gas exchange in the lungfish Neoceratodus forsteri (Krefft). Respiration Physiology 2:1-21

    Article  Google Scholar 

  • Loeschcke HH, Koepchen HP, Gertz KH, (1958) Über den Einfluss von Wasserstoffionenkonzentration und CO2-Druck im Liquor cerebrospinalis auf die Atmung. Pflügers Archiv 266:569-585

    Article  PubMed  CAS  Google Scholar 

  • Lomholt JP (1993) Breathing in the aestivating African Lungfish, Protopterus amphibius.Advances in Fish Research1:17-34

    Google Scholar 

  • McMahon BR (1969) A functional analysis of the aquatic and aerial respiratory movement of an African lungfish, with reference to the evolution of the lung ventilation mechanism in vertebrates. Journal of Experimental Biology 51:407-430

    PubMed  CAS  Google Scholar 

  • Metcalf VJ, George PM, Brennan SO (2007) Lungfish albumin is more similar to tetrapod than to teleost albumins: purification and characterisation of albumin from the Australian lungfish, Neoceratodus forsteri. Comparative Biochemistry and Physiology B Biochemistry and Molecular Biology 147(3):428-437

    Article  Google Scholar 

  • Meyer A, Dolven SI (1992) Molecules, fossils, and the origin of tetrapods. Journal of Molecular Evolution 35:102-113

    Article  PubMed  CAS  Google Scholar 

  • Milsom WK (1995) The role of CO2/pH chemoreceptors in ventilatory control. Brazilian Journal of Medical and Biological Research 28:1147-1160

    PubMed  CAS  Google Scholar 

  • Milsom WK (2002) Phylogeny of CO2/H+ chemoreception in vertebrates. Respiratory Physiology and Neurobiology 131:29-41

    Article  PubMed  CAS  Google Scholar 

  • Milsom WK, Jones DR, Gabbott GR. (1981) On chemoreceptor control of ventilatory responses to CO2 in unanesthetized ducks Journal of Applied Physiology 50(6):1121-1128

    PubMed  CAS  Google Scholar 

  • Milsom WK, Abe AS, Andrade DV, Tattersall GJ (2004) Evolutionary trends in airway CO2/H+ chemoreception. Respiratory Physiology and Neurobiology 144(2-3):191-202

    Article  PubMed  CAS  Google Scholar 

  • Moraes MFPG, Fernandes MN, Höller S, Costa OPF, Glass ML, Perry SF. (2005) Morphometric comparison of the respiratory organs of the South American lungfish Lepidosiren paradoxa (Dipnoi). Physiological and Biochemical Zoology 78:546-559

    Article  PubMed  Google Scholar 

  • Nattie E (1999) CO2 brainstem chemoreceptors and breathing. Progress in Neurobiology 59:299-331

    Article  PubMed  CAS  Google Scholar 

  • Nattie E (2006) Why do we have both peripheral and central chemoreceptors? Journal of Applied Physiology 100(1):9-0

    Article  PubMed  Google Scholar 

  • Orgeig S, Daniels CB (1995) The evolutionary significance of pulmonary surfactant in lungfish (Dipnoi). American Journal of Respiratory Cell and Molecular Biology 13:161-166

    PubMed  CAS  Google Scholar 

  • Pack AJ, Galante RJ, Fishman AP (1990) Control of the interbreath interval in the African lungfish. American of Journal Physiology 259:R139-R146

    CAS  Google Scholar 

  • Pack AJ, Galante RJ, Fishman AP (1992) Role of lung inflation in control of air breath duration in African lungfish (Protopterus annectens). American of Journal Physiology 262:R879-884

    CAS  Google Scholar 

  • Perry SF (2007) Swimbladder-lung homology in basal osteichthyes revisited. In: Fernandes MN, Rantin FT, Glass ML, Kapoor BG (eds) Fish Respiration and the Environment. Science Publishers, Enfield NH, pp 41-55

    Chapter  Google Scholar 

  • Perry SF, Euverman R, Wang T, Loong AM, Chew SF, Ip YK, Gilmour KM (2007) Control of breathing in African lungfish (Protopterus dolloi): a comparison of aquatic and cocooned (terrestrialized) animals. Respiratory Physiology & Neurobiology 160(1):8-17

    Article  Google Scholar 

  • Power JH, Doyle IR, Davidson K, Nicholas TE (1999) Ultrastructural and protein analysis of surfactant in the Australian lungfish Neoceratodus forsteri: evidence for conservation of composition for 300 million years. Journal of Experimental Biology 202(Pt 18):2543-2550

    PubMed  CAS  Google Scholar 

  • Rantin FT, Kalinin AL, Glass ML (2007) The effects of temperature on respiratory and cardiac function of teleost fish. In: Fernandes MN, Rantin FT, Glass ML (eds) Fish Respiration and the Environment. Science Publishers, China

    Google Scholar 

  • Sanchez AP, Glass ML (2001) Effects of environmental hypercapnia on pulmonary ventilation of the South American lungfish. Journal of Fish Biology 58:1181-1189

    Article  Google Scholar 

  • Sanchez AP, Hoffman A, Rantin FT, Glass ML (2001a) The relationship between pH of the cerebro-spinal fluid and pulmonary ventilation of the South American lungfish, Lepidosiren paradoxa. Journal of Experimental Zoology 290:421-425

    Article  CAS  Google Scholar 

  • Sanchez AP, Soncini R, Wang T, Koldkjaer P, Taylor EW, Glass ML (2001b) The differential cardio-respiratory responses to ambient hypoxia and systemic hypoxaemia in the South American lungfish, Lepidosiren paradoxa. Comparative Biochemistry and Physiology A 130:677-687

    Article  CAS  Google Scholar 

  • Sanchez AP, Giusti H, Bassi M, Glass ML (2005) Acid-base regulation in the South American lungfish, Lepidosiren paradoxa: effects of prolonged hypercarbia on blood gases and pulmonary ventilation. Biochemical and Physiological Zoology 78:908-915

    Article  CAS  Google Scholar 

  • Sawaya P (1946) Sobre a biologia de alguns peixes de respiração aérea (Lepidosiren paradoxa Fitzinger e Arapaima gigas Cuvier). Boletim da Faculdade de Filosofia Ciências e Letras da Universidade de São Paulo 11:255-286

    Google Scholar 

  • Schläfke ME, Pokorski M, See WR, Prill RK, Loeschcke HH (1975) Chemosensitive neurons on the ventral medullary surface. Bulletin de physio-pathologie respiratoire (Nancy) 11(2):277-84

    Google Scholar 

  • Shams H (1985) Differential effects of CO2 and H+ as central stimuli of respiration in the cat. Journal Applied Physiology 58(2):357-64

    CAS  Google Scholar 

  • Shams H, Scheid P (1989) Efficiency of parabronchial gas exchange in deep hypoxia: measurements in the resting duck. Respiration Physiology 77:135-146

    Article  PubMed  CAS  Google Scholar 

  • Smatresk NJ, Azizi SQ (1987) Characteristics of lung mechanoreceptors in the spotted gar, Lepisosteus oculatus. American Journal of Physiology 252:R1066-R1072

    PubMed  CAS  Google Scholar 

  • Smith HW (1930) Metabolism of the lungfish, Protopterus aethiopicusJournal of Biological Chemistry88:164-181

    Google Scholar 

  • Smith HM (1935) The metabolism of a lungfish. I. General considerations of the fasting metabolism in an active fish. Journal of Cellular Comparative Physiology 6:43-67

    CAS  Google Scholar 

  • Smith CA, Rodman JR, Chenuel BJA, Henderson KS, Dempsey JA (2006) Response time and sensitivity of the ventilatory response to CO2 in unanesthetized intact dogs: central vs peripheral chemoreceptors. Journal of Applied Physiology 100:13-19

    Article  PubMed  CAS  Google Scholar 

  • Soncini R, Glass ML (2000) Oxygen- and acid-base-related drives to gill ventilation in carp. Journal of Fish Biology 56:528-541

    Article  Google Scholar 

  • Striedter GF (2005) Principles of Brain Evolution. Sinauer, Sunderland, USA

    Google Scholar 

  • Takezawa J, Miller FJ, O’Neil JJ (1980) Single-breath diffusing capacity and lung volumes in small laboratory mammals. Journal of Applied Physiology 48(6):1052-1059

    PubMed  CAS  Google Scholar 

  • Toyama Y, Ichimiya T, Kasama-Yoshida H, Cao Y, Hasegava M, Kojima H, Tamai Y, Kurihari T (2000) Phylogenertic relation of lungfish indicated by the amino acid sequence of myelin DM20. Molecular Brain Research 8:256-259

    Article  Google Scholar 

  • Vidal N, Azvolinsky A, Cruaud C, Hedges SB (2007) Origin of tropical American burrowing reptiles by transatlantic rafting. Biological letters 2007 Dec 11 [Epub ahead of print]

    Google Scholar 

  • Wang T, Branco LGS, Glass ML (1994) Ventilatory responses to hypoxia in the toad (Bufo paracnemis Lutz) before and after reduction of HbO2 concentration. Journal of Experimental Biology 186:1-8

    PubMed  CAS  Google Scholar 

  • Wang T, Abe AS, Glass ML (1998) Temperature effects on lung and blood gases in the toad Bufo paracnemis: the consequences of bimodal gas exchange. Respiration Physiology 113:231-238

    Article  PubMed  CAS  Google Scholar 

  • Watt M, Evans CS, Joss JM (1999) Use of electroreception during foraging by the Australian lungfish. Animal Behavior 58:1039-1045

    Article  Google Scholar 

  • Yokabori S, Hasegawa M, Ueda T, Okada N, Nishikawa K, Watanabe K (1994) Relationships among coelacanths, lungfishes, and tetrapods: a phylogenetic analysis based on mitochondrial cytochrome oxidase i gene sequences. Journal of Molecular Evolution 38:602-609

    Google Scholar 

  • Zardoya R, Cao Y, Hasegava M, Meyer A (1998) Searching for the closest living relative(s) of Tetrapods through evolutionary analyses of mitochondrial and nuclear data. Journal of Molecular Biology and Evolution 15:506-517

    CAS  Google Scholar 

  • Zhu M, Yu X (2002) A primitive fish close to the common ancestor of tetrapods and lungfish. Nature 418:767-770

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

This research was supported by FAPESP (Fundação de Amparo á Pesquisa do Estado de São Paulo); Proc 98/06731-5, CNPq (Conselho Nacional de Desenvolvimento Científico o Tecnológico; Proc. 520769/93-7, FAEPA (Fundação de Apoio ao Ensino, Pesquisa e Assistência do Hospital das Clínicas da FMRP-USP).

Author information

Authors and Affiliations

  1. Department of Physiology, Faculty of Medicine of Ribeirão Preto, University of São Paulo, 14.049-900, Avenida Bandeirantes 3900, Ribeirão Preto, SP, Brazil

    M. L. Glass

Authors
  1. M. L. Glass
    View author publications

    Search author on:PubMed Google Scholar

Corresponding author

Correspondence to M. L. Glass .

Editor information

Editors and Affiliations

  1. Fac. Medicina, Universidade de São Paulo, Avenida Bandeirantes 3900, Ribeirao Preto, 14040-901, Brazil

    Mogens L. Glass

  2. School of Medicine, University of New Mexico, Albuquerque, 87131, U.S.A.

    Stephen C. Wood

Rights and permissions

Reprints and permissions

Copyright information

© 2009 Springer-Verlag Berlin Heidelberg

About this chapter

Cite this chapter

Glass, M.L. (2009). Physiological Evidence Indicates Lungfish as a Sister Group to the Land Vertebrates. In: Glass, M., Wood, S. (eds) Cardio-Respiratory Control in Vertebrates. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-540-93985-6_7

Download citation

Keywords

These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Publish with us

Policies and ethics