Reviews in Fish Biology and Fisheries

, Volume 2, Issue 3, pp 187–216 | Cite as

Gill surface area of water-breathing freshwater fish

  • Margit Palzenberger
  • Hannes Pohla
Article

Summary

To provide a hitherto lacking review which focuses on gill surface area of freshwater fish, we collected and analysed morphometric data from the literature. The scaling exponent of gill area ranges from 0.36 to 1.13, with a mean value of 0.76. The absolute values for the largest gill areas are about 5 times as high as those of the smallest. This range resembles that of marine fish, if specially adapted steady swimmers, such as tunnies and some sharks, are excluded. Generally it appears that the gill areas of freshwater fish are smaller than those of comparable marine species. To establish whether a relationship exists between gill area and swimming activity or oxygen content of water, the activity of each species and the oxygen content of its habitat were estimated and checked against the gill area. ANOVA revealed that activity explains the presence of the smallest gill areas only, while oxygen content does not correlate with gill area at all. The morphometric variables determining gill area (total length of filaments, average lamellar density, average lamellar area) are highly correlated; total gill area correlates mainly with lamellar density and to a lesser degree with filament length; lamellar area varies independently. Different populations of the same species exhibit striking differences with respect to gill areas, total length of filaments, average lamellar density and average lamellar area. These differences point to a substantial morphological plasticity of the gill system.

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References

  1. Al-Kadhomiy, N.K. (1985) Gill development, growth, and respiration of the flounderPlatichthys flesus L. PhD thesis, Bristol University (not seen in original).Google Scholar
  2. Byczkowska-Smyk, W. (1957) The respiratory surface of the gills in teleosts. Part I. The respiratory surface of the gills in the flounder (Pleuronectes platessa) and the perch (Perca fluviatilis).Zool. Polon. 3, 91–111.Google Scholar
  3. Byczkowska-Smyk, W. (1958) The respiratory surface of the gills in teleosts. Part II. The respiratory surface of the gills in the eel (Anguilla anguilla L.), the loach (Misgurnus fossilis L.) and the perch-pike (Lucioperca lucioperca L.)Acta biol. cracov. 1, 83–97.Google Scholar
  4. Byczkowska-Smyk, W. (1959a) The respiratory surface of the gills in teleots. Part III. The respiratory surface of the gills in the tench (Tinca tinca L.), the silver bream (Blicca bjoerkna L.) and the chondrostoma (Chondrostoma nasus L.).Acta biol. cracov. 2, 73–88.Google Scholar
  5. Byczkowska-Smyk, W. (1959b) The respiratory surface of the gills of teleosts: Part IV. The respiratory surface of the gills in the pike (Esox lucius L.), stone-perch (Acerina cernua L.), and the burbot (Lota lota L.).Acta biol. caacov. (Ser. zool.) 2, 113–27.Google Scholar
  6. Byczkowska-Smyk, W. (1962) Vascularization and size of the respiratory surface of gills inAcipenser stellatus Pall.Acta biol. cracov. 5, 303–16.Google Scholar
  7. De, Jager, S and Dekkers, W.J. (1975) Relation between gill structure and activity in fish.Neth. J. Zool. 25, 276–308.Google Scholar
  8. De, Jager, S., Smit-Onel, M.E., Videler, J.J., Van-Gills, B.J.M. and Uffink, E.M. (1977) The respiratory area of the gills of some teleost fishes in relation to their mode of life.Bijdr. Dierk. 46, 199–205.Google Scholar
  9. Dunel, S. and Laurent, P. (1980) Functional organisation of the gill vasculature in different classes of fish. In Lahlou, B., ed.Epithelial Transport in the Lower Vertebrates. Cambridge: University Press, pp. 37–58.Google Scholar
  10. Emery, S.H. and Szcepanski, A. (1986) Gill dimensions in pelagic elasmobranch fishes.Biol. Bull. mar. biol. lab., Woods Hole 171, 441–9.Google Scholar
  11. Galis, F. and Barel, C.D.N. (1980) Comparative functional morphology of the gills of African lacustrine Cichlidae (Pisces, Teleostei). An ecomorphological approach.Neth. J. Zool. 30, 392–430.Google Scholar
  12. Gray, I.E. (1954) Comparative study of the gill area of marine fishes.Biol. Bull. mar. biol. lab., Woods Hole 107, 219–55.Google Scholar
  13. Hakim, A., Munshi, J.S.D. and Hughes, G.M. (1978) Morphometrics of the respiratory organs of the Indian green snake-headed fish,Channa punctata.J. Zool., Lond. 184, 519–43.Google Scholar
  14. Hughes, G.M. (1966) The dimension of fish gills in relation to their function.J. exp. Biol. 45, 177–95.Google Scholar
  15. Hughes, G.M. (1970) Morphological measurements on the gills of fishes in relation to their respiratory function.Folia morph. 28, 78–95.Google Scholar
  16. Hughes, G.M. (1972) Morphometrics of fish gills.Respir. Physiol. 14, 1–25.Google Scholar
  17. Hughes, G.M. (1976) On the respiration ofLatimeria chalumnae.Zool. J. Linn. Soc. 59, 195–208.Google Scholar
  18. Hughes, G.M. (1978) On the respiration ofTorpedo marmorata.J. exp. Biol. 73, 85–105.Google Scholar
  19. Hughes, G.M. (1980) Morphometry of fish gas exchange organs in relation to their respiratory function. In Ali, M.A., ed..Environmental Physiology of Fishes. New York: Plenum Press, pp. 33–56.Google Scholar
  20. Hughes, G.M. (1982) An introduction to the study of gills. In Houlihan, D.F., Rankin, J.C. and Shuttleworth, T.H., eds.Gills. Cambridge: Cambridge Univ. Press, pp. 1–24.Google Scholar
  21. Hughes, G.M. (1984a) Measurement of gill area in fishes: practices and problems.J. mar. biol. Ass. U.K. 64, 637–55.Google Scholar
  22. Hughes, G.M. (1984b) Scaling of respiratory areas in relation to oxygen consumption of vertebrates.Experientia 40, 519–652.Google Scholar
  23. Hughes, G.M. (1984c) General anatomy of the gills. In Hoar, W.S. and Randall, D.J., eds.Fish Physiology, Vol. 10A,Gills, London: Academic Press, pp. 1–72.Google Scholar
  24. Hughes, G.M. (1990) On different methods available for measuring the area of gill lamellae of fishes.J. mar. biol. Ass. U.K. 70, 13–19.Google Scholar
  25. Hughes, G.M. and Al-Kadhomiy, N.K. (1986) Gill morphometry of the mudskipper,Boleophthalmus boddarti,J. mar. biol. Ass. U.K. 66, 671–82.Google Scholar
  26. Hughes, G.M. and Gray, I.E. (1972) Dimensions and ultrastructure of toadfish gills.Biol. Bull. mar. biol. lab., Woods Hole 143, 150–61.Google Scholar
  27. Hughes, G.M. and Iwai, T. (1978) A morphometric study of the gills in some Pacific deep-sea fishes.J. Zool., Lond. 184, 155–70.Google Scholar
  28. Hughes, G.M. and Morgan, M. (1973) The structure of fish gills in relation to their respiratory function.Biol. Rev. 48, 419–75.Google Scholar
  29. Hughes, G.M. and Ojha, J. (1986) Critical study of the gill area of a free-swimming river carp,Catla catla and an air-breathing perch,Anabas testudineus,Proc. Indian natn. Sci. Acad. 51B, 391–404.Google Scholar
  30. Hughes, G.M. and Wright, D.E. (1970) A comparative study of the water-blood pathways in the secondary lamellae of teleost and elasmobranch fishes-benthic forms.Z. Zellforsch. 104, 478–83.Google Scholar
  31. Hughes, G.M., Dube, S.C. and Munshi, J.S.D. (1973) Surface area of the respiratory organs of the climbing perchAnabas testudineus (Pisces: Anabantidae).J. Zool., Lond. 170, 227–43.Google Scholar
  32. Hughes, G.M., Perry, S.F. and Piiper, J. (1986) Morphometry of the gills of the elasmobranchScyliorhinus stellaris in relation to body size.J. exp. Biol. 121, 27–42.Google Scholar
  33. Hughes, G.M., Singh, B.R., Guha, G., Dube, S.C. and Munshi, J.S.D. (1974) Respiratory surface area of an air-breathing siluroid fishSaccobranchus (Heteropneustes) fossilis in relation to body size.J. Zool., Lond. 172, 215–32.Google Scholar
  34. Jakubowski, M. (1977) Size and vascularization of the respiratory surfaces of gills and skin in some cobitids (Cobitidae, Pisces).Bull. Acad. Pol. Sci. 25, 307–16.Google Scholar
  35. Jakubowski, M. (1982) Size and vascularization of the gill and skin respiratory surfaces in the white amur,Ctenopharyngodon idella (Val.) (Pisces, Cyprindae).Acta biol. cracov. 24, 93–105.Google Scholar
  36. Joseph, G.L. (1980) Respiratory surface area (gill area) of the hillstream fishGarra mullya (Sykes).Indian J. Fish 27, 172–6.Google Scholar
  37. Kobayashi, H., Murata, O. and Harada, T. (1988) Some aspects of gill measurement in relation to the growth of the yellowtailSeriola quinqueradiata.Nippon Suisan Gakkaishi 54, 49–54.Google Scholar
  38. Landolt, J.C. and Hill, L.G. (1975) Observations of the gross structure and dimensions of the gills of three species of gars (Lepisosteidae).Copeia 1975, 470–75.Google Scholar
  39. Liszka, E. (1969) The vascularization and respiratory surface of gills in the river bullhead (Cottus gobio L.).Acta biol. cracov. 12, 135–48.Google Scholar
  40. Maina, J.N. and Maloiy, G.M.O. (1986) The morphology of the respiratory organs of the African air-breathing catfish (Clarias mossambicus): a light and scanning microscopic study, with morphometric observations.J. Zool., Lond. 209A, 421–45.Google Scholar
  41. Milton, P. (1971) Oxygen consumption and osmoregulation in the shanny,Blennius pholis.J. mar. biol. Ass. U.K. 51, 247–65.Google Scholar
  42. Morgan, M. (1971) Gill development, growth and respiration in the trout,Salmo gairdneri, PhD thesis, Bristol University (not seen in original).Google Scholar
  43. Muir, B.S. (1969) Gill dimensions as a function of fish size.J. Fish. Res. Bd. Can. 26, 165–70.Google Scholar
  44. Muir, B.S. and Hughes, G.M. (1969) Gill dimensions for three species of tunny.J. exp. Biol. 51, 271–85.Google Scholar
  45. Munshi, J.S.D. (1976) Gross and fine structure of the respiratory organs of air-breathing fishes. In Hughes, G.M. ed.Respiration of Amphibious Vertebrates. New York: Academic Press, pp. 73–104.Google Scholar
  46. Newstead, J.D. (1967) Fine structure of respiratory lamellae of teleostean gills.Z. Zellforsch. mikrosk. Anat. 79, 396–428.Google Scholar
  47. Niimi, A.J. and Morgan, S.L. (1980) Morphometric examination of the gills of walleye,Stizostedion vitreum vitreum (Mitchill) and rainbow trout,Salmo gairdneri Richardson.J. Fish Biol. 16, 685–92.Google Scholar
  48. Oikawa, S. and Itazawa, Y. (1985) Gill and body surface areas of the carp in relation to body mass, with special reference to the metabolism-size relationship.J. exp. Biol. 117, 1–14.Google Scholar
  49. Ojha, J. and Munshi, J.S.D. (1974) Morphometric studies on the gill and skin dimensions in relation to body weight in a fresh-water mudeel,Macrognathus aculeatum.Zool. Anz. 193, 364–81.Google Scholar
  50. Ojha, J. and Singh, R. (1987) Effect of body size on the dimensions of the respiratory organs of freshwater catfish,Mystus vittatus.Jap. J. Ichthyol. 34, 59–65.Google Scholar
  51. Ojha, J., Rooj, N.C. and Munshi, J.S.D. (1982) Dimensions of the gills of an Indian hill-stream cyprinid fish,Garra lamta.Jap. J. Ichthyol 29, 272–8.Google Scholar
  52. Ojha, J., Singh, R. and Singh, N.K. (1985) Structure and dimensions of the respiratory organs of a freshwater catfish,Mystus cavasius (Ham.).Proc. Indian natn. Sci. Acad. 51B, 202–10.Google Scholar
  53. Pandey, A., Kunwar, G.P. and Munshi, J.S.D. (1987) Comparative study of the gill surface area of an Indian shadHilsa ilisha (Ham.) and a major carpLabeo rohita (Ham.).Proc. Indian natn. Sci. Acad. 53B, 205–14.Google Scholar
  54. Pauly, D. (1981) The relationship between gill surface area and growth performance in fish: a generalization of von Bertalanffy's theory of growth.Meeresforschung 28, 251–82.Google Scholar
  55. Piiper, J. and Scheid, P. (1982) Physical principals of respiratory gas exchange in fish gills. In Houlihan, D.F., Rankin, J.C. and Shuttleworth, T.H., eds.Gills. Cambridge: Cambridge Univ. Press, pp. 45–61.Google Scholar
  56. Pohla, H., Bernroider, G., Lametschwandtner, A. and Goldschmid, G. (1987) Computerized measurement of gill respiratory area with corrosion casts of gill vasculature.Proc. Vth Congr. europ. Ichthyol., Stockholm 1985, pp. 105–8.Google Scholar
  57. Prasad, M.S. and Prasad, P. (1984a) Morphometrics of water-blood diffusion barrier at the secondary gill lamellae during early life ofChanna punctatus (Bloch).Arch. Biol. 95, 91–100.Google Scholar
  58. Prasad, M.S. and Prasad, P. (1984b) Changes in the water-blood diffusion barrier at the secondary gill lamellae during early life inChanna (=Ophiocephalus) striatum (Bloch).Folia Morph. 22, 200–207.Google Scholar
  59. Price, J.W. (1931) Growth and gill development in the small mouthed black bass,Micropterus dolomieu, Lacapede.Stud. State Univ. Ohio 4, 3–46.Google Scholar
  60. Ricker, W.E. (1973) Linear regression in fishery research.J. Fish. Res. Bd Can. 30, 409–34.Google Scholar
  61. Robotham, P.W.J. (1978) The dimensions of the gills of two species of loach,Noemacheilus barbatulus andcobitis taenia.J. exp. Biol. 76, 181–4.Google Scholar
  62. Roy, P.K. and Munshi, J.S.D. (1986) Morhometrics of the respiratory organs of a freshwater major carp,Cirrhinus mrigala in relation to body weight.Jap. J. Ichthyol. 33, 269–79.Google Scholar
  63. SAS Institute Inc. (1989) SAS/Graph Users Guide, Release 6.03 Edition. Statistical Analysis Systems Institute Inc., Cary, NC.Google Scholar
  64. Saunders, R.L. (1962) The irrigation of the gills in fishes. II. Efficiency of oxygen uptake in relation to respiratory flow activity and concentration of oxygen and carbon dioxide.Can. J. Zool. 40, 817–62.Google Scholar
  65. Schöttle, E. (1932) Morphologie und Physiologie der Atmung bei wasser-, schlamm- und landlebenden Gobiiformes.Z. wiss. Zool. 140, 1–114.Google Scholar
  66. Sharma, S.N., Guha, G. and Singh, B.R. (1982) Gill dimensions of a hillstream fishBotia lohachata (Pisces, Cobitidae).Proc. Indian natn. Sci. Acad. 48B, 81–91.Google Scholar
  67. SPSS Inc. (1988) SPSS/PC+ Statistical Package for Social Sciences, Release 2.0, SPSS Inc., Chicago, IL.Google Scholar
  68. Starmach, J. (1971) Oxygen consumption and respiratory surface of gills inCottus poecilopus Heckel andCottus gobio L.Acta biol. cracov. 14, 9–15.Google Scholar
  69. Steen, J.B. and Berg, T. (1966) The gills of two species of haemoglobin-free fishes compared to those of other teleosts-with a note on severe anaemia in an eel.Comp. Biochem. Physiol. 18, 517–26.Google Scholar
  70. Ursin, E. (1967) A mathematical model of some aspects of fish growth, respiration and mortality.J. Fish. Res. Bd. Can. 24, 2355–453.Google Scholar
  71. Winberg, G.G. (1956) Rate of metabolism and food requirements of fishes. Belorussian State University Minsk (Fish. Res. Bd. Can. Transl. Ser. No. 194). 253 pp.Google Scholar

Copyright information

© Chapman & Hall 1992

Authors and Affiliations

  • Margit Palzenberger
    • 1
  • Hannes Pohla
    • 1
  1. 1.Zoologisches Institut de Universität SalzburgSalzburgAustria

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