Physiological Roles of the Secondary Circulatory System in Fish

  • A. Ishimatsu
  • G. K. Iwama
  • N. Heisler
Part of the Advances in Comparative and Environmental Physiology book series (COMPARATIVE, volume 21)


Most studies of the secondary circulation or the “secondary vascular system” (Vogel 1981; Vogel and Claviez 1981) have concentrated on descriptions of morphology, rather than function, among various species (see Steffensen and Lomholt 1992). The scarce available evidence at this time characterizes the secondary vascular system in fishes as being a pool of blood which is low in pressure, low in red cell content, absent from the muscle tissues, associated with both the inner and outer surfaces of body including the gills, and of a volume that approaches or exceeds that of the primary circulation. Vogel (1985a) demonstrated the occurrence of an extremely dense capillary network of the secondary system over the scales of trout and tilapia. Satchell (1991) pointed out that similar vascularization on the scales had been observed for both freshwater and seawater teleosts in old anatomical literatures (Jakubowski 1960a,b, 1989; Kaczmarski 1966; Tyszkiewicz 1969), while it is not always clear whether such capillary networks belong to either the primary or secondary vascular system. A similar subepithelial vascular network has also been observed in the Atlantic hagfish Myxine glutinosa (Lametschwandtner et al. 1989). Vogel (1985a) also stated that secondary capillary networks are distributed in the mucous membrane of the mouth and the peritoneum, and possibly in the intestinal wall. The central venous sinus (CVS) which is located within the primary lamella of the gill is currently considered to be part of the secondary vascular system (Vogel 1985a).


Rainbow Trout Chloride Cell Dorsal Aorta Secondary System Trout Gill 
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  1. Avella M, Bornancin M (1989) A new analysis of ammonia and sodium transport through the gills of the freshwater rainbow trout (Salmo gairdneri). J Exp Biol 142: 155–175Google Scholar
  2. Bailly Y, Dunel-Erb S (1986) The sphincter of the efferent filament artery in teleost gills: I. Structure and parasymphathetic innervation. J Morphol 187: 219–237CrossRefGoogle Scholar
  3. Bailly Y, Dunel-Erb S, Geffard M, Laurent P (1989) The vascular and epithelial serotonergic innervation of the actinopterygian gill filament with special reference to the trout, Salmo gairdneri. Cell Tissue Res 258: 349–363CrossRefGoogle Scholar
  4. Boland EJ, Olson KR (1979) Vascular organization of the catfish gill filament. Cell Tissue Res 198: 487–500PubMedCrossRefGoogle Scholar
  5. Cameron JN, Iwama GK (1987) Compensation of progressive hypercapnia in channel catfish and blue crabs. J Exp Biol 133: 183–197Google Scholar
  6. Chan DKO (1971) The urophysis and the caudal circulation of teleost fish. Mem Soc Endocrinol 19: 391–412Google Scholar
  7. Chan DKO (1975) Cardiovascular and renal effects of urotensin I and II in the eel, Angailla rostrata. Gen Comp Physiol 27: 52–61Google Scholar
  8. Claiborne JB, Evans DH (1980) The isolated, perfused head of the marine teleost fish, Myoxocephalus octodecimspinosus: hemodynamic effects of epinephrine. J Comp Physiol 138: 79–85Google Scholar
  9. Davie PS (1981) Neuroanatomy and control of the caudal lymphatic heart of the short-finnedeel (Anguilla australis schmidtii). Can J Zool 59: 1586–1592CrossRefGoogle Scholar
  10. Dewar H, Brill RW, Olson KR (1994) Secondary circulation of the vascular heat exchangers in skipjack tuna, Katsuwonus pelamis. J Exp Zool 269: 566–570CrossRefGoogle Scholar
  11. Dunel-Erb S, Bailly Y (1986) The sphincter of the efferent filament artery in teleost gills: II. Sympathetic innervation. J Morphol 187: 239–246CrossRefGoogle Scholar
  12. Dunel-Erb S, Bailly Y, Laurent P (1989) Neurons controlling the gill vasculature in five species of teleosts. Cell Tissue Res 255: 567–573CrossRefGoogle Scholar
  13. Ellis AE, de Sousa M (1974) Phylogeny of the lymphoid system. I. A study of the fate of circulating lymphocytes in plaice. Eur J Immunol 4: 338–343Google Scholar
  14. Farrell AP, Smith DG (1981) Microvascular pressures in gill filaments of lingcod (Ophiodon elongatus). J Exp Zool 216: 341–344CrossRefGoogle Scholar
  15. Foskett JK, Machen TE (1985) Vibrating probe analysis of teleost opercular epithelium: correlation between active transport and leak pathways of individual chloride cells. J Membr Biol 85: 25–35PubMedCrossRefGoogle Scholar
  16. Foskett JK, Scheffey C (1982) The chloride cell: definitive identification as the salt-secretory cell in teleosts. Science 215: 164–166PubMedCrossRefGoogle Scholar
  17. Fromm PO (1968) Some quantitative aspects of ion regulation in teleosts. Comp Biochem Physiol 27: 865–869CrossRefGoogle Scholar
  18. Gardaire E, Avella M, Isaia J, Bornancin M (1991) Measurement of branchial vascular space of trout, Oncorhynchus my kiss: effects of adrenaline. J Comp Physiol 161B: 265–269Google Scholar
  19. Girard JP, Payan P (1976) Effect of epinephrine on vascular space of gills and head of rainbow trout. Am J Physiol 230: 1555–1560PubMedGoogle Scholar
  20. Goss GG, Laurent P, Perry SF (1992a) Evidence for a morphological component in acid-base regulation during environmental hypercapnia in the brown bullhead (Ictalurus nebulosns). Cell Tissue Res 268: 539–552PubMedCrossRefGoogle Scholar
  21. Goss GG, Perry SF, Wood CM, Laurent P (1992b) Mechanism of ion and acid-base regulation at the gills of freshwater fish. J Exp Zool 263: 143–159PubMedCrossRefGoogle Scholar
  22. Hargens AR, Millard RW, Johansen K (1974) High capillary permeability in fishes. Comp Biochem Physiol 48A: 675–680CrossRefGoogle Scholar
  23. Heisler N (1993) Acid-base regulation. In: Evans DH (ed) The physiology of fishes. CRC Press, Boca Raton, pp 343–378Google Scholar
  24. Henrikson RC, Matoltsy AG (1968) The fine structure of teleost epidermis. III. Club cells and other cell types. J Ultrastruct Res 21: 222–232CrossRefGoogle Scholar
  25. Hipkins SF (1985) Adrenergic responses of the cardiovascular system of the eel, Anguilla australis, in vivo. J Exp Zool 235: 7–20PubMedCrossRefGoogle Scholar
  26. Hwang PP (1989) Distribution of chloride cells in teleost larvae. J Morphol 200: 1–8CrossRefGoogle Scholar
  27. Ishihara A, Mugiya Y (1987) Ultrastructural evidence of calcium uptake by chloride cells in the gills of goldfish, Carassius auratus. J Exp Zool 242: 121–129CrossRefGoogle Scholar
  28. Ishimatsu A, Iwama GK, Heisler N (1988) In vivo analysis of partitioning of cardiac output between systemic and CVS circuits in rainbow trout: a new approach using chronic cannulation of the branchial vein. J Exp Biol 137: 75–88PubMedGoogle Scholar
  29. Ishimatsu A, Iwama GK, Bentley TB, Heisler N (1992) Contribution of the secondary circulatory system to acid-base regulation during hypercapnia in rainbow trout (Oncorhynchus mykiss). J Exp Biol 170: 43–56Google Scholar
  30. Iwama GK, Ishimatsu A, Heisler N (1993) Site of acid-base relevant ion transfer in the gills of rainbow trout (Oncorhynchus mykiss) exposed to environmental hypercapnia. Fish Physiol Biochem 12: 269–280CrossRefGoogle Scholar
  31. Jakubowski M (1960a) The structure and vascularization of the skin of the eel (Anguilla anguilla L.) and the viviparous blenny (Zoarces viviparous L.). Acta Biol Crac Zool 3: 1–22Google Scholar
  32. Jakubowski M (1960b) The structure and vascularization of the skin of the leathern carp (Cyprinus carpio L. var. nuda) and flounder (Pleuronectes flesus luscus Pall.). Acta Biol Crac Zool 3: 139–162Google Scholar
  33. Jakubowski M (1989) Skin vascularization in fishes compared with that in amphibians. In: Splechtna H, Hilgers H (eds) Trends in vertebrate morphology. Gustav Fischer, Stuttgart, pp 542–545Google Scholar
  34. Kaczmarski F (1966) Structure and vascularization of the skin of the ruff (Acerina cernua L.). Acta Biol Crac Zool 9: 165–175Google Scholar
  35. Kampmeier OF (1969) Evolution and comparative morphology of the lymphatic system. Thomas, SpringfieldGoogle Scholar
  36. Kiceniuk JW, Jones DR (1977) The oxygen transport system in trout (Salino gairdneri) during sustained exercise. J Exp Biol 69: 247–260Google Scholar
  37. Lametschwandtner A, Weiger T, Lametschwandtner U, Georgieva-Hanson V, Patzner RA, Adam H (1989) The vascularization of the skin of the Atlantic hagfish, Myxine glutinosa L. as revealed by scanning electron microscopy of vascular corrosion casts. Scanning Microsc 3: 305–314Google Scholar
  38. Laurent P (1984) Gill internal morphology. In: Hoar WS, Randall DJ (eds) Fish physiology, vol XA. Academic Press, New York, pp 73–183Google Scholar
  39. Laurent P (1989) Gill structure and function: fish. In: Wood SC (ed) Comparative pulmonary physiology: current concepts. Lung biology in health and disease, vol 39. Dekker, New York, pp 69–120Google Scholar
  40. Laurent P, Perry SF (1990) Effects of cortisol on gill chloride cell morphology and ionic uptake in the freshwater trout, Salmo gairdneri. Cell Tissue Res 259: 429–442CrossRefGoogle Scholar
  41. Laurent P, Perry SF (1991) Environmental effects on fish gill morphology. Physiol Zool 64: 4–25Google Scholar
  42. Leino RL, McCormick JH (1984) Morphological and morphometrical changes in chloride cells of the gills of Pimephales promelas after chronic exposure to acid water. Cell Tissue Res 236: 121–128PubMedCrossRefGoogle Scholar
  43. Lin H, Randall DJ (1991) Evidence for the presence of an electrogenic proton pump on the trout gill epithelium. J Exp Biol 161: 119–134Google Scholar
  44. Lin H, Randall DJ (1993) H+-ATPase activity in crude homogenates of fish gill tissue: inhibitor sensitivity and environmental and hormonal regulation. J Exp Biol 180: 163–174Google Scholar
  45. Lin H, Pfeiffer DC, Vogl AW, Pan J, Randall DJ (1994) Immunolocalization of H+-ATPase in the gill epithelia of rainbow trout. J Exp Biol 195: 169–183PubMedGoogle Scholar
  46. Marshall WS (1985) Paracellular ion transport in trout opercular epithelium models osmoregulatory effects of acid precipitation. Can J Zool 63: 1816–1822CrossRefGoogle Scholar
  47. Marshall WS, Bryson SE, Wood CM (1992) Calcium transport by isolated skin of rainbow trout. J Exp Biol 166: 297–316PubMedGoogle Scholar
  48. McDonald DG, Prior ET (1988) Branchial mechanisms of ion and acid-base regulation in the freshwater rainbow trout, Salmo gairdneri. Can J Zool 66: 2699–2708CrossRefGoogle Scholar
  49. Nekvasil NP, Olson KR (1985) Localization of 3H-norepinephrine binding sites in the trout gill. J Exp Zool 235: 309–313CrossRefGoogle Scholar
  50. Nilsson S (1983) Autonomic nerve function in the vertebrates. Springer, Berlin Heidelberg New YorkGoogle Scholar
  51. Nilsson S (1984) Innervation and pharmacology of the gills. In: Hoar WS, Randall DJ (eds) Fish physiology, vol XA. Academic Press, New York, pp 185–227Google Scholar
  52. Nilsson S, Pettersson K (1981) Sympathetic nervous control of blood flow in the gills of the Atlantic cod, Gadus morhua. J Comp Physiol 144B: 157–163Google Scholar
  53. Nonnotte G, Nonnotte L, Kirsch R (1979) Chloride cells and chloride exchange in the skin of a sea-water teleost, the shanny (Blennius pholis L.). Cell Tissue Res 199: 387–396PubMedCrossRefGoogle Scholar
  54. Olson KR (1984) Distribution of flow and plasma skimming in isolated perfused gills of three teleosts. J Exp Biol 109: 97–108Google Scholar
  55. Olson KR, Meisheri KD (1989) Effects of atrial natriuretic factor on isolated arteries and perfused organs of trout. Am J Physiol 256: R10 - R18PubMedGoogle Scholar
  56. Olson KR, Kullman D, Narkates AJ, Oparil S (1986) Angiotensin extraction by trout tissues in vivo and metabolism by the perfused gill. Am J Physiol 250: R532 - R538PubMedGoogle Scholar
  57. Olson KR, Duff DW, Farrell AP, Keen J, Kellogg MD, Kullman D, Villa J (1991) Cardiovascular effects of endothelin in trout. Am J Physiol 260: H1214 - H1223PubMedGoogle Scholar
  58. Payan P, Girard JP (1977) Adrenergic receptors regulating patterns of blood flow through the gills of trout. Am J Physiol 232: H18 - H23PubMedGoogle Scholar
  59. Payan P, Girard JP, Mayer-Gostan N (1984) Branchial ion movements in teleosts: the roles of respiratory and chloride cells. In: Hoar WS, Randall DJ (eds) Fish physiology, vol XB. Academic Press, New York, pp 39–63Google Scholar
  60. Perry SF, Goss GG (1994) The effects of experimentally altered gill chloride cell surface area on acid-base regulation in rainbow trout during metabolic alkalosis. J Comp Physiol 164B: 327–336Google Scholar
  61. Perry SF, Davie PS, Daxboeck C, Ellis AG, Smith DG (1984) Perfusion methods for the study of gill physiology. In: Hoar WS, Randall DJ (eds) Fish physiology, vol XB. Academic Press, New York, pp 325–388Google Scholar
  62. Pfeiler E, Lindley V (1989) Chloride-type cells in the skin of the metamorphosing bonefish (Albula sp.) leptocephalus. J Exp Zool 250: 11–16CrossRefGoogle Scholar
  63. Randall DJ (1985) Shunts in fish gills. In: Johansen K, Burggren WW (eds) Cardiovascular shunts: phylogenetic, ontogenetic and clinical aspects. Munksgaard, Copenhagen, pp 71–87Google Scholar
  64. Satchell GH (1991) Physiology and form of fish circulation. Cambridge Univ Press, CambridgeGoogle Scholar
  65. Shephard KL (1992) Studies on the fish gill microclimate. J Comp Physiol 162B: 231–240Google Scholar
  66. Shuttleworth TJ (1989) Overview of epithelial ion-transport mechanisms. Can J Zool 67: 3032–3038CrossRefGoogle Scholar
  67. Smith DG (1977) Sites of cholinergic vasoconstriction in trout gills. Am J Physiol 233 R222 - R229PubMedGoogle Scholar
  68. Stagg RM, Shuttleworth TJ (1984) Hemodynamics and potentials in isolated flounder gills: effects of catecholamines. Am J Physiol 246: R211 - R220PubMedGoogle Scholar
  69. Steffensen JF, Lomholt JP (1992) The secondary vascular system. In: Hoar WS, Randall DJ, Farrell AP (eds) Fish physiology, vol XII. Academic Press, London, pp 185–217Google Scholar
  70. Steffensen JF, Lomholt JP, Vogel WOP (1986) In vivo observations on a specialized microvas-culature, the primary and secondary vessels in fishes. Acta Zool (Stockh) 67: 193–200CrossRefGoogle Scholar
  71. Stuffier DF, Graham JB, Dickson KA, Stockmann W (1986) Cutaneous ion transport in the freshwater teleost Synbranchus marmoratus. Physiol Zool 59: 406–418Google Scholar
  72. Sundin L, Nilsson S, (1992) Arterio-venous branchial blood flow in the Atlantic cod Gadus morhua. J Exp Biol 165: 73–84Google Scholar
  73. Tang Y, Boutilier RG (1988) Correlation between catecholamine release and degree of acidotic stress in trout. Am J Physiol 255: R395 - R399PubMedGoogle Scholar
  74. Tyszkiewicz K (1969) Structure and vascularization of the skin of the pike (Esox lucius L.). Acta Biol Crac Zool 12: 67–79Google Scholar
  75. Vogel WOP (1978) Arteriovenous anastomoses in the afferent region of trout gill filaments (Salmo gairdneri Richardson, Teleostei). Zoomorphologie 90: 205–212CrossRefGoogle Scholar
  76. Vogel WOP (1981) Struktur and Organisationsprinzip im Gefäßsystem der Knochenfische. Gegenbaurs Morphol Jahrb 127: 772–784PubMedGoogle Scholar
  77. Vogel WOP (1985a) Systemic vascular anastomoses, primary and secondary vessels in fish, and the phylogeny of lymphatics. In: Johansen K, Burggren WW (eds) Cardiovascular shunts: phylogenetic, ontogenetic and clinical aspects. Munksgaard, Copenhagen, pp 143–159Google Scholar
  78. Vogel WOP (1985b) The caudal heart of fish: not a lymph heart. Acta Anat 121: 41–45PubMedCrossRefGoogle Scholar
  79. Vogel WOP, Claviez M (1981) Vascular specialization in fish, but no evidence for lymphatics. Z Naturforsch 36C: 490–492Google Scholar
  80. Vogel WOP, Vogel V, Kremers H (1973) New aspects of the intrafilamental vascular system in gills of a euryhaline teleost, Tilapia mossambica. Z Zellforsch 144: 573–583PubMedCrossRefGoogle Scholar
  81. Whitear M (1986) The skin of fishes including cyclostomes. In: Bereiter-Hahn J, Matoltsy AG, Richards KS (eds) Biology of the integument 2. Vertebrates. Springer, Berlin Heidelberg New York, pp 8–64Google Scholar
  82. Whitear M, Mittal AK (1986) Structure of the skin of Agonus cataphractus ( Teleostei ). J Zool Lond 210A: 551–574CrossRefGoogle Scholar
  83. Zadunaisky JA (1984) The chloride cell: the active transport of chloride and the paracellular pathways. In: Hoar WS, Randall DJ (eds) Fish physiology, vol XB. Academic Press, New York, pp 129–176Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 1995

Authors and Affiliations

  • A. Ishimatsu
    • 1
  • G. K. Iwama
    • 2
  • N. Heisler
    • 3
    • 4
  1. 1.Nomo Fisheries StationNagasaki UniversityNomozaki, NagasakiJapan
  2. 2.Department of Animal Science, Faculty of Agricultural SciencesUniversity of British ColumbiaVancouverCanada
  3. 3.Department of Animal PhysiologyHumboldt University at BerlinBerlinGermany
  4. 4.Max-Planck-Institut für experimentelle MedizinGöttingenGermany

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