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Physiological adaptations of the living agnathans

Published online by Cambridge University Press:  03 November 2011

M. W. Hardisty
Affiliation:
School of Biological Sciences, University of Bath, Claverton Down, Avon, BA2 7AY, U.K.
I. C. Potter
Affiliation:
School of Biological and Environmental Sciences, Murdoch University, Perth, W. A. 6150, Australia.
R. W. Hilliard
Affiliation:
School of Biological and Environmental Sciences, Murdoch University, Perth, W. A. 6150, Australia.

Abstract

The modes of life and environments of the extant agnathans (cyclostomes) are discussed in relation to their adaptations to temperature, light, oxygen and salinity. As their antitropical distribution indicates, both hagfishes and lampreys are cold water groups. Since hagfishes live in deeper waters than lampreys, they are not exposed to the marked seasonal changes in temperature and light which influence major events in the lamprey life cycle. Both groups tend to be nocturnally active, either burrowing during daylight as in the case of larval lampreys (ammocoetes) and most hagfishes, or showing cryptic behaviour as in the case of adult lampreys. Olfaction plays a major part in the location of prey, presumably aided in adult lampreys by their eyes and sensitive electrosensory system. Rates of standard oxygen consumption, ventilatory frequency and heart rate of adult lampreys increase at night. Standard oxygen consumption is relatively low in ammocoetes (as it also is in hagfishes) but increases markedly during metamorphosis into the adult lamprey. Ammocoetes and hagfishes, and to a lesser extent adult lampreys, are resistant to reduced environmental oxygen tensions. Differences in the oxygen dissociation curves of ammocoetes, adult lampreys and hagfishes can be related to differences in the characteristics of their monomeric haemoglobins and their environments and modes of life. The extraordinary tolerance of the hagfish heart to hypoxia is a reflection of a robust capacity for glycolysis, an LDH isozyme geared towards anaerobic functioning and a low work output. The hagfishes, which are restricted to marine waters, are osmoconformers. The osmolality of their blood, which is almost wholly attributable to inorganic ions, is virtually identical to that of full strength sea water (c. 1000 mOsmkg−1). By contrast, the osmolality of the blood of larval and adult lampreys when in fresh water is only 205-260 mOsm kg−1, i.e. about one quarter to one fifth of those of hagfish, and these rise only to 240-270 mOsm kg−1 in the adults of anadromous lampreys in sea water. The regulation of ions by adult lampreys is achieved by mechanisms similar to those adopted by teleosts. The implications of the contrasting ionic and osmotic physiology of the two living groups of agnathans are discussed in relation to their possible environmental history and against the background of their Carboniferous fossil representatives.

Type
Physiological adaptations in some recent and fossil organisms
Copyright
Copyright © Royal Society of Edinburgh 1989

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References

Aldridge, R. J., Briggs, D. E. G., Clarkson, E. N. K. & Smith, P. 1986. The affinities of condonts—new evidence from the Carboniferous of Edinburgh, Scotland. LETHAIA 19, 279–91.CrossRefGoogle Scholar
Alt, J. M., Stolte, H., Eisenbach, G. M. & Walvig, F. 1980. Renal electrolyte and fluid excretion in the Atlantic hagfish Myxine glutinosa. J EXP BIOL 91, 323–30.CrossRefGoogle Scholar
Bardack, D. 1985. Les premiers fossiles de hagfish (Myxiniformes) et Enteropneusta (Hemichordata) depots de la faune (Pennsylvanienne) de Mazon Creek dans l'IIIinois, USA. BULL SOC HIST NAT AUTUN (FRANCE) 116, 97.Google Scholar
Bardack, D. & Richardson, E. S. 1977. New agnathous fishes from the Pennsylvanian of Illinois. FIELDIANA GEOL 33, 489510.Google Scholar
Bardack, D. & Zangerl, R. 1971. Lampreys in the fossil record. In Hardisty, M. W. & Potter, I. C. (eds) The Biology of Lampreys 1, 6784. London: Academic Press.Google Scholar
Bartels, H. & Welsch, U. 1986. Mitochondria-rich cells in the gill epithelium of cyclostomes: a thin section and freeze fracture study. In Uyeno, T., Arai, R., Taniuchi, T. & Matsuura, K. (eds) Indo-Pacific Fish Biology: Proceedings of the Second International Conference on Indo-Pacific fishes, 5872. Tokyo: Ichthyological Society of Japan.Google Scholar
Beamish, F. W. H. 1973. Oxygen consumption of adult Petromyzon marinus in relation to body weight and temperature. J FISH RES BD CAN 30, 1367–70.CrossRefGoogle Scholar
Beamish, F. W. H. 1974. Swimming performance of adult sea lampreys in relation to weight and temperature. TRANS AM FISH SOC 103, 355–58.2.0.CO;2>CrossRefGoogle Scholar
Beamish, F. W. H. 1980. Osmoregulation in juvenile and adult lampreys. CAN J FISH AQUAT SCI 37, 1739–50.CrossRefGoogle Scholar
Beamish, F. W. H., Strachan, P. D. & Thomas, E. 1978. Osmotic and ionic performance of the anadromous sea lamprey, Petromyzon marinus. COMP BIOCHEM PHYSIOL 60A, 435–43.CrossRefGoogle Scholar
Beamish, F. W. H. & Mookherjii, P. S. 1964. Respiration of fishes with special emphasis on standard oxygen consumption. CAN J ZOOL 42, 161–75.CrossRefGoogle Scholar
Bird, D. J., Lutz, P. L. & Potter, I. C. 1976. Oxygen dissociation curves of the blood of larval and adult lampreys (Lampetra fluviatilis). J EXP BIOL 65, 449–58.CrossRefGoogle ScholarPubMed
Bird, D. J. & Potter, I. C. 1983. Changes in the fatty acid composition of triacylglycerols and phospholipids during the life cycle of the lamprey Geotria australis Gray. COMP BIOCHEM PHYSIOL 75B, 3141.Google Scholar
Bloom, G., Östlund, E. & Fänge, R. 1963. Functional aspects of the cyclostome heart in relation to recent structural findings. In Brodal, A. & Fänge, R. (eds) The Biology of Myxine, 317–39. Oslo: Universitetsforlaget.Google Scholar
Bodznick, D. & Preston, D. G. 1983. Physiological characterization of electroreceptors in the lamprey Ichthyomyzon unicuspis and Petromyzon marinus. J COMP PHYSIOL 152A, 209–18.CrossRefGoogle Scholar
Brittain, T. & Wells, R. M. G. 1986. Characterization of the changes in the state of aggregation induced by ligand binding in the hemoglobin system of a primitive vertebrate, the hagfish Eptatretus cirrhatus. COMP BIOCHEM PHYSIOL 85A, 785–90.CrossRefGoogle Scholar
Bull, J. M. & Morris, R. 1967. Studies on freshwater osmoregulation in the ammocoete larva of Lampetra planeri (Bloch). 1. Ionic constituents, fluid compartments, ionic compartments and water balance. J EXP BIOL 47, 485–94.CrossRefGoogle Scholar
Bullock, T. H. 1986. Significance of findings on electroreception for general neurobiology. In Bullock, T. H. & Heiligenberg, W. (eds) Electroreception, 651–74. New York: Wiley Interscience.Google Scholar
Burggren, W., Johansen, K. & McMahon, B. 1985. Respiration in phyletically ancient fishes. In Foreman, R. E., Gorbman, A., Dodd, J. M. & Olsson, R. (eds) Evolutionary Biology of Primitive Fishes, 217–52. New York: Plenum Press.CrossRefGoogle Scholar
Cholette, C., Gagnon, A. & Germain, P. 1970. Isosmotic adaptations in Myxine glutinosa L. I. Variations of some parameters and the role of the amino acid pool of the muscle cells. COMP BIOCHEM PHYSIOL 33A, 333–46.CrossRefGoogle Scholar
Claridge, P. N., Potter, I. C. & Hughes, G. M. 1973. Circadian rhythms of activity, ventilatory frequency and heart rate in the adult river lamprey, Lampetra fluviatilis. J ZOOL LONDON 171, 239–50.CrossRefGoogle Scholar
Claridge, P. N. & Potter, I. C. 1975. Oxygen consumption, ventilatory frequency and heart rate of lampreys (Lampetra fluviatilis) during their spawning run. J EXP BIOL 63, 193206.CrossRefGoogle ScholarPubMed
Cole, W. C. & Youson, J. H. 1981. The effect of pinealectomy, continuous light, and continuous darkness on metamorphosis of anadromous Sea Lamprey, Petromyzon marinus L. J EXP ZOOL 218, 387404.CrossRefGoogle Scholar
Cossins, A. R. & Bowler, K. 1987. Temperature biology of animals. London: Chapman and Hall.CrossRefGoogle Scholar
Dawson, J. A. 1963. The oral cavity, the ‘jaws’ and the horny teeth of Myxine glutinosa. In Brodal, A. & Fänge, R. (eds) The Biology of Myxine, 231235. Oslo: Universitetsforlaget.Google Scholar
Eddy, J. M. P. 1972. The pineal complex. In Hardisty, M. W. & Potter, I. C. (eds) The Biology of Lampreys 2, 91103. London: Academic Press.Google Scholar
Enequist, P. 1937. Das Bachneunauge als ökologische Modification des Flüssneunauges. Über die Flüss- und Bachneunaugen Schwedens. ARK ZOOL 29, 122.Google Scholar
Evans, D. H. 1984. Gill Na+/H+ and exchange systems evolved before the vertebrates entered freshwater. J EXP BIOL 113, 465–69.CrossRefGoogle Scholar
Fänge, R. 1985. Regulation of blood and body fluids in primitive fish groups. In Foreman, R. E., Gorbman, A., Dodd, J. M. & Olsson, R. (eds) Evolutionary Biology of Primitive Fishes, 253–73. New York: Plenum Press.CrossRefGoogle Scholar
Farmer, G. J., Beamish, F. W. H. & Robinson, G. A. 1975. Food consumption of the adult landlocked sea lamprey, Petromyzon marinus L. COMP BIOCHEM PHYSIOL 50A, 753–7.CrossRefGoogle Scholar
Febry, R. & Lutz, P. 1987. Energy Partitioning in fish: the activity-related cost of osmoregulation in a euryhaline cichlid. J EXP BIOL 128, 6385.CrossRefGoogle Scholar
Fernholm, B. 1974. Diurnal variations in the behaviour of the hagfish, Eptatretus burgeri. MAR BIOL 27, 351–66.CrossRefGoogle Scholar
Fernholm, B. & Holmberg, K. 1974. The eyes in three genera of hagfish, Eptatretus, Paramyxine and Myxine—a case of degenerative evolution. VISION RES 15, 253–59.CrossRefGoogle Scholar
Forey, P. L. 1984. Yet more reflections on Agnathan-gnathostome relationships. J VERT PALAEONTOL 4, 330–43.CrossRefGoogle Scholar
Franz, V. 1932. Auge und Akkommodation von Petromyzon (Lampetra) fluviatilis L. ZOOL JB 52, 118–78.Google Scholar
Galloway, R., Potter, I. C.Macey, D. J., & Hilliard, R. W. 1987. Oxygen consumption and responses to hypoxia in the ammocoetes of the Southern Hemisphere lamprey, Geotria australis. FISH PHYSIOL BIOCHEM 3, 6372.CrossRefGoogle Scholar
Gladner, J. A., Lewis, M. S. & Chung, S. I. 1981. Molecular properties of lamprey fibrinogen. J BIOL CHEM 256, 1772–81.CrossRefGoogle ScholarPubMed
Goodman, M., Miyamoto, M. M. & Czelusniak, J. 1987. Pattern and process in vertebrate phylogeny revealed by coevolution of molecules and morphologies. In Patterson, C. (ed.) Molecules and Morphology in Evolution: Conflict or Compromise, 141–76. Cambridge: Cambridge University Press.Google Scholar
Griffith, R. W. 1985. Habitat, phylogeny and the evolution of osmoregulatory strategies in primitive fishes. In Foreman, R. E., Gorbman, A., Dodd, J. M., & Olsson, R. (eds) Evolutionary Biology of Primitive Fishes, 6980. New York: Plenum Press.CrossRefGoogle Scholar
Griffith, R. W. 1987. Freshwater or marine origin of the vertebrates? COMP BIOCHEM PHYSIOL 87A, 523–31.CrossRefGoogle Scholar
Gustafson, A. 1935. On the biology of Myxine glutinosa. ARK ZOOL 28, 128.Google Scholar
Hansen, C. A. & Sidell, B. D. 1983. Atlantic hagfish muscle, metabolic basis of tolerance to anoxia. AM J PHYSIOL 244, 356–62.Google ScholarPubMed
Hardisty, M. W. 1956. Some aspects of osmotic regulation in lampreys. J EXP BIOL 33, 431–47.CrossRefGoogle Scholar
Hardisty, M. W. 1957. Osmotic conditions during the embryonic and early larval life of the brook lamprey (Lampetra planeri). J EXP BIOL 34, 2325.CrossRefGoogle Scholar
Hardisty, M. W. 1961. Studies on an isolated spawning population of the brook lamprey (Lampetra planeri). J ANIM ECOL 30, 339–55.CrossRefGoogle Scholar
Hardisty, M. W. 1979. Biology of Cyclostomes. London: Chapman & Hall.CrossRefGoogle Scholar
Hardisty, M. W. 1982. Lampreys and hagfishes: an analysis of cyclostome relationships. In Hardisty, M. W. & Potter, I. C. (eds) The Biology of Lampreys 4B, 165259. London: Academic Press.Google Scholar
Hardisty, M. W., Zelnik, P. R. & Wright, V. C. 1976. The effects of hypoxia on blood sugar levels and on the endocrine pancreas, interrenal and chromaffin tissues of the lamprey, Lampetra fluviatilis L. GEN COMP ENDOCRINOL 28, 184204.CrossRefGoogle Scholar
Hardisty, M. W. & Potter, I. C. 1971a. The general biology of adult lampreys. In Hardisty, M. W. & Potter, I. C. (eds) The Biology of Lampreys 1, 127206. London: Academic Press.Google Scholar
Hardisty, M. W. & Potter, I. C. 1971b. The behaviour, ecology and growth of larval lampreys. In Hardisty, M. W. & Potter, I. C. (eds) The Biology of Lampreys 1, 85125. London: Academic Press.Google Scholar
Hill, B. J. & Potter, I. C. 1970. Oxygen consumption in ammocoetes of the lamprey Ichthyomyzon hubbsi Raney. J EXP BIOL 53, 4757.CrossRefGoogle ScholarPubMed
Hilliard, R. W., Potter, I. C. & Macey, D. J. 1985. The dentition and feeding mechanism in adults of the Southern Hemisphere lamprey Geotria australis Gray. ACTA ZOOL STOCKH 66, 159170.CrossRefGoogle Scholar
Hubbs, C. L. & Potter, I. C. 1971. Distribution, phylogeny and taxonomy. In Hardisty, M. W. & Potter, I. C. (eds) The Biology of Lampreys 1, 165. London: Academic Press.Google Scholar
Janvier, P. 1981. The phylogeny of the Craniata, with particular reference to the significance of fossil “Agnathans”. J VERT PALEONTOL 1, 121–59.CrossRefGoogle Scholar
Janvier, P. 1986. Les nouvelles conceptions de la phylogenie et de la classification des “Agnathes” et des Sarcopterygians. OCEANIS 12, 123–36.Google Scholar
Janvier, P. & Blieck, A. 1979. New data on the internal anatomy of the Heterostraci (Agnatha), with general remarks on the phylogeny of the Craniata. ZOOL SCR 8, 287–96.CrossRefGoogle Scholar
Janvier, P. & Lund, R. 1983. Hardistiella montanensis N. Gen. et Sp. (Petromyzontida) from the Lower Carboniferous of Montana, with remarks on the affinities of the lampreys. J VERT PALEONTOL 2, 407–13.CrossRefGoogle Scholar
Johansen, K., Lenfant, C. & Hanson, D. 1973. Gas exchange in the lamprey, Entosphenus tridentatus. COMP BIOCHEM PHYSIOL 44A, 107–19.CrossRefGoogle Scholar
Joss, J. M. P. 1977. Hydroxyindole-O-methyltransferase (HIOMT) activity and the uptake of 3H-melatonin in the lamprey, Geotria australis Gray. GEN COMP ENDOCR 31, 270–75.CrossRefGoogle ScholarPubMed
Joss, J. M. P. & Potter, I. C. 1982. Circadian rhythms. In Hardisty, M. W. & Potter, I. C. (eds) The Biology of Lampreys 4B, 117–35. London: Academic Press.Google Scholar
Korolewa, N. W. 1964. [Water respiration of lamprey and survival in a moist atmosphere]. ISV VSES NAUCHNO-ISSLED INST OZERN RECHN RYB KHOZ 58, 186–90 [in Russian].Google Scholar
Krejsa, R. J. & Slavkin, H. C. 1987. The hagfish-conodont connection. J DENTAL RES 66, 144.Google Scholar
Lemons, D. E. & Crayshaw, L. I. 1978. Temperature regulation in Pacific lamprey. FED PROC 37, 929.Google Scholar
Lewis, S. V. 1980. Respiration in lampreys. CAN J FISH AQUAT SCI 37, 1711–22.CrossRefGoogle Scholar
Lewis, S. V. & Potter, I. C. 1977. Oxygen consumption during the metamorphosis of the parasitic lamprey, Lampetra fluviatilis (L.) and its non-parasitic derivative, Lampetra planeri (Bloch). J EXP BIOL 69, 187–98.CrossRefGoogle Scholar
Logan, A. G., Moriarty, R. J. & Rankin, J. C. 1980. A micropuncture study of kidney function in the river lamprey adapted to freshwater. J EXP BIOL 85, 137–47.CrossRefGoogle Scholar
Løvtrup, S. 1977. The phytogeny of Vertebrata. New York: Wiley & Sons.Google Scholar
Lund, R. & Janvier, P. 1986. A second lamprey from the Lower Carboniferous of Bear Gulch, Montana (USA). GEOBIOS 19, 647652.CrossRefGoogle Scholar
Lutz, P. 1975. Adaptive and evolutionary aspects of the ionic content of fishes. COPEIA 1975, 369–73.CrossRefGoogle Scholar
Macallum, A. H. 1910. The inorganic composition of the blood in vertebrates and its origin. PROC R SOC LONDON B83, 602–04.Google Scholar
Macey, D. J. & Potter, I. C. 1978. Lethal temperatures of ammocoetes of the Southern Hemisphere lamprey, Geotria australis Gray. ENVIRON BIOL FISHES 3, 241–43.CrossRefGoogle Scholar
Macey, D. J. & Potter, I. C. 1982. The effect of temperature on the oxygen dissociation curves of whole blood of larval and adult lampreys (Geotria australis). J EXP BIOL 97, 253–61.CrossRefGoogle ScholarPubMed
Maisey, J. G. 1986. Heads and tails: a chordate phylogeny. CLADISTICS 2, 201–56.CrossRefGoogle ScholarPubMed
Mallatt, J. 1984. Early vertebrate evolution: pharyngeal structure and the origin of gnathostomes. J ZOOL LONDON 204, 169–83.CrossRefGoogle Scholar
Mallatt, J., Conley, D. M. & Ridgway, R. L. 1987. Why do hagfish have gill ‘chloride cells’ when they need not regulate plasma NaCl concentration?. CAN J ZOOL 65, 1956–65.CrossRefGoogle Scholar
Manion, P. J. & Smith, B. R. 1978. Biology of larval and metamorphosing sea lampreys, Petromyzon marinus, of the 1960 year class in the Big Garlic river, Michigan. Part II, 1966–72. GT LAKES FISH COMM TECH REP 30, 135.Google Scholar
Manwell, C. 1963. The blood proteins of cyclostomes. In Brodal, A. & Fänge, R. (eds) The Biology of Myxine, 372455. Oslo: Universitetsforlaget.Google Scholar
Mathers, J. S. & Beamish, F. W. H. 1974. Changes in serum osmotic and ionic concentration in land-locked Petromyzon marinus. COMP BIOCHEM PHYSIOL 49A, 677–88.CrossRefGoogle Scholar
McCauley, R. W., Reynolds, W. W. & Huggins, N. H. 1977. Photokinesis and behavioural thermoregulation in adult sea lampreys (Petromyzon marinus). J EXP ZOOL 202, 431437.CrossRefGoogle Scholar
McFarland, W. N. & Munz, F. W. 1965. Regulation of body weight and serum composition of hagfish in various media. COMP BIOCHEM PHYSIOL 14A, 383–98.CrossRefGoogle Scholar
McInerney, J. E. 1974. Renal sodium reabsorption in hagfish, Eptatretus stoutii. COMP BIOCHEM PHYSIOL 49A, 273–80.CrossRefGoogle Scholar
McInerney, J. E. & Evans, D. C. 1970. Habitat characteristics of the Pacific hagfish, Polistotrema stoutii. J FISH RES BD CAN 27, 966–68.CrossRefGoogle Scholar
Morris, R. 1958. The mechanism of marine osmoregulation in the lampern (Lampetra fluviatilis) and the causes of its breakdown during the spawning migration. J EXP BIOL 35, 649–65.CrossRefGoogle Scholar
Morris, R. 1980. Blood composition and osmoregulation in ammocoete larva. CAN J FISH AQUAT SCI 37, 1665–79.CrossRefGoogle Scholar
Munz, F. W. & Morris, R. 1965. Metabolic rate of the hagfish Eptatretus stouti (Lockington) 1878. COMP BIOCHEM PHYSIOL 16, 15.CrossRefGoogle Scholar
Newth, D. R. & Ross, D. M. 1955. On the reaction to light of Myxine glutinosa L. J EXP BIOL 32, 421.CrossRefGoogle Scholar
Nikinmaa, M. & Weber, R. E. 1984. Hypoxic acclimation in the lamprey, Lampetra fluviatilis; organismic and erythrocytic responses. J EXP BIOL 109, 109–20.CrossRefGoogle Scholar
Piavis, G. W. 1971. Embryology. In Hardisty, M. W. & Potter, I. C. (eds) The Biology of Lampreys 1, 361400. London: Academic Press.Google Scholar
Pickering, A. D. & Morris, R. 1970. Osmoregulation of Lampetra fluviatilis and Petromyzon marinus (Cyclostomata) in hypertonic solutions. J EXP BIOL 53, 231–43.CrossRefGoogle Scholar
Potter, I. C. 1980a. The ecology of larval and metamorphosing lampreys. CAN J FISH AQUAT SCI 37, 16411657.CrossRefGoogle Scholar
Potter, I. C. 1980b. The Petromyzoniformes with particular reference to paired species. CAN J FISH AQUAT SCI 37, 15951615.CrossRefGoogle Scholar
Potter, I. C., Hill, B. J. & Gentleman, S. 1970. Survival and behaviour of ammocoetes at low oxygen levels. J EXP BIOL 53, 5973.CrossRefGoogle Scholar
Potter, I. C., Lord, Percy R., Barber, D. L. & Macey, D. J. 1982. The morphology, development and physiology of blood cells. In Hardisty, M. W. & Potter, I. C. (eds) The Biology of Lampreys 4A, 233–92. London: Academic Press.Google Scholar
Potter, I. C. & Hilliard, R. W. 1987. A proposal for the functional and phylogenetic significance of differences in the dentition of lampreys. J ZOOL LONDON 212, 513–37.CrossRefGoogle Scholar
Potter, I. C. & Huggins, R. J. 1973. Observations on the morphology, behaviour and salinity tolerance of downstream migrating river lampreys (Lampetra fluviatilis). J ZOOL LONDON 169, 365–79.CrossRefGoogle Scholar
Potter, I. C. & Rogers, M. J. 1972. Oxygen consumption in burrowed and unburrowed ammocoetes of Lampetra planeri (Bloch). COMP BIOCHEM PHYSIOL 41A, 427–32.CrossRefGoogle Scholar
Prosser, C. L., Ayers, J., Green, E. & Nelson, D. 1985. Evolution of temperature regulation and of constancy of function (homeokinesis) at different temperatures. In Foreman, R. E., Gorbman, A., Dodd, J. M. & Olsson, R. (eds) Evolutionary Biology of Primitive Fishes, 203–15. New York: Plenum Press.CrossRefGoogle Scholar
Raven, J. A. 1985. Comparative physiology of plant and arthropod land adaptation. PHILOS TRANS R SOC LONDON B309, 273–88.Google Scholar
Reynolds, W. W. & Casterlin, M. E. 1978. Behavioural thermoregulation by ammocoete larvae of the sea lamprey (Petromyzon marinus) in an electronic shuttlebox. HYDROBIOLOGIA 61, 145–47.CrossRefGoogle Scholar
Riegel, J. A. 1986. Hydrostatic pressures in the glomeruli and renal vasculature of the hagfish, Eptatretus stouti. J EXP BIOL 123, 359–71.CrossRefGoogle ScholarPubMed
Riggs, A. 1972. The haemoglobins. In Hardisty, M. W. & Potter, I. C. (eds) The Biology of Lampreys 2, 261–86. London: Academic Press.Google Scholar
Robertson, J. D. 1954. The chemical composition of the blood of some aquatic chordates, including members of the Tunicata, Cyclostomata and Osteichthyes. J EXP BIOL 31, 424–42.CrossRefGoogle Scholar
Robertson, J. D. 1957. The habitat of the earliest vertebrates. BIOL REV 32, 156–87.CrossRefGoogle Scholar
Robertson, J. D. 1974. Osmotic and ionic regulation in cyclostomes. In Florkin, M. & Scheer, B. T. (eds) Chemical Zoology 8, 149–93. New York: Academic Press.Google Scholar
Robertson, J. D. 1976. Chemical composition of the body fluids and muscle of the hagfish, Myxine glutinosa, and the rabbit fish Chimaera monstrata. J ZOOL LONDON 178, 261–77.CrossRefGoogle Scholar
Robertson, J. D. 1984. The composition of blood plasma and parietal muscle of Oslo Fjord eels [Anguilla anguilla (L.)] and the river lamprey [Lampetra fluviatilis (L.)]. COMP BIOCHEM PHYSIOL 77A, 431–39.CrossRefGoogle Scholar
Ross, D. M. 1963. The sense organs of Myxine glutinosa. In Brodal, A. & Fänge, R. (eds) The Biology of Myxine, 150–60. Oslo: Universitetsforlaget.Google Scholar
Rovainen, C. M. 1982. Neurophysiology. In Hardisty, M. W. & Potter, I. C. (eds) The Biology of Lampreys 4A, 1136. London: Academic Press.Google Scholar
Ruben, J. A. & Bennett, A. F. 1980. Antiquity of the vertebrate patterns of activity metabolism and its possible vertebrate origins. NATURE 286, 886–88.CrossRefGoogle ScholarPubMed
Rubinson, K., Ripps, H., Witkovsky, P. & Kennedy, M. C. 1977. Retinal development in the lamprey, Petromyzon marinus. SOC NEUROSCI ABSTR 3, 575.Google Scholar
Rudy, P. P. & Wagner, R. C. 1970. Water permeability in the Pacific hagfish, Polistotrema stouti and the staghorn sculpin, Leptococcus armatus. COMP BIOCHEM PHYSIOL 34, 339403.CrossRefGoogle Scholar
Runnegar, B. 1982. The Cambrian explosion: animals or fossils? J GEOL SOC AUST 29, 395411.CrossRefGoogle Scholar
Rutten, M. G. 1970. The history of atmospheric oxygen. SPACE LIFE SCI 2, 517.Google ScholarPubMed
Schaeffer, B. & Thomson, K. S. 1980. Reflections on agnathan-gnathostome relationships. In Jacobs, L. L. (ed.) Aspects of Vertebrate History: Essays in Honor of Edwin Harris Colbert, 1933. Flagstaff: University of Northern Arizona Press.Google Scholar
Schmidt-Nielsen, K. 1983. Animal Physiology. Cambridge: Cambridge University Press.Google Scholar
Shelton, R. G. J. 1978. On the feeding of the hagfish, Myxine glutinosa, in the North Sea. J MAR BIOL ASSOC UK 58, 8186.CrossRefGoogle Scholar
Sheren, S. B., Eikenberry, E. F., Broek, D. L., van, der Rest M., Doering, T., Kelly, J., Hardt, T. & Brodsky, B. 1986. Type II collagen of lamprey. COMP BIOCHEM PHYSIOL 85B, 514.Google Scholar
Sidell, B. D. 1983. Cardiac metabolism in the Myxinidae; physiological and phylogenetic considerations. COMP BIOCHEM PHYSIOL 76A, 495505.CrossRefGoogle Scholar
Sidell, B. D. & Beland, K. F. 1980. Lactate dehydrogenase of Atlantic hagfish. Physiological and evolutionary implications of a primitive heart isozyme. SCIENCE 207, 769–70.CrossRefGoogle ScholarPubMed
Smith, H. W. 1932. Water regulation and its evolution in the fishes. Q REV BIOL 7, 126.CrossRefGoogle Scholar
Smith, K. L. & Hessler, R. R. 1974. Respiration of benthopelagic fishes: in situ measurements at 1230 metres. SCIENCE 184, 72–3.CrossRefGoogle Scholar
Steffensen, J. F., Johansen, K., Sindberg, C. D., Sorensen, J. H. & Moller, J. L. 1984. Ventilation and oxygen consumption in the hagfish, Myxine glutinosa L. MAR BIOL ECOL 84, 173–78.CrossRefGoogle Scholar
Steven, D. M. 1955. Experiments on the light sense of the hag, Myxine glutinosa L. J EXP BIOL 32, 2238.CrossRefGoogle Scholar
Strahan, R. 1963. The behaviour of myxinoids. ACTA ZOOL STOCKH 24, 130.Google Scholar
Wells, R. M. G., Forster, M. E., Davison, W., Taylor, H. H., Davie, P. S. & Satchell, G. H. 1986. Blood oxygen transport in the free-swimming hagfish, Eptatretus cirrhatus. J EXP BIOL 123, 4353.CrossRefGoogle ScholarPubMed
Yalden, D. W. 1985. Feeding mechanisms as evidence for cyclostome monophyly. ZOOL J LINN SOC 84, 291300.CrossRefGoogle Scholar