Comprehensive Physiology Wiley Online Library

Invertebrate Blood Oxygen Carriers

Full Article on Wiley Online Library



Abstract

The sections in this article are:

1 The Red Blood Cell Hemoglobins
1.1 Distribution and Localization
1.2 Molecular Structure
1.3 Respiratory Properties
1.4 Physiological Functions
2 The Hemerythrins
2.1 Distribution and Location
2.2 Molecular Structure
2.3 Respiratory Properties
2.4 Physiological Functions
3 The Extracellular Heme Proteins
3.1 Nematodes
3.2 Nemertines
3.3 Annelids, Pogonophorans, and Vestimentiferans
3.4 Molluscs
3.5 Arthropods
4 The Molluscan Hemocyanins
4.1 Distribution and Location
4.2 Molecular Structure
4.3 Respiratory Properties
4.4 Physiological Performance
5 The Arthropod Hemocyanins
5.1 Distribution and Location
5.2 Quaternary Structure
5.3 Molecular Relationships
5.4 Oxygen Carrying Capacity
5.5 Oxygen Binding Properties
5.6 Physiological Performance
6 Are There Unknown Functions of the Oxygen Carriers?
7 Conclusions
Figure 1. Figure 1.

Physiological performance of a cooperative (dashed line) and a noncooperative (solid line) hemoglobin with the same oxygen affinity, in a circulation in which equilibration times are long and the difference between the tissues (left arrow directed upward from the abscissa) and the gill (right arrow) is large. The changes in oxygenation differ very little.

Figure 2. Figure 2.

Oxygen equilibrium of Themiste zostericola tentacular hemerythrins. Represented are the hemerythrin stripped of inorganic ions except 10 mmol · 1−1 Ca (NO3)2 (solid line), the hemerythrin in a saline designed to simulate the inorganic ion environment within the PBC (dashed line), and intact PBCs in an extracellular saline (dotted line). The small difference between tentacular hemerythrin extracts in the intracellular saline and the PBCs is believed to be due to the inevitable inaccuracy of the intracellular saline. 20°C, 0.05 mmol · 1−1 Tris maleate buffer (pH 7.6–7.7).

Data from Mangum and Burnett 67
Figure 3. Figure 3.

Transmission electron micrograph of the extracellular hemoglobin of the annelid Amphitrite ornata, negatively stained with phosphotungstate and prepared by J. L. Scott. The hexagons (top view) measure 24.5 nm across at the parallel sides; each pair in the stack (side view) in the upper central portion of the micrograph measures 16 nm in height.

Figure 4. Figure 4.

Examples of the latitudinal temperature compensation of oxygen affinity in congeneric or otherwise closely related species.

Data from Mangum et al. 77, Brix et al. 13, Mangum and Lykkeboe 73, Mangum 57, Miller and Mangum 92, and J. E. Reese and C. P. Mangum (unpublished observations
Figure 5. Figure 5.

Physiological performance of a cooperative (dashed line) and a noncooperative (solid line) hemocyanin with the same oxygen affinity, when the blood Po2 difference between the two sites of gas exchange is small. Under the Po2 regime (shown by the arrows directed upward from the abscissa), the cooperativity confers a much greater advantage than in Figure 1.

Figure 6. Figure 6.

Free calcium in the blood of Callinectes sapidus. Right: individuals (n = 30) sampled immediately after a summer collection from normoxic seaside (Po2 >135 Torr, 30 o/oo salinity) waters and individuals (n = 43) from hypoxic estuarine (Po2 30–50 Torr, 14–18 o/oo) waters. The blood was sampled on board, immediately after catching the animals by line and net. Left: both groups (N = 21–22) after acclimation in the laboratory to aerated, estuarine water. The samples from the hypoxic animals contained 3.8(± 0.2 S.E.) mmol · 1−1 lactate; no significant quantities were found in the other three groups.



Figure 1.

Physiological performance of a cooperative (dashed line) and a noncooperative (solid line) hemoglobin with the same oxygen affinity, in a circulation in which equilibration times are long and the difference between the tissues (left arrow directed upward from the abscissa) and the gill (right arrow) is large. The changes in oxygenation differ very little.



Figure 2.

Oxygen equilibrium of Themiste zostericola tentacular hemerythrins. Represented are the hemerythrin stripped of inorganic ions except 10 mmol · 1−1 Ca (NO3)2 (solid line), the hemerythrin in a saline designed to simulate the inorganic ion environment within the PBC (dashed line), and intact PBCs in an extracellular saline (dotted line). The small difference between tentacular hemerythrin extracts in the intracellular saline and the PBCs is believed to be due to the inevitable inaccuracy of the intracellular saline. 20°C, 0.05 mmol · 1−1 Tris maleate buffer (pH 7.6–7.7).

Data from Mangum and Burnett 67


Figure 3.

Transmission electron micrograph of the extracellular hemoglobin of the annelid Amphitrite ornata, negatively stained with phosphotungstate and prepared by J. L. Scott. The hexagons (top view) measure 24.5 nm across at the parallel sides; each pair in the stack (side view) in the upper central portion of the micrograph measures 16 nm in height.



Figure 4.

Examples of the latitudinal temperature compensation of oxygen affinity in congeneric or otherwise closely related species.

Data from Mangum et al. 77, Brix et al. 13, Mangum and Lykkeboe 73, Mangum 57, Miller and Mangum 92, and J. E. Reese and C. P. Mangum (unpublished observations


Figure 5.

Physiological performance of a cooperative (dashed line) and a noncooperative (solid line) hemocyanin with the same oxygen affinity, when the blood Po2 difference between the two sites of gas exchange is small. Under the Po2 regime (shown by the arrows directed upward from the abscissa), the cooperativity confers a much greater advantage than in Figure 1.



Figure 6.

Free calcium in the blood of Callinectes sapidus. Right: individuals (n = 30) sampled immediately after a summer collection from normoxic seaside (Po2 >135 Torr, 30 o/oo salinity) waters and individuals (n = 43) from hypoxic estuarine (Po2 30–50 Torr, 14–18 o/oo) waters. The blood was sampled on board, immediately after catching the animals by line and net. Left: both groups (N = 21–22) after acclimation in the laboratory to aerated, estuarine water. The samples from the hypoxic animals contained 3.8(± 0.2 S.E.) mmol · 1−1 lactate; no significant quantities were found in the other three groups.

References
 1. Arp, A. J. The role of heme compounds in sulfide tolerance in the echiuran worm Urechis caupo. In: Structure and Function of Invertebrate Oxygen Carriers, edited by S. N. Vinogradov, Heidelberg: Springer‐Verlag, 1991, pp. 337–346.
 2. Arp, A. J., and J. J. Childress. Blood function in the hydrothermal vent vestimentiferan tube worm. Science 213: 342–344, 1981.
 3. Arp, A. J., J. J. Childress, and R. D. Vetter. The sulphide‐binding protein in the blood of the vestimentiferan tube‐worm, Riftia pachyptila, is the extracellular haemoglobin. J. Exp. Biol. 128: 139–158, 1987.
 4. Baden, S. P., L. Pihl, and R. Rosenberg. Effects of oxygen depletion on the ecology, blood physiology and fishery of the Norway lobster Nephrops norvegicus. Mar. Ecol. Progr. Ser. 67: 141–155, 1990.
 5. Baker, S. Hemoglobin function in a burrowing sea cucumber, Paracaudina chilensis. M.S. thesis, University of Oregon, Eugene, 1988.
 6. Baker, S., and N. B. Terwilliger. Hemoglobin structure and function in the rat‐tailed sea cucumber, Paracaudina chiliensis. Biol. Bull. 185: 115–122, 1993.
 7. Barnhart, M. C. Hemocyanin function in active and dormant land snails, Otala lactea. Physiol. Zool. 59: 725–732, 1986.
 8. Beardsley, A. M., J. M. Colacino, R. Cashon, and C. J. Bonaven‐tura. The hemoglobin of the brittle star, Hemipbolis elongata (Say) (Ophiuroidea, Echinodermata): biochemical and ligand binding properties. Am. Zool. 33: 77, 1993.
 9. Booth, C. R., B. R. McMahon, and A. W. Pinder. Oxygen uptake and the potentiating effects of increased hemolymph lactate on oxygen transport during exercise in the blue crab, Callinectes sapidus. J. Comp. Physiol. 148: 111–121, 1982.
 10. Bouchet, J.‐Y., and J.‐P. Truchot. Effects of hypoxia and l‐lactate on the haemocyanin–oxygen affinity of the lobster, Hontarus vulgaris. Comp. Biochem. Physiol. [A] 80: 69–74, 1985.
 11. Bowen, S. T., J. P. Durkin, G. Sterling, and L. S. Clark. Artemia hemoglobins: genetic variation in parthenogenetic and zygogenetic populations. Biol. Bull. 155: 273–287, 1978.
 12. Breton‐Gorius, J. Etude au microscope électronique des cellulules chloragogènes d'Arenicola marina L. Leur rôle dans la synthèse de l'hémoglobine. PhD Thesis, University of Paris, Paris: Masson, 1963.
 13. Brix, O., G. Lykkeboe, and K. Johansen. Reversed Bohr and Root shifts in hemocyanin of the marine prosobranch, Buccinutn undatum: Adaptation to a periodically hypoxic habitat. J. Comp. Physiol. 129: 97–103, 1979.
 14. Brown, A. C. Effects of temperature and salinity on the respiratory physiology of the Dungeness crab, Cancer magister, during development. Ph.D. diss., University of Oregon, Eugene, 1992.
 15. Burnett, L. E., and C. R. Bridges. The physiological properties and function of ventilatory pauses in the crab Cancer pagurus. J. Comp. Physiol. 145: 81–88, 1981.
 16. Callicott, K. A., and C. P. Mangum. Phenotypic variation and lability of the subunit composition of the hemocyanin of Uca pugilator. J. Exp. Mar. Biol. Ecol. 165: 143–159, 1993.
 17. Cameron, J. N., and D. E. Wohlschlag. Respiratory response to experimentally induced anemia in the pinfish (Lagodon rhomhoides). J. Exp. Biol. 50: 307–317, 1969.
 18. Childress, J. J., A. J. Arp, and C. R. Fisher. Metabolic and blood characteristics of the hydrothermal vent tube worm Riftia pachyptila. Mar. Biol. 83: 109–124, 1984.
 19. Dall, W. Indices of nutritional state in the western rock lobster Panulirus longipes (Milne‐Edwards). I. Blood and tissue constituents and water content. J. Exp. Mar. Biol. Ecol. 16: 167–180, 1974.
 20. Deaton, L. E., and C. P. Mangum. The function of hemoglobin in the arcid clam Noetia ponderosa. II. Oxygen uptake and storage. Comp. Biochem. Physiol. 53A: 181–186, 1976.
 21. Defur, P. L., C. P. Mangum, and J. E. Reese. Respiratory responses of the blue crab Callinectes sapidus to long‐term hypoxia. Biol. Bull. 178: 46–54, 1990.
 22. D'Hondt, J., L. Moens, J. Heip, A. D'Hondt, and M. Kondo. Oxygen binding characteristics of three extracellular haemoglobins of Artemis salina. Biochem. J. 171: 705–710, 1978.
 23. Dixon, B., B. Walker, W. Kimmins, and B. Pohajdak. Isolation and sequencing of a cDNA from an unusual hemoglobin from the parasitic nematode Pseudoterranova decipiens. Proc. Natl. Acad. Sci. U.S.A. 88: 5655–5659, 1991.
 24. Freadman, M. A., and C. P. Mangum. The function of hemoglobin in the arcid clam Noetia ponderosa. I. Oxygenation in vitro and in vivo. Comp. Biochem. Physiol. [A] 53: 173–179, 1976.
 25. Gilchrist, B. M. Haemoglobin in Artemia. Proc. R. Soc. Lond. B 143: 136–146, 1954.
 26. Graham, R. A. A model for l‐lactate binding to Cancer magister hemocyanin. Comp. Biochem. Physiol. [B] 81: 885–887, 1985.
 27. Graham, R. A., C. P. Mangum, R. C. Terwilliger, and N. B. Terwilliger. The effect of organic acids on oxygen binding of hemocyanin from the crab Cancer magister. Comp. Biochem. Physiol. [A] 74: 45–50, 1983.
 28. Hagerman, L. Haemocyanin concentration in the shrimp Crangon crangon (L.) after exposure to moderate hypoxia. Comp. Biochem. Physiol. [A] 85: 721–724, 1986.
 29. Heip, J., L. Moens, M. Joniau, and M. Kondo. Ontogenetical studies on extracellular hemoglobin of Artemia salina. Dev. Biol. 64: 73–81, 1978.
 30. Heip, J., L. Moens, and M. Kondo. Effect of concentrations of salt and oxygen on the synthesis of extracellular hemoglobins during development of Artemia salina. Dev. Biol. 63: 247–251, 1978.
 31. Hessler, R. R., and W. A. Newman. A trilobitomorph origin for the Crustacea. Fossils Strata 4: 437–459, 1975.
 32. Hoffmann, R. J., and C. P. Mangum. The function of coelomic cell hemoglobin in the polychaete Glycera dibranchiata. Comp. Biochem. Physiol. 36: 211–228, 1970.
 33. Horn, E. C., and M. S. Kerr. Hemolymph protein and copper concentrations of adult blue crabs (Callinectes sapidus Rathbun). Biol. Bull. 125: 499–507, 1963.
 34. Imai, K., H. Takizawa, T. Handa, and H. Kihara. Oxygen equilibrium characteristics of hemerythrins from the brachiopod, Lingula unguis, and the sipunculid, Siphonosoma cumanense. In: Structure and Function of Invertebrate Oxygen Carriers, edited by S. N. Vinogradov and O. H. Kapp, Heidelberg: Springer‐Verlag, 1991, pp. 179–189.
 35. Johansen, K., C. Lenfant, and T. A. Mecklenberg. Respiration in the crab, Cancer magister. Z. Vgl. Physiol. 70: 1–19, 1970.
 36. Johnson, B. A., C. Bonaventura, and J. Bonaventura. Allosteric modulation of Callinectes sapidus hemocyanin by binding of l‐lactate. Biochemistry 23: 872–878, 1984.
 37. Jones, J. D. The role of haemoglobin in the aquatic pulmonate, Planorbis corneus. Comp. Biochem. Physiol. 12: 283–296, 1964.
 38. Kobayashi, M., M. Fujiki, and T. Suzuki. Variation in and oxygen‐binding properties of Daphnia magna hemoglobin. Physiol. Zool. 61: 415–419, 1988.
 39. Kobayashi, M., and H. Gonoi. Horizontal movement of pale and red Daphnia magna in low oxygen concentration. Physiol. Zool. 58: 190–196, 1985.
 40. Kobayashi, M., F. Hayakawa, and M. Ninomiya. Hatchability and hemoglobin of Daphnia magna embryo. Physiol. Zool. 60: 507–512, 1987.
 41. Kurtz, D. M. Molecular structure/function relationships of hemerythrins. In: Blood and Tissue Oxygen Carriers, edited by C. P. Mangum, Heidelberg: Springer‐Verlag, 1992, pp. 151–171.
 42. Lallier, F., F. Boitel, and J.‐P. Truchot. The effect of ambient oxygen and temperature on haemolymph l‐lactate and urate concentrations in the shore crab Carcinus maenas. Comp. Biochem. Physiol. [A] 86: 255–260, 1987.
 43. Lallier, F., and J.‐P. Truchot. Hemolymph oxygen transport during environmental hypoxia in the shore crab, Carcinus maenas. Respir. Physiol. 77: 323–336, 1989.
 44. Lallier, F., and P. J. Walsh. Urate does not accumulate in the haemolymph of exercised blue crabs, Callinectes sapidus. J. Exp. Biol. 154: 581–585, 1990.
 45. Lykkeboe, G., and K. Johansen. An O2‐Hb “paradox” in frog blood?. Respir. Physiol. 35: 119–122, 1978.
 46. Mangum, C. P. Primitive respiratory adaptations. In: Adaptation to Environment, edited by R. C. Newell, London: Butterworth, 1976, pp. 191–278.
 47. Mangum, C. P. The annelid hemoglobins: a dichotomy in structure and function. In: Essays in Memory of Dr. Olga Hartman, edited by D. J. Reish and K. Fauchald. Los Angeles: Allan Hancock Found. Spec. Publ. Univ. So. Calif., 1977, pp. 407–428.
 48. Mangum, C. P. A note on blood and water mixing in large marine gastropods. Comp. Biochem. Physiol. [A] 63: 389–391, 1979.
 49. Mangum, C. P. Distribution of respiratory pigments and the role of anaerobic metabolism in the lamellibranch molluscs. In: Animals and Environmental Fitness, edited by R. Gilles. Oxford: Pergamon Press, 1980, pp. 171–184.
 50. Mangum, C. P. On the relationship between P50 and the mode of gas exchange in tropical crustaceans. Pacif. Sci. 36: 403–410, 1982.
 51. Mangum, C. P. Structure and function of invertebrate gills. In: Gills, edited by D. Houlihan and T. Shuttleworth. Cambridge: Cambridge University Press, 1982, pp. 77–98.
 52. Mangum, C. P. The effect of hypoxia on hemocyanin–oxygen binding in the horseshoe crab Limulus polyphemus. Mol. Physiol. 3: 217–224, 1983.
 53. Mangum, C. P. On the distribution of lactate sensitivity among the hemocyanins. Mar. Biol. Lett. 4: 139–149, 1983.
 54. Mangum, C. P. Oxygen transport in the invertebrates. Am. J. Physiol. 248 (Regulatory Integrative Comp. Physiol. 17): R505–R514, 1985.
 55. Mangum, C. P. Adaptability and inadaptability among HcO2 transport systems: an apparent paradox. Life Chem. Rep. Suppl. 1: 335–352, 1984.
 56. Mangum, C. P. The role of physiology and biochemistry in understanding animal phytogeny. Proc. Biol. Soc. Washington 103: 235–247, 1989.
 57. Mangum, C. P. Gas transport in the blood. In: Squid As Experimental Animals, edited by D. L. Gilbert, W. J. Adelman, and J. M. Arnold, Heidelberg: Springer‐Verlag, 1990, pp. 443–468.
 58. Mangum, C. P. Inducible O2 carriers in the crustaceans. In: Animal Nutrition and Transport Processes, edited by J.‐P. Truchot and B. Lalou. Basel: Karger, 1990, vol. 2, pp. 92–103.
 59. Mangum, C. P. Respiratory functions of the red blood cell hemoglobins of six animal phyla. In: Blood and Tissue Oxygen Carriers, edited by C. P. Mangum, Heidelberg: Springer‐Verlag, 1992, pp. 118–149.
 60. Mangum, C. P. Physiological function of the hemerythrins. In: Blood and Tissue Oxygen Carriers, edited by C. P. Mangum, Heidelberg: Springer‐Verlag, 1992, pp. 173–192.
 61. Mangum, C. P. Respiratory function of the molluscan hemocyanins. In: Blood and Tissue Oxygen Carriers, edited by C. P. Mangum, Heidelberg: Springer‐Verlag, 1992, pp. 301–323.
 62. Mangum, C. P. Structural and functional polymorphism of the hemocyanin O2 transport system of the sand fiddler crab, Uca pugilator. J. Exp. Mar. Biol. Ecol. 165: 133–142, 1993.
 63. Mangum, C. P. Hemocyanin subunit composition and oxygen binding in two species of the lobster genus Homarus and their hybrids. Biol. Bull. 184: 105–113, 1993.
 64. Mangum, C. P. Subunit composition of hemocyanin of Callinectes sapidus: Phenotypes from naturally hypoxic waters and isolated oligomers. Comp. Biochem. Physiol. [B] 108: 337–341, 1994.
 65. Mangum, C. P., C. E. Booth, P. L. Defur, N. A. Heckel, R. P. Henry, L. C. Oglesby, and G. Polites. The ionic environment of hemocyanin in Limulus polyphemus. Biol. Bull. 150: 453–467, 1976.
 66. Mangum, C. P., and L. E. Burnett. The CO2 sensitivity of the hemocyanins and its relationship to Cl− sensitivity. Biol. Bull. 171: 248–263, 1986.
 67. Mangum, C. P., and L. E. Burnett. Responses of sipunculid hemerythrin to inorganic ions and CO2. J. Exp. Zool. 244: 59–66, 1987.
 68. Mangum, C. P., and E. M. Cockey. A structural and functional polymorphism in the hemoglobin O2 transport system of the blood clam Noetia ponderosa. J. Exp. Zool. 266: 336–339, 1993.
 69. Mangum, C. P., J. M. Colacino, and J. P. Grassle. Red blood cell oxygen binding in capitellid polychaetes. Biol. Bull. 182: 129–132, 1992.
 70. Mangum, C. P., J. M. Colacino, and T. L. Vandergon. O2 binding by single red blood cells of the anelid bloodworm Glycera dibranchiata. J. Exp. Zool. 249: 166–169, 1989.
 71. Mangum, C. P., and R. P. Dales. Products of haem synthesis in polychaetes. Comp. Biochem. Physiol. 15: 237–257, 1965.
 72. Mangum, C. P., J. Greaves, and J. S. Rainer. 1991. Oligomer composition and oxygen binding of the hemocyanin of the blue crab Callinectes sapidus. Biol. Bull. 181: 453–458, 1991.
 73. Mangum, C. P., and G. Lykkeboe. The influence of inorganic ions and pH on the oxygenation properties of the blood in the gastropod mollusc Busycon canaliculatum. J. Exp. Zool. 207: 417–430, 1979.
 74. Mangum, C. P., B. R. McMahon, P. L. Defur, and M. I. Wheatly. Gas exchange, acid‐base balance and the oxygen supply to the tissues during a molt in the blue crab, Callinectes sapidus Rathbun. J. Crust. Biol. 5: 207–215, 1985.
 75. Mangum, C. P., K. I. Miller, J. L. Scott, K. E. Van Holde, and M. P. Morse. Bivalve hemocyanin: structural, functional and phylogenetic relationships. Biol. Bull. 173: 205–221, 1987.
 76. Mangum, C. P., and G. Polites. Oxygen uptake and transport in the prosobranch mollusc Busycon canaliculatum. I. Gas exchange and the response to hypoxia. Biol. Bull. 158: 77–90, 1980.
 77. Mangum, C. P., and J. Ricci. The influence of temperature on oxygen uptake and transport in the horseshoe crab Limulus polyphemus. J. Exp. Mar. Biol. Ecol. 129: 243–250, 1989.
 78. Mangum, C. P., R. C. Terwilliger, N. B. Terwilliger, and R. Hall. Oxygen binding of intact coelomic cells and extracted hemoglobin of the echiuran Urechis caupo. Comp. Biochem. Physiol. [A] 76: 253–257, 1983.
 79. Mangum, C. P., and A. L. Weiland. The quantitative function of hemocyanin in respiration of the blue crab Callinectes sapidus. J. Exp. Zool. 193: 265–274, 1975.
 80. Mangum, C. P., B. L. Woodin, C. Bonaventura, B. Sullivan, and J. Bonaventura. The role of coelomic and vascular hemoglobins in the annelid family Terebellidae. Comp. Biochem. Physiol. [A] 51: 281–294, 1975.
 81. Manwell, C. Chemistry, genetics, and function of invertebrate respiratory pigments—configurational changes and allosteric effects. In: Oxygen in the Animal Organism, edited by F. Dickens and E. Niel. Oxford: Pergamon Press, 1964, pp. 49–119.
 82. Manwell, C. Superoxide dismutase and NADH diaphorase in haemerythrocytes of sipunculans. Comp. Biochem. Physiol. 58: 331–338, 1977.
 83. Manwell, C., and C.M.A. Baker. Magelona haemerythrin: tissue specificity, molecular weights and oxygen equilibria. Comp. Biochem. Physiol. [B] 89: 453–463, 1988.
 84. Manwell, C., E. C. Southward, and A. M. Southward. Preliminary studies on haemoglobin and other proteins of the Pogonophora. J. Mar. Biol. Assoc. U.K. 46: 115–124, 1966.
 85. Markl, J. Evolution and function of structurally diverse subunits in the respiratory protein hemocyanin from arthropods. Biol. Bull. 171: 90–115, 1986.
 86. Markl, J., and H. Decker. Molecular structure of the arthropod hemocyanins. In: Blood and Tissue Oxygen Carriers, edited by C. P. Mangum, Heidelberg: Springer‐Verlag, 1992, pp. 325–376.
 87. Mason, R. P., C. P. Mangum, and G. Godette. The influence of inorganic ions and acclimation salinity on hemocyanin–oxygen binding in the blue crab Callinectes sapidus. Biol. Bull. 164: 104–123, 1983.
 88. Mauro, N. A., and R. E. Isaacks. Metabolic and functional characteristics of erythrocytes from Glycera and Noetia. Comp. Biochem. Physiol. [A] 88: 397–404, 1987.
 89. Mauro, N. A., and C. P. Mangum. The role of the blood in the temperature dependence of oxidative metabolism in decapod crustaceans. I. Intraspecific responses to seasonal changes in temperature. J. Exp. Zool. 219: 179–188, 1982.
 90. Mauro, N. A., and C. P. Mangum. The role of the blood in the temperature dependence of oxidative metabolism in decapod crustaceans. II. Interspecific adaptation to latitudinal change. J. Exp. Zool. 219: 189–196, 1982.
 91. McMahon, B. R., D. G. McDonald, and C. M. Wood. Ventilation, oxygen uptake and hemolymph oxygen transport following enforced exhausting activity in the Dungeness crab Cancer magister. J. Exp. Biol. 80: 271–285, 1979.
 92. Miller, K. I., and C. P. Mangum. An investigation of the nature of Bohr, Root and Haldane effects in Octopus dofleini hemocyanin. J. Comp. Physiol. [B] 158: 547–552, 1989.
 93. Morris, S. Organic ions as modulators of respiratory pigment function during stress. Physiol. Zool. 63: 253–287, 1990.
 94. Morris, S., and B. R. McMahon. Potentiation of hemocyanin oxygen affinity by catecholamines in the crab Cancer magister: a specific effect of dopamine. Physiol. Zool. 62: 654–667, 1989.
 95. Morris, S., C. R. Bridges, and M. K. Grieshaber. A new role for uric acid: modulator of haemocyanin oxygen affinity in crustaceans. J. Exp. Zool. 235: 135–139, 1985.
 96. Morris, S., C. R. Bridges, and M. K. Grieshaber. The potentiating effect of purine bases and some of their derivatives on the oxygen affinity of haemocyanin from the crayfish Austropotamobius pallipes. J. Comp. Physiol. 156: 431–440, 1986.
 97. Morris, S., C. R. Bridges, and M. K. Grieshaber. The regulation of haemocyanin oxygen affinity during emersion of the crayfish Austropotamobius pallipes. III. The dependence of Ca+2‐haemocyanin binding on the concentration of l‐lactate. J. Exp. Biol. 133: 339–352, 1987.
 98. Morris, S., P. Greenaway, and B. R. McMahon. Oxygen and carbon dioxide transport by the haemocyanin of an amphibious crab, Holothuisana transversa. J. Comp. Physiol. 157: 873–882, 1988.
 99. Morris, S., R. Tyler‐Jones, C. R. Bridges, and E. W. Taylor. The regulation of haemocyanin oxygen affinity during emersion of the crayfish Austropotamobius pallipes. I. An in vitro investigation of the interactive effects of calcium and l‐lactate on oxygen affinity. J. Exp. Biol. 121: 327–337, 1986.
 100. Nicol, P. I., and A. K. O'Gower. Haemoglobin variation in Anadara trapezia. Nature 216: 684, 1967.
 101. Nies, A., B. Zeis, C. R. Bridges, and M. K. Grieshaber. Allosteric modulation of haemocyanin oxygen‐affinity by l‐lactate and urate in the lobster Homarus vulgaris. J. Exp. Biol. 168: 111–124, 1992.
 102. Ochs, R. L., D. C. Ochs, and P. R. Burton. Axons of crayfish nerve cord contain intracellular hemocyanin. J. Cell Biol. 87: 73a, 1980.
 103. Olson, K., N. B. Terwilliger, and J. McDowell. Structure of hemocyanin in larval and adult lobsters. Am. Zool. 28: 47A, 1988.
 104. Padmanabha Naidu, B. Physiological properties of the blood and the haemocyanin of the scorpion, Heterometrus fulvipes. Comp. Biochem. Physiol. 17: 167–181, 1966.
 105. Petersen, J., and K. Johansen. Gas exchange in the giant sea cradle Cryptochiton stelleri (Middendorff). J. Exp. Mar. Biol. Ecol. 12: 27–43, 1973.
 106. Pihl, L., S. P. Baden, and R. J. Diaz. Effects of periodic hypoxia on distribution of demersal fish and crustaceans. Mar. Biol. 108: 349–360, 1991.
 107. Polites, G., and C. P. Mangum. Oxygen uptake and transport in the gastropod mollusc Busycon canaliculatum. II. The influence of temperature and salinity. Biol. Bull. 158: 118–128, 1980.
 108. Poluhowich, J. J. Oxygen consumption and the respiratory pigment in the fresh‐water nemertean Prostoma rubrum. Comp. Biochem. Physiol. 36: 817–821, 1970.
 109. Redfield, A. C., T. Coolidge, and A. L. Hurd. The transport of oxygen and carbon dioxide by some bloods containing hemocyanin. J. Biol. Chem. 69: 475–509, 1926.
 110. Redfield, A. C., and R. Goodkind. The significance of the Bohr effect in the respiration and asphyxiation of the squid, Loligo pealei. J. Exp. Biol. 6: 340–349, 1929.
 111. Redmond, J. R. The respiratory function of hemocyanin. In: Physiology and Biochemistry of Haemocyanins, edited by F. Ghiretti. London: Academic Press, 1966, pp. 5–23.
 112. Roberts, M. S., R. C. Terwilliger, and N. B. Terwilliger. Comparison of sea cucumber hemoglobin structures. Comp. Biochem. Physiol. 77B: 237–243, 1984.
 113. Royer, W. E. Structures of red blood cell hemoglobins. In: Blood and Tissue Oxygen Carriers, edited by C. P. Mangum, Heidelberg: Springer‐Verlag, 1992, pp. 87–116.
 114. Ruppert, E. E. and M. E. Rice. Microanatomy and ultrastructure of subepidermal coelomic canals in Sipunculus nudus (Sipuncula). Am. Zool. 30: 115A, 1990.
 115. Sanders, N. K., S. Morris, J. J. Childress, and B. R. McMahon. Effects of ammonia, trimethylamine, l‐lactate and CO2 on some decapod crustacean haemocyanins. Comp. Biochem. Physiol. [A] 101: 511–516, 1992.
 116. Scholnick, D. A., and C. P. Mangum. The sensitivity of the elasmobranch hemoglobins to intracellular effectors: primitive and derived features. J. Exp. Zool. 259: 32–42, 1991.
 117. Shishikura, F., J. W. Snow, T. Gotoh, S. N. Vinogradov, and D. A. Walz. Amino acid sequence of the monomer subunit of the extracellular hemoglobin of Lumbricus terrrestris. J. Biol. Chem. 262: 3123–3131, 1987.
 118. Smith, D. M., and W. Dall. Blood protein, blood volume, and extracellular space relationships in two Penaeus spp. (Decapoda: Crustacea). J. Exp. Mar. Biol. Ecol. 63: 1–15, 1982.
 119. Smith, M. H., and D. L. Lee. Metabolism of haemoglobin and haematin compounds in Ascaris lumbricoides. Proc. R. Soc. B 157: 234–257, 1963.
 120. Snyder, G. K. Erythrocyte evolution: the significance of the Fahraeus‐Lindqvist phenomenon. Respir. Physiol. 19: 271–278, 1973.
 121. Snyder, G. K. Blood viscosity in annelids. J. Exp. Zool. 206: 271–277, 1978.
 122. Snyder, G. K., and C. P. Mangum. The relationship between the size and shape of an extracellular oxygen carrier and the capacity for oxygen transport. In: Physiology and Biology of Horseshoe Crabs, edited by J. Bonaventura, C. Bonaventura, and S. Tesh. New York, Allan Liss Co., 1982, pp. 173–188.
 123. Southward, E. C. Development of the gut and segmentation of the newly settled stages of Ridgeia (Vestimentifera): implications for relationship between Vestimentifera and Pogonophora. J. Mar. Biol. Assoc. U.K. 68: 465–487, 1988.
 124. Spicer, J. I., and B. R. McMahon. Haemocyanin oxygen binding and the physiological ecology of a range of talitroidean amphipods (Crustacea) I. PH, temperature, and l‐lactate sensitivity. J. Comp. Physiol. [B] 160: 195–200, 1990.
 125. Spindler, K. D., R. Hennecke, and G. Gellissen. Protein production and the molting cycle in the crayfish Astacus leptodactylus (Nordmann, 1842). II. Hemocyanin and protein synthesis in the midgut gland. Gen. Comp. Endocrinol. 85: 248–253, 1992.
 126. Stocker, W., U. Raeder, M.M.C. Bijlholt, T. Wichertjes, E.J.F. Van Bruggen, and J. Markl. The quaternary structure of four crustacean two‐hexameric hemocyanins: immunocorrelation, stoichiometry, reassembly and topology of individual subunits. J. Comp. Physiol. [B] 158: 271–289, 1988.
 127. Storch, V., R. P. Higgins, and M. P. Morse. Ultrastructure of the body wall of Meiopriapulus fijiensis. Trans. Am. Microsc. Soc. 100: 319–331, 1989.
 128. Suzuki, T., and T. Gotoh. The complete amino acid sequence of giant multisubunit hemoglobin from the polychaete Tylorrhynchus heterocbaetus. J. Biol. Chem. 261: 9257–9267, 1986.
 129. Suzuki, T., T. Tagaki and S. Ohta. N‐terminal amino acid sequences of the deep‐sea tube worm haemoglobin remarkably resembles that of annelid haemoglobin. Biochem. J. 255: 541–545, 1988.
 130. Suzuki, T., T. Tagaki, and S. Ohta. Primary structure of a linker subunit of the tube worm 3000 kDa hemoglobin. J. Biol. Chem. 265: 1531–1535, 1990.
 131. Taylor, E. W. Control and co‐ordination of ventilation and circulation in crustaceans: responses to hypoxia and exercise. J. Exp. Biol. 100: 289–319, 1982.
 132. Taylor, E. W., and N. M. Whiteley. Oxygen transport and acid‐base balance in the haemolymph of the lobster, Homarus gammarus, during aerial exposure and resubmersion. J. Exp. Biol. 144: 417–436, 1989.
 133. Terwilliger, N. B. Molecular structure of the extracellular heme proteins. In: Blood and Tissue Oxygen Carriers, edited by C. P. Mangum, Heidelberg: Springer‐Verlag, 1992, pp. 193–229.
 134. Terwilliger, N. B., N. Sanders, R. Griffis, and K. O. O'Brien. Hemocyanin structure and function in Callianassa californiensis from Baja to Bamfield. Am. Zool. 31: 72A, 1991.
 135. Terwilliger, N. B., and R. C. Terwilliger. Oxygen binding domains of a clam (Cardita borealis) extracellular hemoglobin. Biochim. Biophys. Acta 537: 77–85, 1978.
 136. Terwilliger, N. B., and R. C. Terwilliger. Changes in the subunit structure of Cancer magister hemocyanin during larval development. J. Exp. Zool. 221: 181–192, 1982.
 137. Terwilliger, N. B., R. C. Terwilliger, and E. Schabtach. The quaternary structure of a molluscan (Helisoma trivolvis) extracellular hemoglobin. Biochem. Biophys. Acta 453: 101–110, 1976.
 138. Terwilliger, R. C., R. L. Garlick, and N. B. Terwilliger. Characterization of the hemoglobins and myoglobin of Travisia foetida. Comp. Biochem. Physiol. [B] 66: 261–266, 1980.
 139. Terwilliger, R. C. and N. B. Terwilliger. Molluscan hemoglobins. Comp. Biochem. Physiol. 81B: 255–261, 1985.
 140. Terwilliger, R. C., N. B. Terwilliger, C. Bonaventura, J. Bonaventura, and E. Schabtach. Structural and functional properties of hemoglobin from the vestimentiferan Pogonophora, Lamellibrachia. Biochim. Biophys. Acta 829: 27–33, 1985.
 141. Terwilliger, R. C., N. B. Terwilliger, G. M. Hughes, A. J. Southward, and E. C. Southward. Studies of the haemoglobin of the small Pogonophora. J. Mar. Biol. Assoc. U.K. 67: 219–234, 1987.
 142. Terwilliger, R. C., N. B. Terwilliger, and E. Schabtach. Comparison of chlorocruorin and annelid hemoglobin quaternary structures. Comp. Biochem. Physiol. [A] 55: 51–55, 1976.
 143. Terwilliger, R. C., N. B. Terwilliger, and E. Schabtach. The structure of hemoglobin from an unusual deep sea worm (Vestimentifera). Comp. Biochem. Physiol. [B] 65: 531–536, 1980.
 144. Toulmond, A. Tide‐related changes of blood respiratory variables in the lugworm Arenicola marina (L.). Respir. Physiol. 19: 130–144, 1973.
 145. Toulmond, A. Properties and functions of extracellular heme pigments. In: Blood and Tissue Oxygen Carriers, edited by C. P. Mangum, Heidelberg: Springer‐Verlag, 1992, pp. 231–256.
 146. Trewitt, P., D. Saffarini, and G. Bergtrom. Multiple clustered genes of the haemoglobin VIIB subfamily of Chironomus thummi thummi (Diptera). Gene 69: 91–100, 1988.
 147. Truchot, J.‐P. Factors controlling the in vitro and in vivo oxygen affinity of the hemocyanin of the crab, Carcinus maenas (L.). Respir. Physiol. 24: 173–189, 1975.
 148. Truchot, J.‐P. Lactate increases the oxygen affinity of crab hemocyanin. J. Exp. Zool. 214: 205–208, 1980.
 149. Truchot, J.‐P. Respiratory function of arthropod hemocyanins. In: Blood and Tissue Oxygen Carriers, edited by C. P. Mangum, Heidelberg: Springer‐Verlag, 1992, pp. 377–410.
 150. van den Branden, C., J. D'Hondt, L. Moens, and W. Decleir. Functional properties of the hemoglobins of Artemia salina L. Comp. Biochem. Physiol. [A] 60: 185–188, 1978.
 151. van Holde, K. E., K. I. Miller, and W. H. Lang. Molluscan hemocyanins: structure and function. In: Blood and Tissue Oxygen Carriers, edited by C. P. Mangum, Heidelberg: Springer‐Verlag, 1992, pp. 258–300.
 152. Vinogradov, S. N. The structure of invertebrate extracellular hemoglobins (erythrocruorins and chlorocruorins). Comp. Biochem. Physiol. [B] 82: 1–16, 1985.
 153. Vinogradov, S. N., S. D. Long, M. G. Mainwaring, O. H. Kapp, and A. V. Crewe. Bracelet protein: a quaternary structure proposed for the giant extracellular hemoglobin of Lumbricus terrestris. Proc. Natl. Acad. Sci. U.S.A. 83: 8034–8038, 1986.
 154. Vinogradov, S. N., P. K. Sharma, and D. A. Walz. Iron and heme contents of the extracellular hemoglobins and chlorocruorins of annelids. Comp. Biochem. Physiol. [B] 98: 187–194, 1991.
 155. Vinson, C. R., and J. Bonaventura. Structure and oxygen equilibrium of the three coelomic cell hemoglobins of the echiuran worm Thalassema melitta (Conn). Comp. Biochem. Physiol. [B] 87: 361–366, 1987.
 156. Vismann, B. Sulfide detoxification and tolerance in Nereis (Hediste) diversicolor and Nereis (Neanthes) virens (Annelida: Polychaeta). Mar. Ecol. Progr. Ser. 59: 229–238, 1990.
 157. Wache, S., N. B. Terwilliger, and R. C. Terwilliger. Hemocyanin structure changes during early development of the crab Cancer productus. J. Exp. Zool. 247: 23–32, 1988.
 158. Weber, R. E. Functions of invertebrate hemoglobins with special reference to environmental hypoxia. Am. Zool. 20: 79–102, 1980.
 159. Weber, R. E. Cationic control of O2 affinity in lugworm erythrocruorin. Nature 292: 386–387, 1981.
 160. Weber, R. E., G. Braunitzer, and T. Kleinschmidt. Functional multiplicity and structural correlations in the hemoglobin system of larvae of Chironomus thummi thummi (Insecta: Diptera): Hb components CTT I, CTT II, CTT III, CTT IV, CTT VI, CTT VIIB, CTT IX and CTT X. Comp. Biochem. Physiol. [B] 80: 747–753, 1985.
 161. Weber, R. E., R. Fange, and K. K. Rasmussen. Respiratory significance of priapulid hemerythrin. Mar. Biol. Lett. 1: 87–97, 1979.
 162. Wells, R.M.G. Hemoglobin physiology in vertebrate animals: a cautionary approach to adaptationist thinking. In: Vertebrate Gas Exchange, edited by R. G. Boutilier, Heidelberg: Springer‐Verlag, 1990, pp. 143–161.
 163. Wells, R. M.G. and R. P. Dales. The respiratory significance of chlorocruorin. In: Proc. 9th Eur. Mar. Biol. Symp., edited by H. Barnes. Aberdeen: Aberdeen University Press, 1975, pp. 673–681.
 164. Wells, R.M.G. and R. P. Dales. A preliminary investigation into the oxygen‐combining properties of pogonophore haemoglobin. Comp. Biochem. Physiol. [A] 54: 395–396, 1976.
 165. Wieser, W. Temperature Adaptation in Homeothermic Organisms Heidelberg: Springer‐Verlag, 1973.
 166. Wilkins, R. G. and P. C. Harrington. The chemistry of hemerythrin. Adv. Inorg. Biochem. 5: 51–85, 1983.
 167. Wittenberg, J. B. Functions of cytoplasmic hemoglobins and myohemerythrin. In: Blood and Tissue Oxygen Carriers, edited by C. P. Mangum, Heidelberg: Springer‐Verlag, 1992, pp. 60–85.
 168. Yano, H., K. Satake, Y. Ueno, K. Kondo, and A. Tsugita. Amino acid sequence of the hemerythrin alpha subunit from Lingula unguis. J. Biochem. 110: 376–380, 1991.
 169. Zatta, P. The relationship between plasma proteins and intracellular free amino acids during osmotic regulation in Carcinus maenas. J. Exp. Zool. 242: 131–136, 1987.
 170. Zeis, B., A. Nies, C. R. Bridges, and M. K. Grieshaber. Allosteric modulation of haemocyanin oxygen affinity by l‐lactate and urate in the lobster Homarus vulgaris. I. Specific and additive effects on haemocyanin—oxygen affinity. J. Exp. Biol. 168: 93–110, 1992.
 171. Zhang, J.‐H., and D. M. Kurtz. Two distinct subunits of hemerythrin from the brachiopod Lingula reevii: an apparent requirement for cooperativity in O2 binding. Biochemistry 30: 9121–9125, 1991.

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Charlotte P. Mangum. Invertebrate Blood Oxygen Carriers. Compr Physiol 2011, Supplement 30: Handbook of Physiology, Comparative Physiology: 1097-1135. First published in print 1997. doi: 10.1002/cphy.cp130215