Decline in pelagic cephalopod metabolism with habitat depth reflects differences in locomotory efficiency

Biological Bulletin

Volumn 192, Issue 2, 1997, Pages 262-278

  Seibel, Brad A ^a   Thuesen, Erik V ^a,b   Childress, James J ^a   Gorodezky, Laura A ^a,c  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b EVERGREEN STATE COLLEGE   (United States)

^c Channel Islands National Marine Sanctuary   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMALIA; CEPHALOPODA; CRUSTACEA; GONATUS ONYX; HAWAIIA; JAPETELLA HEATHI; OCTOPODA; ONYX; PISCES; VAMPYROTEUTHIS INFERNALIS;

EID: 0031006682     PISSN: 00063185     EISSN: None     Source Type: Journal    
DOI: 10.2307/1542720     Document Type: Article

References (91)

1. Aldred, R. G., M. Nixon, and J. Z. Young. 1983. Cirrothauma murrayi Chun, a finned octopod. Philos. Trans. R. Soc. Lond. B 301: 1-54.
2. Alexander, R. M. 1990. Size, speed and buoyancy adaptations in aquatic animals. Am. Zool. 30: 189-196.
3. Baldwin, J. 1982. Correlations between enzyme profiles in cephalopod muscle and swimming behavior. Pac. Sci. 36: 349-356.
4. Belman, B. 1978. Respiration and the effects of pressure on the mesopelagic vertically migrating squid Histioteuthis heteropsis. Limnol. Oceanogr. 23: 735-739.
5. Belman, B. W., and J. J. Childress. 1976. Circulatory adaptations to the oxygen minimum layer in the bathypelagic mysid Gnathophausia ingens. Biol. Bull. 150: 15-37.
6. Boletzky, S. V., M. Rio, and M. Roux. 1992. Octopod 'ballooning' response. Nature 356: 199.
7. Boucher-Rodoni, R., and K. Mangold. 1989. Respiration and nitrogen excretion by the squid Loligo forbesi. Mar. Biol. 103: 333-338.
8. Boutilier, R. G., T. G. West, G. H. Pogson, K. A. Mesa, J. Wells, and M. J. Wells. 1996. Nautilus and the art of metabolic maintenance. Nature 382: 534-536.
9. Brix, O., A. Bardgard, A. Cau, A. Colosimo, S. G. Condo, and B. Giardina. 1989. Oxygen-binding properties of cephalopod blood with special reference to environmental temperatures and ecological distribution. J. Exp. Zool. 252: 34-42.
10. Carey, F. G., and B. H. Robison. 1980. Daily patterns in the activities of swordfish, Xiphias gladius, observed by acoustic telemetry. Fish. Bull. 79: 277-292.
11. Castellini, M. A., and G. N. Somero. 1981. Buffering capacity of vertebrate muscle: correlations with potentials for anaerobic function. J. Comp. Physiol. 143: 191-198.
12. Childress, J. J. 1968. Oxygen minimum layer: vertical distribution and respiration of the mysid Gnathophausia ingens. Science 160: 1242-1243.
13. Childress, J. J. 1971a. Respiratory adaptations to the oxygen minimum layer in the bathypelagic mysid Gnathophausia ingens. Biol. Bull. 141: 109-121.
14. Childress, J. J. 1971b. Respiratory rate and depth of occurrence of midwater animals. Limnol. Oceanogr. 16: 104-106.
15. Childress, J. J. 1975. The respiratory rates of midwater crustaceans as a function of depth occurrence and relation to the oxygen minimum layer off Southern California. Comp. Biochem. Physiol. 50A: 787-799.
16. Childress, J. J. 1995. Are there physiological and biochemical adaptations of metabolism in deep-sea animals? Trends Ecol. Evol. 10: 30-36.
17. Childress, J. J., and T. J. Mickel. 1980. A motion compensated shipboard precision balance system. Deep-Sea Res. 27A: 965-970.
18. Childress, J. J., and T. J. Mickel. 1985. Metabolic rates of animals from the hydrothermal vents and other deep-sea habitats. Biol. Soc. Wash. Bull. 6: 249-260.
19. Childress, J. J., and M. H. Nygaard. 1974. The chemical composition and relative buoyancy of midwater crustaceans as a function of depth off Southern California. Mar. Biol. 27: 225-238.
20. Childress, J. J., and G. N. Somero. 1979. Depth related enzymic activities in muscle, brain and heart of deep-living pelagic marine teleosts. Mar. Biol. 52: 273-283.
21. Childress, J. J., and E. V. Thuesen. 1993. The effect of hydrostatic pressure on the metabolic rates of six species of gelatinous zooplankton. Limnol. Oceanogr. 38: 665-670.
22. Childress, J. J., A. T. Barnes, L. B. Quetin, and B. H. Robison. 1978. Thermally protecting cod ends for recovery of living deep-sea animals. Deep-Sea Res. 25: 419-422.
23. Childress, J. J., D. L. Cowles, J. A. Favuzzi, and T. J. Mickel. 1990. Metabolic rates of benthic deep-sea decapod crustaceans decline with increasing depth primarily due to the decline in temperature. Deep-Sea Res. 37: 929-949.
24. Clarke, A., M. R. Clarke, L. J. Holmes, and T. D. Waters. 1985. Calorific values and elemental analysis of eleven species of oceanic squids (Mollusca: Cephalopoda). J. Mar. Biol. Assoc. U.K. 65: 983-986.
25. Clarke, M. R. 1962. Respiratory and swimming movements in the cephalopod Cranchia scabra. Nature 196: 351-352.
26. Clarke, M. R. 1988. Evolution of buoyancy and locomotion in recent cephalopods. Mollusca 12: 203-213.
27. Clarke, M. R., E. J. Denton, and J. B. Gilpin-Brown. 1979. On the use of ammonium for buoyancy in squids. J. Mar. Biol. Assoc. U.K. 59: 259-276.
28. Cole, S. K., and D. L. Gilbert. 1970. Jet propulsion of squid. Biol. Bull. 138: 245-246.
29. Cowles, D. L., and J. J. Childress. 1988. Swimming speed and oxygen consumption in the bathypelagic mysid Gnathophausia ingens. Biol. Bull. 175: 111-121.
30. Cowles, D. L., and J. J. Childress. 1996. Aerobic metabolism of the anglerfish Melanocetus johnsoni, a deep-pelagic marine sit-and-wait predator. Deep-Sea Res. 42: 1631-1638.
31. Cowles, D. C., J. J. Childress, and M. E. Wells. 1991. Metabolic rates of midwater crustaceans as a function of depth of occurrence off the Hawaiian Islands: food availability as a selective factor? Mar. Biol. 110: 75-83.
32. DeMont, M. E., and R. K. O'Dor. 1984. The effects of activity, temperature and mass on the respiratory metabolism of the squid, Illex illecebrosus. J. Mar. Biol. Assoc. U.K. 64: 535-543.
33. Denton, E. J., and J. B. Gilpin-Brown. 1973. Floatation mechanisms in modern and fossil cephalopods. Adv. Mar. Biol. 11: 197-268.
34. Donnelly, J., and J. J. Torres. 1988. Oxygen consumption of midwater fishes and crustaceans from the eastern Gulf of Mexico. Mar. Biol. 97: 483-494.
35. Eberlee, J. C., and K. B. Storey. 1984. Buffering capacities of the tissues of marine molluscs. Physiol. Zool. 57: 567-572.
36. Finke, E., H. O. Portner, P. G. Lee, and D. M. Webber. 1996. Squid (Lolliguncula brevis) life in shallow waters: oxygen limitation of metabolism and swimming performance. J. Exp. Biol. 199: 911-921.
37. Fischer, A. G., and D. J. Bottjer. 1995. Oxygen-depleted waters: a lost biotope and its role in ammonite and bivalve evolution. N. Jb. Geol. Palaont. Abh. 195: 133-146.
38. Fleisher, K. J., and J. F. Case. 1995. Cephalopod predation facilitated by dinoflagellate luminescence. Biol. Bull. 189: 263-271.
39. Grieshaber, M., and G. Gäde. 1976. The biological role of octopine in the squid, Loligo vulgaris (Lamarck). J. Comp. Physiol. 108: 225-232.
40. Harvey, P. H., and M. D. Pagel. 1991. The Comparative Method in Evolutionary Biology. Oxford University Press, New York. 239 pp.
41. Herring, P. J., P. N. Dilly, and C. Cope. 1994. The bioluminescent organs of the deep-sea cephalopod Vampyroteuthis infernalis (Cephalopoda: Vampyromorpha). J. Zool. Lond. 223: 45-55.
42. Hoar, J. A., E. Sim, D. M. Webber, and R. K. O'Dor. 1994. The role of fins in the competition between squid and fish. Pp. 27-43 in Mechanics and Physiology of Animal Swimming. L. Maddock, Q. Bone, and J. M. V. Rayner, eds. Cambridge University Press, New York.
43. Ikeda, T. 1988. Metabolism and chemical composition of crustaceans from the Antarctic mesopelagic zone. Deep-Sea Res. 35: 1991-2002.
44. Kerfoot, W. B. 1970. Bioenergetics of vertical migration. Am. Nat. 104: 529-546.
45. Lu, C. C., and C. F. E. Roper. 1979. Cephalopods from deepwater dumpsite 106 (western Atlantic): vertical distribution and seasonal abundance. Smithson. Contrib. Zool. 288: 1-36.
46. Madan, J. J., and M. J. Wells. 1996. Why squid breathe easy. Nature 380: 590.
47. Marshall, N. B. 1979. Developments in Deep-Sea Biology. Blandford Press, Poole, England. 566 pp.
48. McFall-Ngai, M. J. 1990. Crypsis in the pelagic environment. Am. Zool. 30: 175-178.
49. Mickel, T. J., L. B. Quetin, and J. J. Childress. 1983. Construction of a polarographic oxygen sensor in the laboratory. Pp. 81-89 in Polarographic Oxygen Sensors. E. Gnaiger and H. Forstner, eds. Springer-Verlag, Berlin.
50. Nixon, M. 1983. Teuthowenia megalops. Pp. 233-247 in Cephalopod Life Cycles. P. R. Boyle, ed. Academic Press, London.
51. O'Dor, R. K. 1982. The respiratory metabolism and swimming performance of the squid, Loligo opalescens. Can. J. Aquat. Sci. 39: 580-587.
52. O'Dor, R. K. 1992. Big squid in big currents. S. Afr. J. Mar. Sci. 12: 225-235.
53. O'Dor, R. K., and R. E. Shadwick. 1989. Squid, the olympic cephalopods. J. Ceph. Biol. 1: 33-54.
54. O'Dor, R. K., and D. M. Webber. 1986. The constraints on cephalopods: why squid aren't fish. Can. J. Zool. 64: 1591-1605.
55. O'Dor, R. K., and D. M. Webber. 1991. Invertebrate athletes: trade-offs between transport efficiency and power density in cephalopod evolution. J. Exp. Biol. 160: 93-112.
56. O'Dor, R. K., J. Wells, and M. J. Wells. 1990. Speed, jet pressure, and oxygen consumption relationships in free-swimming Nautilus. J. Exp. Biol. 154: 383-396.
57. Packard, A. 1972. Cephalopods and fish: the limits of convergence. Biol. Rev. 47: 241-307.
58. Pickford, G. E. 1946. Vampyroteuthis infernalis Chun, an archaic di-branchiate cephalopod, I: Natural history and distribution. Dana-Rep. 29: 1-40.
59. Pickford, G. E. 1952. The Vampyromorpha of the Discovery expeditions. Discovery Rep. 26: 197-210.
60. Portner, H. O., D. M. Webber, R. K. O'Dor, and R. G. Boutilier. 1993. Metabolism and energetics in squid (Illex illecebrosus, Loligo pealei) during muscular fatigue and recovery. Am. J. Physiol. 265: R157-R165.
61. Roper, C. F. E. 1969. Systematics and zoogeography of the worldwide bathypelagic squid Bathyteuthis (Cephalopoda: Oegopsida). U. S. Nat. Mus. Bull. Washington D.C. 291.
62. Roper, C. F. E., and R. E. Young. 1975. Vertical distribution of pelagic cephalopods. Smithson. Contrib. Zool. 209: 1-51.
63. Roper, C. F. E., M. J. Sweeney, and C. E. Nauen. 1984. FAO Species Catalogue. Vol. 3. Cephalopods of the World. An Annotated and Illustrated Catalogue of Species of Interest to Fisheries. 277 pp.
64. Sanders, N. K., and J. J. Childress. 1990. Adaptations to the deep-sea oxygen minimum layer: oxygen binding by the hemocyanin of the bathypelagic mysid, Gnathophausia ingens Dohrn. Biol. Bull. 178: 286-294.
65. Schmidt-Nielsen, K. 1983. Animal Physiology: Adaptation and Environment. Cambridge University Press, Cambridge. 619 pp.
66. Seapy, R. R., and R. E. Young. 1986. Concealment in epipelagic pterotracheid heteropods (Gastropoda) and cranchiid squids (Cephalopoda). J. Zool. 210: 137-147.
67. Seibel, B. A., and J. J. Childress. 1996. Deep-breathing cephalopods? Nature 384: 421.
68. Smith, K. L., and R. R. Hessler. 1974. Respiration of benthopelagic fishes: in situ measurements at 1230 m. Science 184: 72-73.
69. Sullivan, K. M., and G. N. Somero. 1980. Enzyme activities of fish skeletal muscle and brain as influenced by depth of occurrence and habits of feeding and locomotion. Mar. Biol. 60: 91-99.
70. Sweeney, M. J., C. F. E. Roper, K. M. Mangold, M. R. Clarke, and S. V. Boletzky. 1992. "Larval" and juvenile cephalopods: a manual for their identification. Smithson. Contrib. Zool. 513: 282.
71. Thuesen, E. V., and J. J. Childress. 1993a. Enzymatic activities and metabolic rates of pelagic chaetognaths: lack of depth-related declines. Limnol. Oceanogr. 38: 935-948.
72. Thuesen, E. V., and J. J. Childress. 1993b. Metabolic rates, enzyme activities, and chemical compositions of some deep-sea pelagic worms, particularly Nectonemertes mirabilis (Nemertea; Hoplonemertinea) and Poeobius meseres (Annelida; Polychaeta). Deep-Sea Res. I 40: 937-951.
73. Thuesen, E. V., and J. J. Childress. 1994. Respiratory rates and metabolic enzyme activities of oceanic California medusae in relation to body size and habitat depth. Biol. Bull. 187: 84-98.
74. Torres, J. J., and G. N. Somero. 1988. Vertical distribution and metabolism in antarctic mesopelagic fishes. Comp. Biochem. Physiol. 90B: 521-528.
75. Torres, J. J., B. W. Belman, and J. J. Childress. 1979. Oxygen consumption rates of midwater fishes as a function of depth of occurrence. Deep-Sea Res. 26A: 185-197.
76. Vecchione, M., and C. F. E. Roper. 1991. Cephalopods observed from submersibles in the Western North Atlantic. Bull. Mar. Sci. 49: 433-445.
77. Vecchione, M., B. H. Robison, and C. F. E. Roper. 1992. A tale of two species: tail morphology in paralarval Chiroteuthis (Cephalopoda: Chiroteuthidae). Proc. Biol. Soc. Wash. 105(4): 683-692.
78. Voight, J. R., H. O. Portner, and R. K. O'Dor. 1994. A review of ammonia-mediated buoyancy in squids (Cephalopoda: Teuthoidea). Mar. Fresh. Behav. Physiol. 25: 193-203.
79. Vogel, S. 1994. Life in Moving Fluids. Second Edition. Princeton University Press, Princeton. 467 pp.
80. Voss, G. L. 1967. The biology and bathymetric distribution of deep-sea cephalopods. Stud. Trop. Oceanogr. 5: 511-535.
81. Voss, N. A., and R. S. Voss. 1983. Phylogenetic relationships in the cephalopod family Cranchiidae (Oegopsida). Malacologia 23(2): 397-426.
82. Wells, M. J. 1988. Oxygen extraction and jet propulsion in cephalopods. Can. J. Zool. 68: 815-824.
83. Wells, M. J., and R. K. O'Dor. 1991. Jet propulsion and the evolution of the cephalopods. Bull. Mar. Sci. 49: 419-432.
84. Wells, M. J., J. Wells, and R. K. O'Dor. 1992. Life at low oxygen tensions: the behaviour and physiology of Nautilus pompilius and the biology of extinct forms. J. Mar. Biol. Assoc. U.K. 72: 313-328.
85. Wormuth, J. H. 1976. The biogeography and numerical taxonomy of the oegopsid squid family Ommastrephidae in the Pacific Ocean. Bull. Scripps Inst. Oceanogr. Univ. Calif. 23.
86. Young, R. E. 1972. The systematics and areal distribution of pelagic cephalopods from the seas off southern California. Smithson. Contrib. Zool. 97: 1-159.
87. Young, R. E. 1975a. Leachia pacifica (Cephalopoda, Teuthoidea): spawning habitat and function of the brachial photophores. Pac. Sci. 29: 19-25.
88. Young, R. E. 1975b. Transitory eye shapes and the vertical distribution of two midwater squids. Pac. Sci. 29: 243-255.
89. Young, R. E. 1978. Vertical distribution and photosensitive vesicles of pelagic cephalopods from Hawaiian waters. Fish. Bull. 76: 583-615.
90. Young, R. E., E. M. Kampa, S. D. Maynard, F. M. Mencher, and C. F. E. Roper. 1980. Counterillumination and the upper depth limits of midwater animals. Deep-Sea Res. 27A: 671-691.
91. Zammit, V. A. 1978. Possible relationship between energy metabolism of muscle and oxygen binding characteristics of haemocyanin of cephalopods. J. Mar. Biol. Assoc. U.K. 58: 421-424.