The rate of metabolism in marine animals: Environmental constraints, ecological demands and energetic opportunities

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 362, Issue 1487, 2007, Pages 2061-2078

  Seibel, Brad A ^a   Drazen, Jeffrey C ^b  

^a UNIVERSITY OF RHODE ISLAND   (United States)

^b UNIVERSITY OF HAWAII   (United States)

Author keywords

Deep sea; Locomotion; Marine; Metabolism; Oxygen consumption; Scaling

Indexed keywords

ABYSSAL ORGANISM; BIOENERGETICS; DEEP SEA; ENVIRONMENTAL CONSTRAINT; LOCOMOTION; MARINE ECOSYSTEM; METABOLISM; OXYGEN CONSUMPTION; PREDATOR;

ANIMALIA;

EID: 35848944899     PISSN: 09628436     EISSN: None     Source Type: Journal    
DOI: 10.1098/rstb.2007.2101     Document Type: Article

References (182)

1. Angel, M. V. 1989 Does mesopelagic biology affect the vertical flux? In Productivity of the ocean: present and past (eds W. H. Berger, V. S. Smetacek & G. Wefer), pp. 155-173. New York, NY: Wiley.
2. Angel, M. V. & Baker, A. C. 1982 Vertical distribution of the standing crop of plankton and micronekton at three stations in the northeast Atlantic. Biol. Oceanogr. 2, 1-30.
3. Aksnes, D. L. & Giske, J. 1993 A theoretical model of aquatic visual feeding. Ecol. Model. 67, 233-250. (doi:10.1016/0304-3800(93) 90007-F)
4. Aksnes, D. L., Nejstgaard, J., Soedberg, E. & Sornes, T. 2004 Optical control of fish and zooplankton populations. Limnol. Oceanogr. 49, 233-238.
5. Arkhipkin, A. & Bizikov, V. 1996 Possible imitation of jellyfish by the squid paralarvae of the family Gonatidae (Cephalopoda, Oegopsida). Polar Biol. 16, 531-534.
6. Bailey, T. G. & Robison, B. H. 1986 Food availability as a selective factor on the chemical compositions of midwater fishes in the eastern North Pacific. Mar. Biol. 91, 131-141. (doi:10.1007/BF00397578)
7. Bailey, T. G., Torres, J. J., Youngbluth, M. J. & Owen, G. P. 1994 Effect of decompression on mesopelagic gelatinous zooplankton: a comparison of in situ and shipboard measurements of metabolism. Mar. Ecol. Prog. Ser. 113, 12-27.
8. Bailey, D. M., Jamieson, A. J., Bagley, P. M., Collins, M. A. & Priede, I. G. 2002 Measurement of in situ oxygen consumption of deep-sea fish using an autonomous lander vehicle. Deep Sea Res. I 49, 1519-1529. (doi:10.1016/S0967-0637(02)00036-5)
9. Bailey, D. M., Bagley, P. M., Jamieson, A. J., Collins, M. A. & Priede, I. G. 2003 In situ investigation of burst swimming and muscle performance in the deep-sea fish Antimora rostrata. J. Exp. Mar. Biol. Ecol. 285-286, 295-311. (doi:10.1016/S0022-0981(02)00534-8)
10. Bailey, D. M., Bagley, P. M., Jamieson, A. J., Cromarty, A., Collins, M. A., Tselepidis, A. & Priede, I. G. 2005 Life in a warm deep sea: routine activity and burst swimming performance of the shrimp Acanthephyra eximia in the abyssal Mediterranean. Mar. Biol. 146, 1199-1206. (doi:10.1007/s00227-004-1525-1)
11. Barham, E. G. 1971 Deep-sea fishes: lethargy and vertical orientation. In Proc. Int. Symp. Biological Sound Scattering in the Ocean (ed. G. B. Farquhar), pp. 100-118. Washington, DC: Superintendent of Documents.
12. Bartol, I. K., Mann, R. & Patterson, M. R. 2001 Aerobic respiratory costs of swimming in the negatively buoyant brief squid Lolliguncula brevis. J. Exp. Biol. 204, 3639-3653.
13. Belman, B. W. 1978 Respiration and the effects of pressure on the mesopelagic vertically migrating squid Histioteuthis heteropsis. Limnol. Oceanogr. 23, 735-739.
14. Belman, B. W. & Gordon, M. S. 1979 Comparative studies on the metabolism of shallow-water and deep-sea marine fishes. 5. Effects of temperature and hydrostatic pressure on oxygen consumption in the mesopelagic Melanostigma pammelas. Mar. Biol. 50, 275-281. (doi:10.1007/BF00394209)
15. Bennett, A. F. 1991 The evolution of activity capacity. J. Exp. Biol. 160, 1-23.
16. Bernal, D., Dickson, K. A., Shadwick, R. E. & Graham, J. B. 2001 Review: analysis of the evolutionary convergence for high performance swimming in lamnid sharks and tunas. Comp. Biochem. Physiol. A 129, 695-726.
17. Block, B. A. & Stevens, E. D. 2001 Tuna physiology, ecology and evolution. London, UK: Academic Press.
18. Block, B. A., Costa, D. P., Boehlert, G. W. & Kochevar, R. E. 2002 Revealing pelagic habitat use: the tagging of Pacific pelagics program. Oceanologka Acta 25, 255-266. (doi:10.1016/S0399-1784(02)01212-4)
19. Bridges, C. R. 1994 Bohr and Root effects in cephalopod haemocyanins - paradox or pressure in Sepia officinalis? In Physiology of cephalopod molluscs: lifestyle and performance adaptations (eds H. O. Portner, R. K. O'Dor & D. L. MacMillan), pp. 121-130. New York, NY: Gordon and Breach.
20. Brown, J. H., Gillooly, J. F., Allen, A. P., Savage, V. M. & West, G. B. 2004 Toward a metabolic theory of ecology. Ecology 85, 1771-1789.
21. Bullard, S. G. & Hay, M. E. 2002 Palatability of marine macro-holoplankton: nematocysts, nutritional quality, and chemistry as defense against consumers. Limnol. Oceanogr. 47, 1456-1467.
22. Cailliet, G. M., Andrews, A. H., Burton, E. J., Watters, D. L., Kline, D. E. & Ferry-Graham, L. A. 2001 Age determination and validation studies of marine fishes: do deep-dwellers live longer? Exp. Gerontol. 36, 739-764. (doi:10.1016/S0531-5565(00)00239-4)
23. Castelini, M. A. & Somero, G. N. 1981 Buffering capacity of vertebrate muscle: correlations with potentials for anaerobic function. J. Comp. Physiol. B 143, 191-198.
24. Childress, J. J. 1971 Respiratory rate and depth of occurrence of midwater animals. Limnol. Oceanogr. 16, 104-106.
25. Childress, J. J. 1975 The respiratory rates of midwater crustaceans as a function of depth of occurrence and relation to the oxygen minimum layer off southern California. Comp. Biochem. Physiol. A 50, 787-799. (doi:10.1016/0300-9629(75)90146-2)
26. Childress, J. J. 1977 Effects of pressure, temperature and oxygen on the oxygen-consumption rate of the midwater copepod Gausia princeps. Mar. Biol. 39, 19-24. (doi:10.1007/BF00395588)
27. Childress, J. J. 1985 Capture and live recovery of deep-sea crustaceans. Natl Geogr. Soc. Res. Rep. 21, 67-69.
28. Childress, J. J. 1995 Are there physiological and biochemical adaptations of metabolism in deep-sea animals? Trends Ecol. Evol. 10, 30-36. (doi:10.1016/S0169-5347(00)88957-0)
29. Childress, J. J. & Mickel, T. J. 1985 Metabolic rates of animals from the hydrothermal vents and other deep-sea habitats. Biol. Soc. Wash. 6, 249-260.
30. Childress, J. J. & Nygaard, M. H. 1974 Chemical composition and buoyancy of midwater crustaceans as function of depth of occurrence off Southern California. Mar. Biol. 27, 225-238. (doi:10.1007/BF00391948)
31. Childress, J. J. & Seibel, B. A. 1998 Life at stable low oxygen: adaptations of animals to oceanic oxygen minimum layers. J. Exp. Biol. 201, 1223-1232.
32. Childress, J. J. & Somero, G. N. 1979 Depth-related enzymatic activities in muscle, brain, and heart of deep-living pelagic teleosts. Mar. Biol. 52, 273-283. (doi:10.1007/BF00398141)
33. Childress, J. J. & Somero, G. N. 1990 Metabolic scaling: a new perspective based on scaling of glycolytic enzyme activities. Am. Zool. 30, 161-173.
34. Childress, J. J. & Thuesen, E. V. 1995 Metabolic potentials of deep-sea fishes: a comparative approach. In Biochemistry and molecular biology of fishes (eds P. W. Hochachka & T. P. Mommsen), pp. 175-195. Berlin, Germany: Elsevier Science.
35. Childress, J. J., Barnes, A. T., Quetin, L. B. & Robison, B. H. 1978 Thermally protecting cod ends for the recovery of living deep-sea animals. Deep Sea Res. 25, 419-422. (doi:10.1016/0146-6291(78)90568-4)
36. Childress, J. J., Taylor, S. M., Cailliet, G. M. & Price, M. H. 1980 Patterns of growth, energy utilization and reproduction in some meso- and bathypelagic fishes off southern California. Mar. Biol. 61, 27-40. (doi:10.1007/BF00410339)
37. Childress, J. J., Cowles, D. L., Favuzzi, J. A. & Mickel, T. J. 1990a Metabolic rates of benthic deep-sea decapod crustaceans decline with increasing depm primarily due to the decline in temperature. Deep Sea Res. 37, 929-949. (doi:10.1016/0198-0149(90)90104-4)
38. Childress, J. J., Price, M. H., Favuzzi, J. & Cowles, D. 1990b Chemical composition of midwater fishes as a function of depth of occurrence off the Hawaiian Islands: food availability as a selective factor? Mar. Biol. 105, 235-246. (doi:10.1007/BF01344292)
39. Clarke, A. 1983 Life in cold water: the physiological ecology of polar marine ectotherms. Oceanogr. Mar. Biol. 21, 341-453.
40. Clarke, A. 2004 Is there a universal temperature dependence of metabolism? Funct. Ecol. 18, 252-256. (doi:10.1111/j.0269-8463. 2004.00842.x)
41. Clarke, A. & Johnston, N. M. 1999 Scaling of metabolic rate with body mass and temperature in teleost fish. J. Anim. Ecol. 68, 893-905. (doi:10.1046/j.1365-2656.1999.00337.x)
42. Collins, M. A., Priede, I. G. & Bagley, P. M. 1999 In situ comparison of activity in two deep-sea scavenging fishes occupying different depth zones. Proc. R. Soc. B 266, 2011-2016. (doi:10.1098/rspb. 1999.0879)
43. Company, J. B. & Sarda, F. 1998 Metabolic rates and energy content of deep-sea benthic decapod crustaceans in the western Mediterranean Sea. Deep Sea Res. I 45, 1861-1880. (doi:10.1016/S0967-0637(98)00034-X)
44. Cowles, D. L. 1994 Swimming dynamics of the mesopelagic vertically migrating penaeid shrimp Sergestes similis: modes and speeds of swimming. J. Crustacean Biol. 14, 247-257. (doi:10.2307/1548905)
45. Cowles, D. L. 2001 Swimming speed and metabolic rate during routine swimming and simulated diel vertical migration of Sergestes similis in the laboratory. Pac. Sci 55, 215-226. (doi:10.1353/psc.2001.0021)
46. Cowles, D. L. & Childress, J. J. 1988 Swimming speed and oxygen consumption of the bathypelagic mysid Gnathophausia ingens. Biol. Bull. 175, 111-121. (doi:10.2307/1541898)
47. Cowles, D. L., Childress, J. J. & Wells, M. E. 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. (doi:10.1007/BF01313094)
48. Dalhoff, E. P. 2004 Biochemical indicators of stress and metabolism: applications for marine ecological studies. Annu. Rev. Physiol. 66, 183-207. (doi:10.1146/annurev.physiol.66.032102.114509)
49. del Giorgio, P. A. & Duarte, C. M. 2002 Respiration in the open ocean. Nature 420, 379-384. (doi:10.1038/nature01165)
50. de Queiroz, A. 1999 Do image-forming eyes promote evolutionary diversification? Evolution 53, 1654-1664. (doi:10.2307/2640429)
51. Dewar, H. & Graham, J. 1994 Studies of tropical tuna swimming performance in a large water tunnel - kinematics. J. Exp. Biol. 192, 45-59.
52. Dickson, K. A. 1995 Unique adaptations of the metabolic biochemistry of tunas and billfishes for life in the pelagic environment. Environ. Biol. Fishes 42, 65-97. (doi:10.1007/BF00002352)
53. Dickson, K. A. 1996 Locomotor muscle of high-performance fishes: what do comparisons of tunas with ectothermic sister taxa reveal? Comp. Biochem. Physiol. A 113, 39-49. (doi:10.1016/0300-9629(95)02056-X)
54. Dickson, K. A. & Somero, G. N. 1987 Partial characterization of the buffering components of the red and white myotomal muscle of marine teleosts, with special emphasis on scombrid fishes. Physiol. Zool. 60, 699-706.
55. Domenici, P. 2002 The visually mediated escape response in fish: predicting prey responsiveness and the locomotor behaviour of predators and prey. Mar. Freshw. Behav. Physiol. 35, 87-110. (doi:10.1080/10236240290025635)
56. Donley, J., Sepulveda, C. A., Konstantinidis, P., Gemballa, S. & Shadwick, R. E. 2004 Convergent evolution in mechanical design of lamnid sharks and tunas. Nature 429, 61-65. (doi:10.1038/nature02435)
57. Drazen, J. C. 2002a Energy budgets and feeding rates of Coryphaenoides acrolepis and C. armatus. Mar. Biol. 140, 677-686. (doi:10.1007/s00227-001-0747-8)
58. Drazen, J. C. 2002b A seasonal analysis of the nutritional condition of deep-sea macrourid fishes in the north-east Pacific. J. Fish Biol. 60, 1280-1295. (doi:10.1111/j.1095-8649.2002.tb01720.x)
59. Drazen, J. C. 2007 Depth related trends in proximate composition of demersal fishes in the eastern North Pacific. Deep Sea Res. I 54, 203-219. (doi:10.1016/j.dsr.2006.10.007)
60. Drazen, J. C. & Robison, B. H. 2004 Direct observations of the association between deep-sea fish and a giant scyphomedusa. Mar. Freshw. Behav. Physiol. 37, 209-214. (doi:10.1080/10236240400006190)
61. Drazen, J. C. & Seibel, B. A. Submitted. Depth-related trends in metabolism of benthic and benthopelagic fishes. Limnol. Oceanogr.
62. Drazen, J. C., Bird, L. B. & Barry, J. P. 2005 Development of a hyperbaric trap-respirometer for the capture and maintenance of live deep-sea organisms. Limnol. Oceanogr. Methods 3, 488-498.
63. Eiane, K., Aksnes, D. L., Bagoien, E. & Kaartvedt, S. 1999 Fish or jellies - a question of visibility? Limnol. Oceanogr. 44, 1352-1357.
64. Farrell, A. P. 1991 From hagfish to tuna: a perspective on cardiac function in fish. Physiol. Zool. 64, 1137-1164.
65. Frank, T. & Widder, E. 1997 The correlation of down-welling irradiance and staggered vertical migration patterns of zooplankton in Wilkinson Basin Gulf of Maine. J. Plankton Res. 19, 1975-1991. (doi:10.1093/plankt/19.12.1975)
66. Ghalambor, C. K., Walker, J. A. & Reznick, D. N. 2003 Multi-trait selection, adaptation, and constraints on the evolution of burst swimming performance. Integr. Comp. Biol. 43, 431-438. (doi:10.1093/icb/43. 3.431)
67. +-adenosine triphosphatase activities in gills of marine teleost fishes: changes with depth, size and locomotory activity level. Mar. Biol. 106, 315-321. (doi:10.1007/BF01344307)
68. Gillooly, J. F., Brown, J. H., West, G. B., Savage, V. M. & Charnov, E. L. 2001 Effects of size and temperature on metabolic rate. Science 293, 2248-2251. (doi:10.1126/science.1061967)
69. Glazier, D. S. 2005 Beyond the '3/4-power law': variation in the intra- and interspecific scaling of metabolic rate in animals. Biol. Rev. 80, 611-662. (doi:10.1017/S1464793105006834)
70. Gordon, M. S., Belman, B. W. & Chow, P. H. 1976 Comparative studies on the metabolism of shallow-water and deep-sea marine fishes. IV. Patterns of aerobic metabolism in the mesopelagic deep-sea fangtooth fish Anoplogaster cornuta. Mar. Biol. 35, 287-293. (doi:10.1007/BF00396876)
71. Haddock, H. D. 2004 A golden age of gelata: past and future research on planktonic ctenophores and cnidarians. Hydrobiologia 530/531, 549-556. (doi:10.1007/s10750-004-2653-9)
72. Haddock, H. D., Dunn, C. W., Pugh, P. R. & Schnitzler, C. E. 2005 Bioluminescent and red fluorescent lures in a deep-sea siphonophore. Science 309, 263. (doi:10.1126/science.1110441)
73. Hamner, W. M. 1995 Predation, cover, and convergent evolution in epipelagic oceans. Mar. Freshw. Behav. Physiol. 26, 71-89.
74. Harvey, P. H. & Pagel, M. D. 1991 The comparative method in evolutionary biology. Oxford, UK: Oxford University Press.
75. Helly, J. J. & Levin, L. A. 2004 Global distribution of naturally occurring marine hypoxia on continental margins. Deep Sea Res. 51, 1159-1168. (doi:10.1016/j.dsr.2004.03.009)
76. Henry, R. P., Handley, H. L., Krarup, A. & Perry, H. M. 1990 Respiratory and cardiovascular physiology of two species of deep-water crabs, Chaceon fenneri and C. quinquidens: in nomoxia and hypoxia. J. Crustacean Biol. 10, 413-422. (doi:10.2307/1548331)
77. Hernandez-Leon, S. & Ikeda, T. 2005 A global assessment of mesozooplankton respiration in the ocean. J. Plankton Res. 27, 153-158. (doi:10.1093/plankt/fbh166)
78. Herring, P. J. 1977 Bioluminescence of marine animals. Nature 267, 788-793. (doi:10.1038/267788a0)
79. Hochachka, P. W. & Somero, G. N. 2002 Biochemical adaptation: mechanism and process in physiological evolution. Oxford, UK: Oxford University Press.
80. Humphriese, S. & Ruxton, G. D. 2002 Why did some ichthyosaurs have such large eyes? J. Exp. Biol. 205, 439-441.
81. Hunt, J. C. 1996 The behavior and ecology of midwater cephalopods from Monterey Bay. PhD dissertation, UMI Press, pp. 231.
82. Hunt, J. C. & Lindsay, D. J. 1998 Observations on the behavior of Atolla (Scyphozoa: Coronatae) and Nanomia (Hydrozoa: Physonectae): use of the hypertrophied tentacle in prey capture. Plankton Biol. Ecol. 45, 239-224.
83. Hunt, J. C. & Seibel, B. A. 2000 Life history of Gonatus onyx (Cephalopoda: Teuthoidea): ontogenetic changes in habitat, behavior and physiology. Mar. Biol. 136, 543-552. (doi:10.1007/s002270050714)
84. Ikeda, T. 1988 Metabolism and chemical composition of crustaceans from the Antarctic mesopelagic zone. Deep Sea Res. I 35, 1991-2002. (doi:10.1016/0198-0149(88)90121-5)
85. Janssens, B., Childress, J. J., Baguet, F. & Rees, J. 2000 Reduced enzymatic antioxidative defense in deep-sea fish. J. Exp. Biol. 203, 3717-3725.
86. Johnsen, S. 2001 Hidden in plain sight: the ecology and physiology of organismal transparency. Biol. Bull. 201, 301-318. (doi:10.2307/1543609)
87. Kleiber, M. 1932 Body size and metabolism. Hilgardia 6, 315-352.
88. Koslow, J. A. 1996 Energetic and life-history patterns of deep-sea benthic, benthopelagic and seamount-associated fish. J. Fish Biol. 49A, 54-74. (doi:10.1111/j.1095-8649.1996.tb06067.x)
89. Koyama, S., Miwa, T., Horii, M., Ishikawa, Y., Horikoshi, K. & Aizawa, M. 2002 Pressure-stat aquarium system designed for capturing and maintaining deep-sea organisms. Deep Sea Res. I 49, 2095-2102. (doi:10.1016/S0967-0637(02)00098-5)
90. Longhurst, A. R., Bedo, A. W., Harrison, W. G., Head, E. J. H. & Sameoto, D. D. 1990 Vertical flux of respiratory carbon by oceanic diel migrant biota. Deep Sea Res. I 37, 685-694. (doi:10.1016/0198-0149(90) 90098-G)
91. Lythgoe, J. N. 1988 Light and vision in the aquatic environment. In Sensory biology of aquatic animals (eds J. Atema, R. R. Fay, A. Popper & W. N. Tavolga), pp. 57-87. New York, NY: Springer.
92. Mahaut, M. L., Sibuet, M. & Shirayama, Y. 1995 Weight-dependent respiration rates in deep-sea organisms. Deep Sea Res. I 42, 1575-1582. (doi:10.1016/0967-0637(95)00070-M)
93. Markaida, U., Rosenthal, J. J. C. & Gilly, W. F. 2005 Tagging studies of the Humboldt squid Dosidicus gigas, in the Gulf of California, Mexcio. Fish. Bull. 103, 219-226.
94. Marshall, N. J. & Diebel, C. 1995 Deep-sea 'spiders' that walk through the water. J. Exp. Biol. 198, 1371-1379.
95. Matsumoto, G. I. & Harbison, G. R. 1993 In situ observations of foraging, feeding, and escape behavior in three orders of oceanic ctenophores: Lobata, Cestida, and Beroida. Mar. Biol. 117, 279-287. (doi:10.1007/BF00345673)
96. McClintock, J. B. & Janssen, J. 1990 Pteropod abduction as a chemical defense in a pelagic antarctic amphipod. Nature 346, 462-464. (doi:10.1038/346462a0)
97. Meek, R. P. & Childress, J. J. 1973 Respiration and the effect of pressure in the mesopelagic fish Anoplogaster cornuta (Beryciformes). Deep Sea Res. 20, 1111-1118.
98. Moyes, C. D. & LeMoine, C. M. R. 2005 Control of muscle bioenergetic gene expression: implications for allometric scaling relationships of glycolytic and oxidative enzymes. J. Exp. Biol. 208, 1601-1610. (doi:10.1242/jeb.01502)
99. Nelson, J. A. & Claireaux, G. 2005 Spring swimming performance of juvenile European Sea Bass. Trans. Am. Fish. Soc. 134, 1274-1284. (doi:10.1577/T04-087.1)
100. O'Dor, R. K. 1982 Respiratory metabolism and swimming performance of the squid Loligo opalescens. Can. J. Fish. Aquat. Sci. 39, 580-587.
101. O'Dor, R. K. 2002 Telemetered cephalopod energetics: swimming, soaring and blimping. Integr. Comp. Biol. 42, 1065-1070. (doi:10.1093/icb/42.5.1065)
102. O'Dor, R. K. & Webber, D. M. 1986 The constraints on cephalopods: why squid aren't fish. Can. J. Zool. 64, 1591-1605.
103. Packard, A. 1972 Cephalopods and fish: the limits of convergence. Biol. Rev. 47, 241-307. (doi:10.1086/407285)
104. + leak in mitochondria and its relevance to metabolic rate. Nature 362, 628-630. (doi:10.1038/362628a0)
105. Pörtner, H. O. 2002 Environmental and functional limits to muscular exercise and body size in marine invertebrate athletes. Comp. Biochem. Physiol. A 133, 303-321. (doi:10.1016/S1095-6433(02)00162-9)
106. Poulson, T. L. 2001 Adaptations of cave fishes with some comparisons to deep-sea fishes. Environ. Biol. Fishes 62, 345-364. (doi:10.1023/A:1011893916855)
107. Priede, I. G. & Bagley, P. M. 2000 In situ studies on deep-sea demersal fishes using autonomous unmanned ladder platforms. Annu. Rev. Oceanogr. Mar. Biol. 38, 357-392.
108. Priede, I. G., Smith Jr, K. L. & Armstrong, J. D. 1990 Foraging behavior of abyssal grenadier fish: inferences from acoustic tagging and tracking in the North Pacific Ocean. Deep Sea Res. 37, 81-101. (doi:10.1016/0198-0149(90)90030-Y)
109. Priede, I. G., Deary, A. R., Bailey, D. M. & Smith, K. L. 2003 Low activity and seasonal change in population size structure of granadiers in the oligotrophic abyssal central North Pacific Ocean. J. Fish Biol. 63, 187-196. (doi:10.1046/j.1095-8649.2003.00142.x)
110. Quetin, L. B., Ross, R. M. & Clarke, A. 1994 Krill energetics: seasonal and environmental aspects of the physiology of Euphausia superba. In Southern ocean ecology: the BIOMASS perspective (ed. S. Z. El-Sayed), pp. 165-184. Cambridge, UK: Cambridge University Press.
111. Raskoflf, K. A. 2002 Foraging, prey capture, and gut contents of the mesopelagic narcomedusae, Solmissus spp. (Cnidaria: Hydrozoa). Mar. Biol. 141, 1099-1107. (doi:10.1007/s00227-002-0912-8)
112. Reinhold, K. 1999 Energetically costly behavior and the evolution of resting metabolic rate in insects. Funct. Ecol. 13, 221-224. (doi:10.1046/j.1365-2435.1999.00300.x)
113. Robison, B. H. 1999 Shape-change behavior by mesopelagic animals. Mar. Freshw. Behav. Physiol. 32, 17-25.
114. Robison, B. H. 2000 The coevolution of undersea vehicles and deep-sea research. Mar. Tech. Soc. J. 33, 65-73.
115. Robison, B. H. 2004 Deep pelagic biology. J. Exp. Mar. Biol. Ecol. 300, 245-264. (doi:10.1016/j.jembe.2004.01.012)
116. Robison, B. H., Reisenbichler, K. R., Hunt, J. C. & Haddock, S. H. D. 2003 Light production by the arm tips of the deep-sea cephalopod Vampyroteuthis infernalis. Biol. Bull. 205, 102-109. (doi:10.2307/1543231)
117. Roper, C. F. E. & Vecchione, M. 1997 In situ observations test hypotheses of functional morphology in Mastigoteuthis (Cephalopoda, Oegopsida). Vie Milieu 47, 87-94.
118. Samerotte, S. L., Drazen, J. C., Brand, G. L., Seibel, B. A. & Yancey, P. H. 2007 Correlation of trimethylamine oxide and habitat depth within and among species of teleost fishes: an analysis of causation. Physiol. Biochem. Zool. 80, 197-208. (doi:10.1086/510566)
119. Sanders, N. K. & Childress, J. J. 1988 Ion replacement as a buoyancy mechanism in a pelagic deep-sea crustacean. J. Exp. Biol. 138, 333-343.
120. Schmidt-Nielsen, K. 1984 Scaling: why is animal size so important? Cambridge, UK: Cambridge University Press.
121. Seibel, B. A. 2007 On the depth and scale of metabolic rate variation: scaling of oxygen consumption and enzymatic activity in the Class Cephalopoda (Mollusca). J. Exp. Biol. 210, 1-11. (doi:10.1242/jeb.02588)
122. Seibel, B. A. & Carlini, D. B. 2001 Metabolism of pelagic cephalopods as a function of habitat depth: a reanalysis using phylogenetically independent contrasts. Biol. Bull. 201, 1-5. (doi:10.2307/1543519)
123. Seibel, B. A. & Childress, J. J. 2000 Metabolism of benthic octopods (Cephalopoda) as a function of habitat depth and oxygen concentration. Deep Sea Res. 47, 1247-1260. (doi:10.1016/S0967-0637(99)00103-X)
124. Seibel, B. A. & Dierssen, H. M. 2003 Tip of the iceberg: cascading trophic impacts of the iceberg, B-15, in the Ross Sea, Antarctica. Biol. Bull. 205, 93-99. (doi:10.2307/1543229)
125. 2 injection on deep-sea biota. Science 294, 319-320. (doi:10.1126/science.1065301)
126. Seibel, B. A. & Walsh, P. J. 2002 Trimethylamine oxide accumulation in marine animals: relationship to acylglycerol storage. J. Exp. Biol. 205, 297-306.
127. Seibel, B. A. & Walsh, P. J. 2003 Biological impacts of deep-sea carbon dioxide injection inferred from indices of physiological performance. J. Exp. Biol. 206, 641-650. (doi:10.1242/jeb.00141)
128. Seibel, B. A., Thuesen, E. V., Childress, J. J. & Gorodezky, L. A. 1997 Decline in pelagic cephalopod metabolism with habitat depth reflects differences in locomotory efficiency. Biol. Bull. 192, 262-278. (doi:10.2307/1542720)
129. Seibel, B. A., Thuesen, E. V. & Childress, J. J. 1998 Flight of the vampire: ontogenetic gait-transition in Vampyroteuthis infernalis (Cephalopoda: Vampyromorpha). J. Exp. Biol. 201, 2413-2424.
130. Seibel, B. A., Chausson, F., Lallier, F. H., Zal, F. & Childress, J. J. 1999 Vampire blood: respiratory physiology of the vampire squid (Cephalopoda: Vampyromorpha) in relation to the oxygen minimum layer. Exp. Biol. Online 4, 1-10.
131. Seibel, B. A., Thuesen, E. V. & Childress, J. J. 2000 Light-limitation on predator-prey interactions: consequences for metabolism and locomotion of deep-sea cephalopods. Biol. Bull. 198, 284-298. (doi:10.2307/1542531)
132. Seibel, B. A., Goffredi, S. K., Thuesen, E. V., Childress, J. J. & Robison, B. H. 2004 Ammonium content and buoyancy in midwater cephalopods. J. Exp. Mar. Biol. Ecol. 313, 375-387. (doi:10.1016/j.jembe.2004.08. 015)
133. Seibel, B. A., Robison, B. H. & Haddock, S. D. H. 2005 First observations of post-spawning egg-care in a squid. Nature 438, 929. (doi:10.1038/438929a)
134. Shadwick, R. E., O'Dor, R. K. & Gosline, J. M. 1990 Respiratory and cardiac function during exercise in squid. Can. J. Zool. 68, 792-798.
135. Shirayama, Y. 1992 Respiration rates of bathyal meiobenthos collected using a deep-sea submersible SHINKAI 2000. Deep Sea Res. 39, 781-788. (doi:10.1016/0198-0149(92)90120-I)
136. Siebenaller, J. F., Somero, G. N. & Haedrich, R. L. 1982 Biochemical characteristics of macrourid fishes differing in their depths of distribution. Biol. Bull. 163, 240-249. (doi:10.2307/1541512)
137. Smith Jr, K. L. 1978 Metabolism of the abyssopelagic rattail Coryphaenoides armatus measured in situ. Nature 274, 362-364. (doi:10.1038/274362a0)
138. Smith Jr, K. L. 1983 Metabolism of two dominant epibenthic echinoderms measured at bathyal depths in the Santa Catalina Basin. Mar. Biol. 72, 249-256. (doi:10.1007/BF00396830)
139. Smith Jr, K. L. & Baldwin, R. J. 1997 Laboratory and in situ methods for studying deep-sea fishes. In Deep-sea fishes (eds D. J. Randall & A. P. Farrell), pp. 351-378. San Diego, CA: Academic Press.
140. Smith Jr, K. L. & Baldwin, R. J. 1982 Scavenging deep-sea amphipods: effects of food odour on oxygen consumption and a proposed metabolic strategy. Mar. Biol. 68, 287-298. (doi:10.1007/BF00409595)
141. Smith Jr, K. L. & Hessler, R. R. 1974 Respiration of benthopelagic fishes: in situ measurements at 1230 meters. Science 184, 72-73. (doi:10.1126/science.184.4132.72)
142. Smith Jr, K. L. & Laver, M. B. 1981 Respiration of the bathypelagic fish Cyclothone acclinidens. Mar. Biol. 61, 261-266. (doi:10.1007/BF00401564)
143. Smith Jr, K. L. & Teal, J. M. 1973 Temperature and pressure effects on respiration of thecosomatous pteropods. Deep Sea Res. 20, 853-858.
144. Somero, G. N. 1992 Adaptations to high hydrostatic pressure. Annu. Rev. Physiol. 54, 557-577. (doi:10.1146/annurev.ph.54.030192.003013)
145. Somero, G. N. & Childress, J. J. 1980 A violation of the metabolism-size scaling paradigm: activities of glycolytic enzymes in muscle increase in larger-size fish. Physiol. Zool. 53, 322-337.
146. Somero, G. N. & Siebenaller, J. F. 1979 Inefficient lactate dehydrogenases of deep-sea fishes. Nature 282, 100-102. (doi:10.1038/282100a0)
147. Suarez, R. K. 1996 Upper limits to mass-specific metabolic rates. Annu. Rev. Physiol. 58, 583-605. (doi:10.1146/annurev.ph.58. 030196.003055)
148. Sullivan, K. M. & Somero, G. N. 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. (doi:10.1007/ BF00389152)
149. Taylor, C. R., Maloiy, G. M., Weibel, E. R., Langman, V. A., Kamau, J. M., Seeherman, H. J. & Heglund, N. C. 1981 Design of the mammalian respiratory system. III. Scaling maximum aerobic capacity to body mass: wild and domestic mammals. Respir. Physiol. 44, 25-37. (doi:10.1016/0034-5687(81)90075-X)
150. Thistle, D., Carman, K. R., Sedlacek, L., Brewer, P. G., Fleeger, J. W. & Barry, J. P. 2005 Deep-ocean, sediment-dwelling animals are sensitive to sequestered carbon dioxide. Mar. Ecol. Prog. Ser. 289, 1-4.
151. Thuesen, E. V. & Childress, J. J. 1993a Enzymatic activities and metabolic rates of pelagic chaetognaths: lack of depth-related declines. Limnol. Oceanogr. 38, 935-948.
152. Thuesen, E. V. & Childress, J. J. 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. (doi:10.1016/0967-0637(93)90082-E)
153. Thuesen, E. V. & Childress, J. J. 1993c Effects of hydrostatic pressure on metabolic rates of six deep-sea gelatinous zooplankton. Limnol. Oceanogr. 38, 665-670.
154. Thuesen, E. V. & Childress, J. J. 1994 Oxygen consumption rates and metabolic enzyme activities of oceanic California medusae in relation to body size and habitat depth. Biol. Bull. 187, 84-98. (doi:10.2307/1542168)
155. Thuesen, E. V., Miller, C. B. & Childress, J. J. 1998 Ecophysiological interpretation of oxygen consumption rates and enzymatic activities of deep-sea copepods. Mar. Ecol. Prog. Ser. 168, 95-107.
156. Thuesen, E. V., Rutherford Jr, L. D., Brommer, P. L., Garrison, K., Gutowska, M. A. & Towanda, T. 2005a Intragel oxygen promotes hypoxia tolerance of scyphomedusae. J. Exp. Biol. 208, 2475-2482. (doi:10.1242/jeb.01655)
157. Thuesen, E. V., McCullough, K. D. & Childress, J. J. 2005b Metabolic enzyme activities in swimming muscle of medusae: is the scaling of glycolytic activity related to oxygen availability? J. Mar. Biol. Assoc. UK 85, 603-611. (doi:10.1017/S0025315405011537)
158. Thurston, M. H., Bett, B. J., Rice, A. L. & Jackson, P. A. B. 1994 Variations in the invertebrate abyssal megafauna in the North Atlantic Ocean. Deep Sea Res. 141, 1321-1348. (doi:10.1016/0967-0637(94)90100-7)
159. Thurston, M. H., Rice, A. L. & Bett, B. J. 1998 Latitudinal variation in invertebrate megafaunal abundance and biomass in the North Atlantic Ocean Abyss. Deep Sea Res. II 45, 1-3. (doi:10.1016/S0967-0645(97)00077- 5)
160. Torres, J. J. & Somero, G. N. 1988 Metabolism, enzymic activities and cold adaption in Antarctic mesopelagic fishes. Mar. Biol. 98, 169-180. (doi:10.1007/BF00391192)
161. Torres, J. J., Belman, B. W. & Childress, J. J. 1979 Oxygen consumption rates of midwater fishes as a function of depth of occurrence. Deep Sea Res. 26, 185-197. (doi:10.1016/0198-0149(79)90075-X)
162. Treberg, J. R., Martin, R. A. & Driedzic, W. R. 2003 Muscle enzyme activities in a deep-sea squaloid shark, Centroscyllium fabricii, compared with its shallow-living relative, Squalus acanthias. J. Exp. Zool. A 300, 133-139. (doi:10.1002/jez.a.10318)
163. Treude, T., Janssen, F., Queisser, W. & Witte, U. 2002 Metabolism and decompression tolerance of scavenging lysianassoid deep-sea amphipods. Deep Sea Res. I 49, 1281-1289. (doi:10.1016/S0967-0637(02)00023-7)
164. Verity, P. G., Smetacek, V. & Smayda, T. J. 2002 Status, trends and the future of the marine pelagic ecosystem. Environ. Conserv. 29, 207-237. (doi:10.1017/S0376892902000139)
165. Villanueva, R., Segonzac, M. & Guerra, A. 1997 Locomotion modes of deep-sea cirrate octopods (Cephalopoda) based on observations from video recordings on the Mid-Atlantic Ridge. Mar. Biol. 129, 113-122. (doi:10.1007/s002270050152)
166. Walsh, P. J. & Henry, R. P. 1990 Activities of metabolic enzymes in the deep-water crabs Chaceon fenneri and C. quinquedens and the shallow-water crab Callinectes sapidus. Mar. Biol. 106, 343-346. (doi:10.1007/BF01344310)
167. Warrant, E. J. 2004 Vision in the dimmest habitats on Earth. J. Comp. Physiol. A 190, 765-789. (doi:10.1007/s00359-004-0546-z)
168. Warrant, E. J. & Locket, N. A. 2004 Vision in the deep-sea. Biol. Rev. Camb. Phil. Soc. 79, 671-712. (doi:10.1017/S1464793103006420)
169. Webber, D. M., Aitken, J. & O'Dor, R. K. 2000 Costs of vertical locomotion and vertic dynamics of cephalopods and fish. Physiol. Biochem. Zool. 73, 651-662. (doi:10.1086/318100)
170. Weibel, E. & Hoppeler, H. 2005 Exercise-induced maximal metabolic rate scales with muscle aerobic capacity. J. Exp. Biol. 208, 1635-1644. (doi:10.1242/jeb.01548)
171. 2/3. Proc. Natl Acad. Sci. USA 100, 4046-4049. (doi:10.1073/pnas.0436428100)
172. Widder, E. A. 2002 Bioluminescence and the pelagic visual environment. Mar. Freshw. Behav. Physiol. 35, 1-26. (doi:10.1080/ 10236240290025581)
173. Williams, T. M. 1999 The evolution of cost efficient swimming in marine mammals: limits to energetic optimization. Phil. Trans. R. Soc. B 354, 193-201. (doi:10.1098/rstb.1999.0371)
174. Wishner, K., Levin, L. A., Gowing, M. & Mullineaux, L. 1990 Involvement of the oxygen minimum in benthic zonation on a deep seamount. Nature 346, 57-59. (doi:10.1038/346057a0)
175. Withers, P., Hefter, G. & Pang, T. S. 1994 The role of urea and methylamines in buoyancy of elasmobranchs. J. Exp. Biol. 188, 175-189.
176. Witte, U. & Graf, G. 1996 Metabolism of deep-sea sponges in the Greenland-Norwegian Sea. J. Exp. Mar. Biol. Ecol. 198, 223-235. (doi:10.1016/0022-0981(96)00006-8)
177. Yamada, Y. & Ikeda, T. 2003 Metabolism and chemical composition of four pelagic amphipods in the Oyashio region, western subarctic Pacific Ocean. Mar. Ecol. Prog. Ser. 253, 233-241.
178. Yancey, P. H. 2005 Organic osmolytes as compatible, metabolic and counteracting croprotectants in high osmolarity and other stresses. J. Exp. Biol. 208, 2819-2830. (doi:10.1242/jeb.01730)
179. Yang, T. H., Lai, N. C., Graham, J. B. & Somero, G. N. 1992 Respiratory, blood, and heart enzymatic adaptations of Sebastobbus alascanus (Scorpaenidae; Teleostei) to the oxygen minimum zone: a comparative study. Biol. Bull. 183, 490-499. (doi:10.2307/1542026)
180. Young, R. E. 1983 Oceanic bioluminescence: an overview of general functions. Bull. Mar. Sci. 33, 829-845.
181. Youngbluth, M. J. & Båmstedt, U. 2001 Distribution, abundance, behavior and metabolism of Periphylla periphylla, a mesopelagic coronate medusa in a Norwegian fjord. Hydrobiolgia 451, 321-333. (doi:10.1023/A:1011874828960)
182. Zeidberg, L. D. 2004 Allometry measurements from in situ video recordings can detemine the size and swimming speeds of juvenile and adult squid Loligo opalescens (Cephalopoda: Myopsida). J. Exp. Biol. 207, 4195-4203. (doi:10.1242/jeb.01276)