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Marine Biology

, Volume 120, Issue 1, pp 145–159 | Cite as

Depth zonation and metabolic adaptation in Dover sole, Microstomus pacificus, and other deep-living flatfishes: factors that affect the sole

  • R. D. Vetter
  • E. A. Lynn
  • M. Garza
  • A. S. Costa
Article
  • 164 Downloads

Abstract

Flatfishes of Monterey Bay, central California, undergo species replacements with increasing depth along a transect from 100 m on the continental shelf down to a depth of 1400 m on the continental slope. The Dover sole, Microstomus pacificus, differs from the other local flatfish species by undergoing an extensive ontogenetic vertical migration, occupying all depth zones at different life stages, and having its maximum spawning biomass in the oxygen minimum zone between 600 and 1000 m. Size-activity relationships and depth-activity relationships for the glycolytic enzyme lactate dehydrogenase (LDH) and for two enzymes associated with aerobic metabolism, malate dehydrogenase and citrate synthase (CS), were examined in white-muscle tissue of shallow-living, deep-living and ontogenetically-migrating species. Scaling coefficients (b) for weight-specific enzyme activity (log activity)=a+b (log wet weight), varied in sign as well as magnitude for fishes living at different depths. In the shallow-living California halibut Paralichthys californicus, LDH scaled positively (0.39) and CS scaled negatively (-0.15) with size, a pattern observed previously for most shallow-water fish species. The permanently deep-living species, the deepsea sole Embassichthys bathybius, differed in that both LDH and CS scaled strongly negative (-2.0 and-1.5, respectively). For the ontogenetically migrating Dover sole Microstomus pacificus, there was a shelf-slope transition. For the shelf specimens (≤200 m), LDH scaled positive (0.11) and CS negative (-0.29) and for the slope specimens (≥400 m), LDH scaled negative (-0.65) and CS strongly negative (-0.63). Rex sole, Glyptocephalus zachirus, showed a similar shelf-slope transition. Intraspecific depth-enzyme activity differences were not incremental, but changed abruptly between the continental shelf stations (100 to 200 m) and the continental slope (400 to 1400 m). Based on comparisons with laboratory-maintained individuals, the decline in the metabolic capacity of the white muscle of Dover sole is a phenotypic response to the low food and oxygen conditions of the continental slope. Contrary to expectation, anaerobic capacity (LDH activity) decreased in response to low oxygen conditions, suggesting that in a permanently hypoxic environment such as the oxygen minimum zone the metabolic strategy may be to not incur an oxygen debt that would be difficult to pay back.

Keywords

Continental Shelf Continental Slope Malate Dehydrogenase Anaerobic Capacity Oxygen Minimum Zone 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

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References

  1. Anderson GC (1971) Oxygen analysis, Marine Technicians Handbook, Scripps Institution of Oceanography, Berkeley, California [Sea Grant Publ No 9. Ref. 71-8]Google Scholar
  2. Beamish FWH (1964) Influence of starvation on standard and routine oxygen consumption. Trans Am Fish Soc 93:103–107Google Scholar
  3. Becker SD, Chew KK (1987) Predation on Capitella spp. by small-mouthed pleuronectids in Puget Sound, Washington. Fish Bull US 85:471–479Google Scholar
  4. Carpenter JH (1965) The Chesapeake Bay Institute technique for the Winkler dissolved oxygen method. Limnol Oceanogr 10:141–143Google Scholar
  5. Childress JJ, Cowles DL, Favuzzi JA, Mickel TJ (1990) Metabolic rates in deep-sea decapod crustaceans decline with increasing depth primarily due to the decline in temperature. Deep-Sea Res 37:929–949Google Scholar
  6. Childress JJ, Somero GN (1979) Depth-related enzymic activities in muscle, brain and heart of deep-living pelagic marine teleosts. Mar Biol 52:273–283Google Scholar
  7. Childress JJ, Somero GN (1990) Metabolic scaling: a new perspective based on scaling of glycolytic enzyme activities. Am Zool 30:161–173Google Scholar
  8. Childress JJ, Taylor SM, Cailliet GM, Price MH (1980) Patterns of growth, energy utilization and reproduction in some meso- and bathypelagic fishes off Southern California. Mar Biol 61:27–40Google Scholar
  9. Childress JJ, Thuesen EV (1992) Metabolic potential of deep-sea animals: regional and global scales. In: Rowe GT, Pariente V (eds) Deep-sea food chains and the global carbon cycle. Kluwer Academy Publishers, Netherlands, p 217–236Google Scholar
  10. Cowles DL, Childress JJ, Wells ME (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 110:75–83Google Scholar
  11. Gabriel WL, Pearcy WG (1981) Feeding selectivity of Dover sole, Microstomus pacificus, off Oregon. Fish Bull US 79:749–763Google Scholar
  12. Gesser H, Poupa O (1974) Relations between heart muscle enzyme pattern and directly measured tolerance to acute anoxia. Comp Biochem Physiol 48 A:97–103Google Scholar
  13. Hochachka PW (1991) The metabolic arrest and channel arrest concepts of defence against hypoxia in vertebrates. In: Bryant C (ed) Metazoan life without oxygen. Chapman & Hall, New York, p 238–249Google Scholar
  14. Hunter JR, Butler JL, Kimbrell CL, Lynn EA (1990) Bathymetric patterns in size, age, sexual maturity, water content, and caloric density of Dover sole, Microstomus pacificus. Rep Calif coop ocean Fish Invest (CalCOFI) 31:132–144Google Scholar
  15. Hunter JR, Macewicz BJ, Lo NC, Kimbrell CA (1992) Fecundity, spawning, and maturity of female Dover sole Microstomus pacificus, with an evaluation of assumptions and precision. Fish Bull US 90:101–128Google Scholar
  16. Jacobson LD, Hunter JR (1993) Bathymetric demography and management of Dover sole. N Am J Fish Mgmt 13:405–420Google Scholar
  17. Jahnke RA, Reimers CE, Craven DB (1990) Intensification of recycling of organic matter at the sea floor near ocean margins. Nature, Lond 348:50–54Google Scholar
  18. Lowery MS, Roberts SJ, Somero GN (1987) Effects of starvation on the activities and localization of glycolytic enzymes in the white muscle of the barred sand bass Paralabrax nebulifer. Physiol Zoöl 60:538–549Google Scholar
  19. Martin JH, Knauer GA, Karl DM, Broenkow WW (1987) VERTEX: carbon cycling in the northeast Pacific. Deep-Sea Res 34:267–285Google Scholar
  20. Mullins HT, Thompson JB, McDougall K, Vercoutere TL (1985) Oxygen-minimum zone edge effects: evidence from the central California coastal upwelling system. Geology (Boulder, Colorado) 13:491–494Google Scholar
  21. Pearcy WG, Hancock D (1978) Feeding habits of Dover sole, Microstomus pacificus; rex sole, Glyptocephalus zachirus; slender sole, Lyopsetta exilis, and Pacific sanddab, Citharichthys sordidus, in a region of diverse sediments and bathymetry off Oregon. Fish Bull US 76:641–651Google Scholar
  22. Siebenaller JF (1984) Analysis of the biochemical consequences of ontogenetic vertical migration in a deep-living teleost fish. Physiol Zoöl 57:598–608Google Scholar
  23. Siebenaller JF, Somero GN (1982) The maintenance of different enzyme activity levels in congeneric fishes living at different depths. Physiol Zoöl 55:171–179Google Scholar
  24. Siebenaller JF, Somero GN (1989) Biochemical adaptation to the deep sea. CRC critical Rev aquat Sciences 1:1–25Google Scholar
  25. Somero GN, Childress JJ (1980) A violation of the metabolism-scaling paradigm: activities of glycolytic enzymes increase in larger-size fish. Physiol Zoöl 53:322–337Google Scholar
  26. Somero GN, Childress JJ (1990) Scaling of ATP-supplying enzymes, myofibrillar proteins and buffering capacity in fish muscle: relationship to locomotory habit. J exp Zool 149:319–333Google Scholar
  27. Sullivan KM, Somero GN (1980) Enzyme activities of fish skeletal muscle and brain as influenced by depth of occurrence and habits of feeding and locomotion. Mar Biol 60:91–99Google Scholar
  28. Sullivan KM, Somero GN (1983) Size- and diet-related variations in enzymatic activity and tissue composition in the sablefish, Anoplopoma fimbria. Biol Bull mar biol Lab, Woods Hole 164: 315–326Google Scholar
  29. Torres JJ, Belman BW, Childress JJ (1979) Oxygen consumption rates of midwater fishes as a function of depth of occurrence. Deep-Sea Res 26A:185–197CrossRefGoogle Scholar
  30. Torres JJ, Somero GN (1988) Metabolism, enzymic activities and cold adaptation in Antarctic mesopelagic fishes. Mar Biol 98: 169–180Google Scholar
  31. Vetter RD, Hodson RE (1982) Use of adenylate concentrations and adenylate energy charge as indicators of hypoxic stress in estuarine fish. Can J Fish aquat Sciences 39:535–541Google Scholar
  32. Weiss RF (1970) The solubility of nitrogen, oxygen and argon in water and seawater. Deep-Sea Res 17:721–735Google Scholar
  33. White BN (1987) Oceanic anoxic events and allopatric speciation in the deep sea. Biol Oceanogr 5:243–259Google Scholar
  34. Yang T-H, Lai NC, Graham JB, Somero GN (1992) Respiratory, blood, and heart enzymatic adaptations of Sebastolobus alascanus (Scorpaenidae; Teleostei) to the oxygen minimum zone: a comparative study. Biol Bull mar biol Lab, Woods Hole 183: 490–499Google Scholar
  35. Yang T-H, Somero GN (1993) Effects of feeding and food deprivation on oxygen consumption, muscle protein concentration and activities of energy metabolism enzymes in muscle and brain of shallow-living (Scorpaena guttata) and deep-living (Sebastolobus alascanus) scorpaenid fishes. J exp Biol 181:213–232Google Scholar

Copyright information

© Springer-Verlag 1994

Authors and Affiliations

  • R. D. Vetter
    • 1
  • E. A. Lynn
    • 1
  • M. Garza
    • 1
  • A. S. Costa
    • 1
  1. 1.National Oceanic and Atmospheric AdministrationSouthwest Fisheries Science CenterLa JollaUSA

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