A Review of Measurements of Respiration Rates of Marine Plankton Populations

  • P. J. leB. Williams
Part of the NATO Conference Series book series (NATOCS, volume 15)


The biological cycle in the oceans may be viewed to be comprised of two fundamental processes: photosynthesis and respiration. The introduction by Steemann Nielsen of the 14C-technique for measuring planktonic photosynthesis has enabled this particular process to be extensively and easily studied. As a consequence there is now a considerable body of data available of measurements of plankton photosynthesis. This contrasts with respiration for which there are still remarkably few direct measurements. Although the processes of respiration and photosynthesis may be regarded to be in balance and essentially equal on the oceanic scale, food chain processes cause them to be separated both in space and time. In contrast to photosynthesis, planktonic respiration may be expected to occur throughout the water column. Thus in any one situation, respiration cannot be taken to be simply equal to photosynthesis but needs to be measured independently. Furthermore respiration is not restricted to a single group of organisms but common to all. Thus the study of respiration is inherently more complex and extensive than photosynthesis from both the trophodynamic and geographical points of view. The distribution of respiration between the major planktonic groups (net zooplankton, microzooplankton, heterotrophic microorganisms, algae) will give insight into the trophic structure of the planktonic community. The vertical distribution of respiration in the water column can given accounts of the export to and fate of the products of phytoplankton photosynthesis in the deeper parts of the ocean.


Respiration Rate Particulate Organic Carbon Reef Flat Euphotic Zone Electron Transport System 


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  1. Andrews, P., and P. J. leB. Williams. 1971. Heterotrophic utilization of organic compounds in the sea. III. Measurement of the oxidation rates and concentrations of glucose and amino acids in sea water. J. Mar. Biol. Assoc. UK 51: 111–125.CrossRefGoogle Scholar
  2. Antia, N. J., C. D. McAllister, T. R. Parson, K. Stephens, and J. D. H. Strickland. 1963. Further measurements of primary production using a large-volume plastic sphere. Limnol. Oceanogr. 8: 166–183.CrossRefGoogle Scholar
  3. Ben-Yaakov, S. 1972. On the CO2-O2 system in the northeastern Pacific. Mar. Chem. 1: 3–26.CrossRefGoogle Scholar
  4. Beyers, R. J., and H. T. Odum. 1959. The use of carbon dioxide to construct pH curves for the measurement of productivity. Limnol. Oceanogr. 4: 499–502.CrossRefGoogle Scholar
  5. Billen, G., C. Joiris, J. Winant, and G. Gillain. 1980. Concentration and metabolism of small organic molecules in estuarine, coastal and open sea environments of the Southern North Sea. Estuarine Coastal Mar. Sei. 11: 279–294.CrossRefGoogle Scholar
  6. Bolin, B., and E. Eriksson. 1959. Changes in the carbon dioxide content of the atmosphere and sea due to fossil fuel combustion, pp. 130–146. In B. Bolin [ed.], Rossby Memorial Volume. Rockefeller Press, New York.Google Scholar
  7. Bryan, J. R., J. P. Riley, and P. J. leB. Williams. 1976. A Winkler procedure for making precise measurements of oxygen concentration for productivity and related studies. J. Exp. Mar. Biol. Ecol. 21: 191–197.CrossRefGoogle Scholar
  8. Carritt, D. E., and J. H. Carpenter. 1966. Comparison and evaluation of currently employed modifications of the Winkler method for determining dissolved oxygen in seawater: a NASCO report. J. Mar. Res. 24: 286–318.Google Scholar
  9. Christensen, J. P., and T. T. Packard. 1979. Respiratory electron transport activities in phytoplankton and bacteria: Comparison of methods. Limnol. Oceanogr. 24: 576–583.CrossRefGoogle Scholar
  10. Codispotti, L. A., G. E. Friederich, R. L. Iverson, and D. W. Wood. 1982. Temporal changes in the inorganic carbon system of the southeast Bering Sea during spring 1980. Nature 296: 242–245.ADSCrossRefGoogle Scholar
  11. Cooper, L. H. N. 1933. Chemical constituents of biological importance in the English Channel, November 1930 to January 1932. Part II. Hydrogen ion concentration, excess base, carbon dioxide and oxygen. J. Mar. Biol. Assoc. UK 18: 729–751.Google Scholar
  12. Crawford, C. C., J. E. Robbie and K. L. Webb. 1974. The utilization of dissolved free amino acids by estuarine microorganisms. Ecology 55: 551–563.CrossRefGoogle Scholar
  13. Davies, J. M., and P. J. leB. Williams. 1984. Verification of 14C and O2 derived primary organic production measurements using an enclosed ecosystem. J. Plank. Res. In press.Google Scholar
  14. Dawson, R., and K. Gocke. 1978. Heterotrophic activity in comparison to the free amino acid concentration in Baltic sea water samples. Oceanol. Acta 1: 45–54.Google Scholar
  15. Derenbach, J. B., and P. J. leB. Williams. 1974. Autotrophic and bacterial production: fractionation of plankton populations by differential filtration of samples from the English Channel. Mar. Biol. 25: 263–269.CrossRefGoogle Scholar
  16. Eppley, R. W. 1980. Estimating phytoplankton growth rates in the central oligotrophic oceans, pp. 231–242. In P. Falkowski [ed.]. Primary Productivity in the Sea. Plenum Press, New York.Google Scholar
  17. Eppley, R. W., and J. H. Sharp. 1975. Photosynthetic measurements in the Central North Pacific. The dark loss of carbon in 24-hr incubations. Limnol. Oceanogr. 20: 981–987.Google Scholar
  18. Eppley, R. W., E. H. Renger, E. L. Venrick, and M. M. Mullin. 1973. A study of plankton dynamics and nutrient cycling in the central gyre of the North Pacific Ocean. Limnol. Oceanogr. 18: 534–551.CrossRefGoogle Scholar
  19. Fuhrman, J. A., and F. Azam. 1980. Bacterial secondary production estimates for coastal waters of British Columbia, Antarctica, and California. Appl. Environ. Microbiol. 39: 1085–1095.Google Scholar
  20. Gaarder, T., and H. H. Gran. 1927. Investigation of the production of plankton in the Oslo Fjord. Rapp. P.V. Cons. Int. Explor. Mer 42: 1–48.Google Scholar
  21. Gamble, J. C., J. M. Davies, and J. H. Steele. 1977. Loch Ewe bag experiment 1974. Bull. Mar. Sei. 27: 146–175.Google Scholar
  22. Gieskes, W. W. C., G. W. Kraay, and M. A. Baars. 1979. Current 14C methods for measuring primary productivity: gross underestimates in oceanic waters. Neth. J. Sea Res. 13: 58–78.CrossRefGoogle Scholar
  23. Gocke, K. 1976. Respiration von gelösten organischen Verbindungen durch naturliche Mikroorganismen-Populationen. Ein Vergleich zwischen verschiedenen Biotopen. Mar. Biol. 35: 375–383.Google Scholar
  24. Harrison, W. G. 1980. Nutrient regeneration and primary production in the sea, pp. 433–460. In: P. Falkowski [ed.]. Primary Productivity in the Sea. Plenum Press, New York.Google Scholar
  25. Robbie, J. E., and C. C. Crawford. 1969. Respiration corrections for bacterial uptake of dissolved organic compounds in natural waters. Limnol. Oceanogr. 14: 528–532.CrossRefGoogle Scholar
  26. Robbie, J. E., O. Holm-Hansen, T. T. Packard, L. R. Pomeroy, R. W. Sheldon, J. P. Thomas, and W. J. Wiebe. 1972. A study of the distribution and activity of microorganisms in ocean water. Limnol. Oceanogr, 17: 544–555.CrossRefGoogle Scholar
  27. Holm-Ransen, O., T. T. Packard, and L. R. Pomeroy. 1970. Efficiency of the reverse-flow filter technique for the concentration of particulate matter. Limnol. Oceanogr. 15: 832–835.CrossRefGoogle Scholar
  28. Itturiaga, R., and G.-G. Hoppe. 1977. Observations of heterotrophic activity in photoassimilated organic matter. Mar. Biol. 40: 101–108.CrossRefGoogle Scholar
  29. Ivanenkov, V. N., V. V. Sapozhnikov, A. M. Chernyackova, and A. N. Jusarova. 1972. Rate of chemical processes in the photosynthetic layer of the tropical Atlantic. Oceanology 12: 207–214.Google Scholar
  30. Johnson, K. M., C. M. Burney, and J. McN. Sieburth. 1981. Enigmatic marine ecosystem metabolism measured by direct diel CO2 and O2 flux in conjunction with DOC release and uptake. Mar. Biol. 65: 49–60.CrossRefGoogle Scholar
  31. Johnson, K. S., R. M. Pytkowicz, and C. S. Wong. 1979. Biological production and the exchange of oxygen and carbon dioxide across the sea surface in Stuart Channel, British Columbia. Limnol. Oceanogr. 24: 474–482.CrossRefGoogle Scholar
  32. Kadota, H., Y. Rata, and H. Miyoshii. 1966. A new method for estimating the mineralization activity of lake water and sediment. Mem. Res. Inst. Food Sei. Kyoto Univ. 27: 28–30.Google Scholar
  33. King, F. D., A. H. Devol, and T. T. Packard. 1978. Plankton metabolic activity in the eastern tropical North Pacific. Deep-Sea Res. 25: 689–704.CrossRefGoogle Scholar
  34. Kuntz, D., T. T. Packard, A. Devol, and J. Anderson. 1975. Chemical, physical and biological observations in the vicinity of the Costa Rica Dome (January-February 1973). Tech. Ref. No. 321, Dept. of Oceanography, Univ. of Washington. 187 pp.Google Scholar
  35. Kuo, H. H., and G. Veronis. 1970. Distribution of tracers in the deep oceans of the world. Deep-Sea Res. 17: 29–46.Google Scholar
  36. Lancelot, C. 1979. Gross excretion rates of natural marine phytoplankton and heterotrophic uptake of excreted products in the Southern North Sea, as determined by short-term kinetics. Mar. Ecol. Prog. Ser. 1: 179–186.CrossRefGoogle Scholar
  37. Larsson, U., and Ä. Hagström. 1979. Phytoplankton exudate release as an energy source for the growth of pelagic bacteria. Mar. Biol. 52: 199–206.CrossRefGoogle Scholar
  38. Menzel, D. W., and J. H. Ryther. 1960. The annual cycle of primary production in the Sargasso Sea off Bermuda. Deep-Sea Res. 6: 351–367.Google Scholar
  39. Münk, W. H. 1966. Abyssal recipes. Deep-Sea Res. 13: 707–730.Google Scholar
  40. Newell, R. C., M. I. Lucas, and E. A. S. Linley. 1981. Rate of degradation and efficiency of conversion of phytoplankton debris by marine microorganisms. Mar. Ecol. Prog. Ser. 6: 123–136.CrossRefGoogle Scholar
  41. Odum, H. T., and C. M. Hoskin. 1958. Comparative studies on the metabolism of marine waters. Publ. Inst. Mar. Sei. Univ. Tex. 5: 16–46.Google Scholar
  42. Packard, T. T. 1971. The measurement of respiratory electron transport activity in marine phytoplankton. J. Mar. Res. 29: 235–244.Google Scholar
  43. Packard, T. T. 1979. Respiration and respiratory electron transport activity in plankton from the Northwest African upwelling area. J. Mar. Res. 37: 711–742.Google Scholar
  44. Packard, T. T., A. H. Devol, and F. D. King. 1975. The effect of temperature on the respiratory electron transport system in marine plankton. Deep-Sea Res. 22: 237–249.Google Scholar
  45. Packard, T. T., D. Harman, and J. Boucher. 1974. Respiratory electron transport activity in plankton from upwelled waters. Tethys 6: 213–222.Google Scholar
  46. Packard, T. T., M. L. Healy, and F. A. Richards. 1971. Vertical distribution of the activity of the respiratory electron transport system in marine plankton. Limnol, Oceanogr. 16: 60–70.CrossRefGoogle Scholar
  47. Packard, T. T., T. Moore, D. Harmon, A. Devol, and F. D. King. 1973. Respiratory electron transport activity in the euphotic zone plankton of the western Mediterranean Sea, North Atlantic Ocean, and the North Pacific Ocean, pp. 201–207. In: J. J. Maclsaac [ed.]. Report of the working conference on a systems approach to eutrophication problems in the eastern Mediterranean. Special Report No. 53 of the Dept. of Oceanography, Univ. of Washington, Seattle. 270 pp.Google Scholar
  48. Packard, T. T., and P. J. leB. Williams. 1981. Respiration and respiratory electron transport activity in sea surface seawater from the northeast Atlantic. Oceanol. Acta. 4: 351–358Google Scholar
  49. Park, K., D. W. Hood, and H. T. Odum. 1958. Diurnal pH variation in Texas bays, and its application to primary production estimation. Publ. Inst. Mar. Sei. Univ. Tex. 5: 47–64.Google Scholar
  50. Parsons, T. R., L. J. Albright, F. Whitney, C. S. Wong, and P. J. leB. Williams. 1981. The effect of glucose on the productivity of sea water: an experimental approach using controlled aquatic ecosystems. Mar. Env. Res. 4: 229–242.CrossRefGoogle Scholar
  51. Parsons, T. R., and J. D. H. Strickland. 1961. On the production of particulate organic carbon by heterotrophic processes in sea water. Deep-Sea Res. 8: 211–222.CrossRefGoogle Scholar
  52. Pomeroy, L. R., and R. E. Johannes. 1966. Total plankton respiration. Deep-Sea Res. 13: 971–973.Google Scholar
  53. Pomeroy, L. R., and R. E. Johannes. 1968. Occurrence and respiration of ultraplankton in the upper 500 metres of the ocean. Deep-Sea Res. 15: 381–391.Google Scholar
  54. Riley, G. A. 1939. Plankton studies III. The Western North Atlantic, May-June 1939. J. Mar. Res. 2: 145–162 .Google Scholar
  55. Riley, G. A. 1941. Plankton studies IV Georges Bank. Bull. Bingham Oceanogr. Collect. 7: 1–74.Google Scholar
  56. Riley, G. A. 1951. Oxygen, phosphate, and nitrate in the Atlantic Ocean. Bull. Bingham Oceanogr. Collect. 13: 1–126.Google Scholar
  57. Ryther, J. H. 1959. Potential productivity of the sea. Science 130: 602–608.ADSCrossRefGoogle Scholar
  58. Schmalz, R. F., and F. J. Swanson. 1969. Diurnal variations in the carbonate saturation of seawater. J. Sediment. Petrol. 39: 255–267.Google Scholar
  59. Setchell, F. W., and T. T. Packard. 1979. Phytoplankton respiration in the Peru upwelling. J. Plankton Res. 1: 343–354.CrossRefGoogle Scholar
  60. Sharp, J. H., M. J. Perry, E. H. Renger, and R. W. Eppley. 1980. Phytoplankton rate processes in the oligotrophic waters of the central North Pacific Ocean. J. Plankton Res. 2: 335–353.CrossRefGoogle Scholar
  61. Sheldon, R. W., and W. H. Sutcliffe. 1978. Generation times of 3 h for Sargasso Sea microplankton as determined by ATP analysis. Limnol. Oceanogr. 23: 1051–1055.CrossRefGoogle Scholar
  62. Shulenberger, E., and J. L. Reid. 1981. The Pacific shallow oxygen maximum deep chlorophyll maximum, and primary production, reconsidered. Deep-Sea Res. 28: 901–919.CrossRefGoogle Scholar
  63. Sieburth, J. McN. 1977. International Helgoland Symposium: Convenor’s report on the informal session on biomass and productivity of microorganisms in planktonic ecosystems. Helgol. Wiss. Meeresunters. 30: 697–704.CrossRefGoogle Scholar
  64. Slawyk, G., H. J. Minas, and T. T. Packard. 1976. A further Investigation on the primary productivity in the divergent zone near the French Mediterranean Coast. Int. Revue ges. Hydrobiol. 61: 373–381.CrossRefGoogle Scholar
  65. Smith, S. V. 1973. Carbon dioxide dynamics: a record of organic carbon production, respiration, and calcification in the Eniwetok reef flat community. Limnol. Oceanogr. 18: 106–120.CrossRefGoogle Scholar
  66. Smith, S. v., and J. A. Marsh. 1973. Organic carbon production on the windward reef flat of Eniwetok Atoll. Limnol. Oceanogr. 18: 953–961.CrossRefGoogle Scholar
  67. Smith, W. O. 1977. The respiration of photosynthetic carbon in eutrophic areas of the ocean. J. Mar. Res. 35: 557–565.ADSGoogle Scholar
  68. Smith, W. O., R. T. Barber, and S. A. Huntsman. 1977. Primary production off the coast of Northwest Africa: excretion of dissolved organic matter and its heterotrophic uptake. Deep-Sea Res. 24: 35–47.CrossRefGoogle Scholar
  69. de Souza Lima, H., and P. J. leB. Williams. 1978. Oxygen consumption by the planktonic population of an estuary. Estuarine Coastal Mar. Sei. 6: 515–521.CrossRefGoogle Scholar
  70. Steele, J. H., D. W. Farmer, and E. W. Henderson. 1977. Temperature structure in large marine enclosures. J. Fish. Res. Board Canada 34: 1095–1104.CrossRefGoogle Scholar
  71. Steemann Nielsen, E. 1952. The use of radioactive carbon (14C) for measuring organic production in the sea. J. Cons. Explor. Mer 18: 117–140.Google Scholar
  72. Steemann Nielsen, E. 1955. The interaction of photosynthesis and respiration and its importance for the determination of 14C- discrimination in photosynthesis. Physiol. Plant. 8: 945–953.CrossRefGoogle Scholar
  73. Tailing, J. F. 1973. The application of some electrochemical methods to the measurement of photosynthesis and respiration in fresh waters. Freshw. Biol. 3: 335–362.CrossRefGoogle Scholar
  74. Teal, J. M., and J. Kanwisher. 1966. The use of pCO2 for the calculation of biological production, with examples from waters off Massachusetts. J. Mar. Res. 24: 4–14.Google Scholar
  75. Tijssen, S. B. 1979. Diurnal oxygen rhythm and primary production in the mixed layer of the Atlantic Ocean at 20°N. Neth. J. Sea Res. 13: 79–84.CrossRefGoogle Scholar
  76. Tijssen, S. B., and B. Eijgenraam. 1980. Diurnal oxygen rhythm in the Southern Bight of the North Sea: net and gross production in April 1980 in a Phaeocystis bloom. ICES C.M. 1980/C:17.Google Scholar
  77. Vinogradov, M. E., V. V. Menshutkin, and E. A. Shushkina. 1972. On a mathematical simulation of a pelagic ecosystem in tropical waters of the ocean. Mar. Biol. 16: 261–268.CrossRefGoogle Scholar
  78. Vinogradov, M. Y., V. F. Krapivin, V. V. Menshutkin, B. S. Fleyshman, and E. A. Shushkina. 1973. Mathematical model of the functions of the pelagic ecosystem in tropical regions (from 50th voyage of the R/V Vityaz). Oceanology 13: 704–717.Google Scholar
  79. Weichart, G. 1980. Chemical changes and primary productionin the Fladen Ground area (North Sea) during the first phase of the spring phytoplankton bloom. “Meteor” Forsch.-Ergebnisse 22: 79–86.Google Scholar
  80. Wiebe, W. J., and D. F. Smith. 1977. Direct measurement of dissolved organic carbon release by phytoplankton and incorporation by microheterotrophs. Mar. Biol. 42: 213–223.CrossRefGoogle Scholar
  81. Williams, P. J. leB. 1970. Heterotrophic utilization of dissolved organic compounds in the sea. I. Size distribution of population and relationship between respiration and incorporation of growth substances. J. Mar. Biol. Assoc. UK 50: 859–870.CrossRefGoogle Scholar
  82. Williams, P. J. leB. 1973. On the question of growth yields of natural heterotrophic populations, pp. 399–400. In: T. Rosswall [ed.]. Modern Methods in the Study of Microbial Ecology. Bull. Ecol. Res. Comm. (Stockholm) 1973. Swedish Natural Science Research Council.Google Scholar
  83. Williams, P. J. leB. 1981a. Microbial contribution to overall marine plankton metabolism: direct measurements of respiration. Oceanol. Acta 4: 359–364.Google Scholar
  84. Williams, P. J. leB. 1981b. Incorporation of microbeterotrophic processes into the classical paradigm of the planktonic food web. 15th European Symposium on Marine Biology, Kiel, F.G.R. Kiel. Meei;esforsch. 5: 1–28.Google Scholar
  85. Williams, P. J. leB. 1981c. Microbial contribution to overall plankton community respiration - studies in CEE’s, pp. 305–321. In; G. D. Grice and H. R. Reeve [eds.]. Marine Mesocosms: Biological and Chemical Research in Experimental Ecosystems. Springer-Verlag, Berlin.Google Scholar
  86. Williams, P. J. leB. Bacterial production in the marine food chain: the emperor’s new suit of clothes. In: M. J. Fasham [ed.]. Flow of Energy and Material in Marine Ecosystems: Theory and Practice. Plenum, New York. In press.Google Scholar
  87. Williams, P. J. leB., and C. Askew. 1968. A method of measuring the mineralization by microorganisms of organic compounds in sea water. Deep-Sea Res. 15: 365–375.Google Scholar
  88. Williams, P. J. leB., T. Berman, and O. Holm-Hansen. 1976. Amino acid uptake and respiration by marine heterotrophs. Mar. Biol. 35: 41–47.CrossRefGoogle Scholar
  89. Williams, P. J. leB., K. R. Heinemann, J. Marra, and D. A. Purdie. 1983. Comparison of 14C and O2 measurements of phytoplankton production in oligotrophic waters. Nature (London) 305:49–50.ADSCrossRefGoogle Scholar
  90. Williams, P. J. leB., and N. W. Jenkinson. 1982. A transportable microprocessor-controlled precise Winkler titration suitable for field station and shipboard use. Limnol. Oceanogr. 27: 576–584.CrossRefGoogle Scholar
  91. Williams, P. J. leB., and C. S. Yentsch. 1976. An examination of photosynthetic production, excretion of photosynthetic products, and heterotrophic utilization of dissolved organic compounds with reference to results from a coastal subtropical sea. Mar. Biol. 35: 31–40.CrossRefGoogle Scholar
  92. Wong, C. S., R. D. Bellegay, and A. B. Cornford. 1975. Measurable inorganic carbon parameters in seawater, pp. 47–57. Spec. Tech. Publ. No. 573. Am. Soc. Testing and Materials, Philadelphia.Google Scholar
  93. Wyrtki, K. 1962. The oxygen minimum in relation to oceanic circulation. Deep-Sea Res. 9: 11–23.Google Scholar

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© Plenum Press, New York 1984

Authors and Affiliations

  • P. J. leB. Williams
    • 1
  1. 1.Department of OceanographySouthampton UniversitySouthamptonEngland

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