Skip to main content
Log in

Diel variation of TCO2 in the upper layer of oceanic waters reflects microbial composition, variation and possibly methane cycling

  • Published:
Marine Biology Aims and scope Submit manuscript

Abstract

Six diel TCO2 cycles determined by infrared (IR) photometry from five drift stations occupied between 24 February and 16 March 1979 in the mixed layer of the northwestern Caribbean Sea are examined. Comparison of TCO2 variation with coincident salinity and O2 variation demonstrated that TCO2 often co-varied with these independently measured variables. During five diel cycles TCO2 variation was characterized by nocturnal production and diurnal consumption. The inverse, diurnal production of CO2, occurred downstream from Misteriosa Bank, whose corals apparently contributed to a water mass having a twofold increase of POC and a sixfold larger population of heterotrophic nanoplankters. For the five diel studies carried out in waters with balanced or nearly blanced heterotrophic and phototrophic components of the nanoplankton, CO2 consumption at constant salinity always occurred between 06.00 and 09.00 hrs. Net uptake often continued through 15.00 hrs, but not always in the absence of significant salinity changes. At constant salinity net O2 evolution never exceeded 0.5 μmol l-1 h-1 while net CO2 uptake consistently averaged 3 μmol l-1 h-1 for an apparent net production of 36 mg C m-3 h-1, which greatly exceeds the O2 changes and open ocean 14C estimates from the literature. Diurnal consumption was apparently balanced by nocturnal production of CO2 so that no significant net daily change in TCO2 was observed. Departures from theoretical PQ and RQ and the possibility of nocturnal variations in formaldehyde and carbonate alkalinity imply that chemotrophs, both methane producers and methane oxidizers, play a significant role in CO2 cycling. This could be through the metabolism of the nonconservative gases CH4, CO, and H2, and a link between chemotrophy and phototrophy through these gases is hypothesized. These open system measurements were subject to diffusion and documentable patchiness, but temporal TCO2 changes appear to indicate the net direction of microbiological activity and join a growing body of literature showing dynamic variation in CO2 and O2 that exceeds estimates by 14C bottle assays of carbon fixation.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

Literature cited

  • Burney, C. M., P. G. Davis, K. M. Johnson and J. McN. Sieburth: Dependence of dissolved carbohydrate concentrations upon small scale nanoplankton and bacterioplankton distributions in the western Sargasso Sea. Mar. Biol. 65, 289–296 (1981)

    Google Scholar 

  • Burney, C. M., P. G. Davis, K. M. Johnson and J. McN. Sieburth: Diel relationships of microbial trophic groups and in-situ dissolved carbohydrate dynamics in the Caribbean Sea. Mar. Biol. 67, 311–322 (1982)

    Google Scholar 

  • Burney, C. M., K. M. Johnson, D. M. Lavoie and J. McN. Sieburth: Dissolved carbohydrate and microbial ATP in the North Atlantic: concentrations and interactions. Deep-Sea Res. 26A, 1267–1290 (1979)

    Google Scholar 

  • Carpenter, E. J. and J. S. Lively: Review of estimates of algal growth using 14C tracer techniques. In: Primary productivity in the sea, pp 167–178. Ed. by P. G. Falkowski. New York: Plenum Press 1980

    Google Scholar 

  • Cassell, E. A.: Rapid graphical method for estimating the precision of direct microscopic counting data. Appl. Microbiol. 13, 293–296 (1965)

    Google Scholar 

  • Conrad, R., W. Seiler, G. Bunse and H. Giehl: Carbon monoxide in seawater (Atlantic Ocean). J. geophys. Res. 87, 8839–8852 (1982)

    Google Scholar 

  • Cooper, W. J. and R. G. Zika: Photochemical formation of hydrogen peroxide in surface and ground waters exposed to sunlight. Science, N.Y. 220, 711–712 (1983)

    Google Scholar 

  • Daniels, L., G. Fuchs, R. K. Thauer and J. G. Zeikus: Carbon monoxide oxidation by methanogenic bacteria. J. Bacteriol. 132, 118–126 (1977)

    Google Scholar 

  • Davis, P. G. and J. McN. Sieburth: Differentiation of phototrophic and heterotrophic nanoplankton in marine waters by epifluorescence microscopy. Ann. Inst. Oceanogr., Paris, 58(s): 249–260 (1982)

    Google Scholar 

  • Ducklow, H. W. and R. Mitchell: Bacterial populations and adaptations in the mucus layers on living corals. Limnol. Oceanogr. 24, 715–725 (1979)

    Google Scholar 

  • Eppley, R. W.: Estimating phytoplankton growth rates in the central oligotrophic oceans. In: Primary productivity in the sea, pp 231–242. Ed. by P. G. Falkowski, New York: Plenum Press 1980

    Google Scholar 

  • Fenchel, T. and T. H. Blackburn: Bacterial and mineral cycling, 25 pp. New York: Academic Press 1979

    Google Scholar 

  • Ferguson, R. L. and A. V. Palumbo: Distribution of suspended bacteria in neritic waters south of Long Island during stratified conditions. Limnol. Oceanogr. 24, 697–705 (1979)

    Google Scholar 

  • Fuhrman, J. A., F. Azam, R. W. Eppley and A. Hagstrom: Diel variations in phytoplankton, bacterioplankton, and related parameters in the southern California bight. EOS 63, 946 (1982)

    Google Scholar 

  • Gieskes, W. W. C., G. W. Kraay and M. A. Baars: Current 14C methods for measuring primary production: gross underestimates in oceanic waters. Neth. J. Sea Res. 13, 58–78 (1979)

    Google Scholar 

  • Goldman, J. C., J. J. McCarthy and D. G. Peavey: Growth rate influence on the chemical composition of phytoplankton in oceanic waters. Nature, Lond. 279, 210–215 (1979)

    Google Scholar 

  • Griffiths, R. P., B. A. Caldwell, J. D. Cline, W. A. Broich and R. Y. Morita: Field observations of methane concentrations and oxidation rates in the Southeastern Bering Sea. Appl. environ. Microbiol. 44, 435–446 (1982)

    Google Scholar 

  • Herr, F. L., M. I. Scranton and W. R. Barger: Dissolved hydrogen in the Norwegian Sea: mesoscale surface variability and deepwater distribution. Deep-Sea Res. 28A, 1001–1016 (1981)

    Google Scholar 

  • Higgins, I. J., D. J. Best and R. C. Hammond: New findings in methane-utilizing bacteria highlight their importance in the biosphere and their commerical potential. Nature, Lond. 286, 561–564 (1980)

    Google Scholar 

  • Higgins, I. J., D. J. Best, R. C. Hammond and D. Scott: Methane-oxidizing microorganisms. Microbiol. Rev. 45, 556–590 (1981)

    Google Scholar 

  • Hobbie, J. E., R. J. Daley and S. Jasper: Use of Nuclepore filters for counting bacteria by fluorescence microscopy. Appl. environ. Microbiol. 33, 1225–1228 (1977)

    Google Scholar 

  • Hoffman, P. S., L. Pine, and S. Bell: Production of superoxide and hydrogen peroxide in medium used to culture Legionella pneumophila: catalytic decomposition by charcoal. Appl. environ. Microbiol. 45, 784–791 (1983)

    Google Scholar 

  • Hood, D. W.: Preliminary observations of the carbon budget of the eastern Bering Sea Shelf. In: The Bering Sea Shelf: oceanography and resources, pp 347–358, Vol. 1. Ed. by Hood and Caldor. Seattle: University of Washington Press 1981

    Google Scholar 

  • Jenkins, W. J.: Oxygen utilization rates in North Atlantic subtropical gyre and primary production in oligotrophic systems. Nature, Lond. 300, 246–248 (1982)

    Google Scholar 

  • Johannes, R. E.: Ecology of organic aggregates in the vicinity of a coral reef. Limnol. Oceanogr. 12, 189–195 (1967)

    Google Scholar 

  • Johnson, K. M., C. M. Burney and J. McN. Sieburth: Enigmatic marine ecosystem metabolism measured by direct diel TCO2 and O2 flux in conjunction with DOC release and uptake. Mar. Biol. 65, 49–60 (1981a)

    Google Scholar 

  • Johnson, K. M., C. M. Burney and J. McN. Sieburth: Doubling the production and precision of the MBTH spectrophotometric assay for dissolved carbohydrates in seawater. Mar. Chem. 10, 467–473 (1981b)

    Google Scholar 

  • Johnson, K. M., C. M. Burney and J. McN. Sieburth: Precise and accurate determination by infrared photometry of CO2 dynamics in marine ecosystems. Mar. Ecol. Prog. Ser. 10, 251–256 (1983)

    Google Scholar 

  • Johnson, K. M. and J. McN. Sieburth: Dissolved carbohydrates in seawater. I, A precise spectrophotometric analysis for monosaccharides. Mar. Chem. 5, 1–13 (1977)

    Google Scholar 

  • Johnson, P. W. and J. McN. Sieburth: Chroococcoid cyanobacteria in the sea: a ubiquitous and diverse phototrophic biomass. Limnol. Oceanogr. 24, 928–935 (1979)

    Google Scholar 

  • Junge, C., W. Seiler, R. Bock, K. D. Greese and F. Radler: Über die CO-produktion von Mikroorganismen. Naturwiss. 58, 362–363 (1971)

    Google Scholar 

  • Kerr, R. A. and J. G. Quinn: Chemical studies on the dissolved organic matter in seawater. Isolation and fractionation. Deep-Sea Res. 22, 107–116 (1975)

    Google Scholar 

  • Marshall, N.: Detritus over the reef and its potential contribution to adjacent waters of Eniwetok Atoll. Ecology 46, 343–344 (1965)

    Google Scholar 

  • Menzel, D. W. and R. F. Vaccaro: The measurement of dissolved organic and particulate carbon in seawater. Limnol. Oceanogr. 9, 138–142 (1964)

    Google Scholar 

  • Mopper, K. and P. Lindroth: Diel and depth variations in dissolved free amino acids and ammonium in the Baltic Sea determined by shipboard HPLC analysis. Limnol. Oceanogr. 27, 336–347 (1982)

    Google Scholar 

  • Nixon, S. W., C. A. Oviatt, J. Garber and V. Lee: Diel metabolism and nutrient dynamics in a salt marsh embayment. Ecology 57, 740–750 (1976)

    Google Scholar 

  • Odum, H. T. and C. M. Hoskin: Comparative studies on the metabolism of marine waters. Publ. Inst. mar. Sci., Univ. Texas 5, 16–46 (1958)

    Google Scholar 

  • Olson, R. J.: Differential photoinhibition of marine nitrifying bacteria: a possible mechanism for the formation of the primary nitrite maximum. J. mar. Res. 39, 227–238 (1981)

    Google Scholar 

  • Padgett, P. J., W. H. Cover, and N. R. Krieg: The microaerophile Spirillum volutans: cultivation on complex liquid and solid media. Appl. environ. Microbiol. 43, 469–477 (1982)

    Google Scholar 

  • Park, K., D. W. Hood and H. T. Odum: Diurnal pH variation in Texas bays, and its application to primary production estimation. Publ. Inst. mar. Sci., Univ. Texas 5, 47–64 (1958)

    Google Scholar 

  • Parsons, T. R., K. Stephens and J. D. H. Strickland: On the chemical composition of eleven species of marine phytoplankters. J. Fish. Res. Bd Can. 18, 1001–1016 (1961)

    Google Scholar 

  • Quayle, J. R.: The metabolism of one-carbon compounds by microorganisms. Adv. microbial Physiol. 7, 119–203 (1972)

    Google Scholar 

  • Rich, P. A.: Differential CO2 and O2 benthic community metabolism in a softwater lake. J. Fish. Res. Bd Can. 36, 1377–1389 (1979)

    Google Scholar 

  • Rudd, J. W. M. and C. D. Taylor: Methane cycling in aquatic environments. Adv. aquat. Microbiol. 2, 77–150 (1980)

    Google Scholar 

  • Salonen, K. and A.-L. Holopainen: A comparison of methods for the estimation of phytoplankton primary production. Int. Revue ges. Hydrobiol. 64, 147–155 (1979)

    Google Scholar 

  • Schindler, D. W. and E. J. Fee: Diurnal variation of dissolved inorganic carbon and its use in estimating primary production and CO2 invasion in Lake 227. J. Fish. Res. Bd Can. 30, 1501–1510 (1973)

    Google Scholar 

  • Seki, H.: Relation between production and mineralization of organic matter in Aburatsubo Inlet, Japan, J. Fish. Res. Bd Can. 25, 625–637 (1968)

    Google Scholar 

  • Shulenberger, E. and J. L. Reid: The Pacific shallow oxygen maximum, deep chlorophyll maximum, and primary productivity, reconsidered. Deep-Sea Res. 28A, 901–919 (1981)

    Google Scholar 

  • Sieburth, J. McN.: International Helgoland Symposium: Convener's report on the Informal Session on biomass and productivity of microorganisms in planktonic ecosystems. Helgol. wiss. Meeresunters. 30, 697–704 (1977)

    Google Scholar 

  • Smith, S. V. and P. Kroopnick: Carbon-13 isotopic fractionation as a measure of aquatic metabolism. Nature, Lond. 294, 252–253 (1981)

    Google Scholar 

  • Sorokin, Yu. I.: Bacterial populations as components of oceanic ecosystems. Mar. Biol. 11, 101–105 (1971)

    Google Scholar 

  • Sournia, A.: Circadian periodicities in natural populations of marine phytoplankton. Adv. mar. Biol. 12, 325–389 (1974)

    Google Scholar 

  • Sournia, A.: B. Delesalle and M. Ricard: Premiers bilans de production organique et de calcification d'un récif-barrière de la Polynésie Francaise. Oceanol. Acta 4, 423–431 (1981)

    Google Scholar 

  • Strathmann, R. R.: Estimating the organic carbon content of phytoplankton from cell volume or plasma volume. Limnol. Oceanogr. 12, 411–418 (1967)

    Google Scholar 

  • Swinnerton, J. W., V. J. Linnenbom and R. A. Lamontagne: The ocean: a natural source of carbon monoxide. Science, N.Y. 167, 984–986 (1970)

    Google Scholar 

  • Taguchi, S. and T. Platt: Assimilation of 14CO2 in the dark compared to phytoplankton production in a small coastal inlet. Estuar. coasto. mar. Sci. 5, 679–684 (1977)

    Google Scholar 

  • Taylor, G. T. and S. J. Pirt: Nutrition and factors limiting the growth of a methanogenic bacterium. Arch. Microbiol. 113, 17–22 (1977)

    Google Scholar 

  • Teal, J. M. and J. Kanwisher: The use of pCO2 for the calculation of biological production, with examples from waters off Massachusetts. J. mar. Res. 24, 4–14 (1966)

    Google Scholar 

  • Tijssen, S. B.: Diurnal oxygen rhythm and primary production in the mixed layer of the Atlantic Ocean at 20° N. Neth. J. Sea Res. 13, 79–84 (1979)

    Google Scholar 

  • Venrick, E. L., J. R. Beers and J. F. Heinbokel: Possible consequences of containing microplankton for physiological rate measurements. J. exp. mar. Biol. Ecol. 26, 55–76 (1977)

    Google Scholar 

  • Verduin, J.: Phytoplankton communities of western Lake Erie and the CO2 and O2 changes associated with them. Limnol. Oceanogr. 5, 372–380 (1960)

    Google Scholar 

  • Weichart, G.: Chemical changes and primary production in the Fladen Ground area (North Sea) during the first phase of a spring phytoplankton bloom. “METEOR” Forschungs., Reihe A, 22, 79–86 (1980)

    Google Scholar 

  • Wesely, M. L., D. R. Cook, R. L. Hart and R. M. Williams: Air-sea exchange of CO2 and evidence for enhanced upward fluxes. J. geophys. Res. 87, 8827–8832 (1982)

    Google Scholar 

  • Williams, P. J. LeB: Incorporation of microheterotrophic processes into the classical paradigm of the planktonic food web. Kieler Meeresforsch. 5, 1–28 (1981)

    Google Scholar 

  • Wilson, D. F., J. W. Swinnerton and R. A. Lamontagne: Production of carbon monoxide and gaseous hydrocarbons in seawater: relation to dissolved organic carbon. Science, N.Y. 168, 1577–1579 (1970)

    Google Scholar 

  • Wood, J. M., I. Moura, J. J. G. Moura, M. H. Santos, A. V. Xavier, J. LeGall and M. Scandellari: Role of vitamin B 12 in methyl transfer for methane biosynthesis by Methanosarcina barkeri. Science, N.Y. 216, 303–305 (1982)

    Google Scholar 

  • Wood, K. G. and J. Verduin: Correlation between CO2 and O2 concentrations in Lake Erie, USA. Arch. Hydrobiol. 71, 1–16 (1972)

    Google Scholar 

  • Wüst, G.: Stratification and circulation in the Antillean-Caribbean Basins, 201 pp. New York: Columbia University Press 1964

    Google Scholar 

  • Zika, R. G.: Marine organic photochemistry. In: Marine organic chemistry, pp 299–325. Ed. by E. K. Duursma and R. Dawson. Amsterdam: Elsevier Scientific Publ. Co. 1981

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Additional information

Communicated by S. K. Pierce, College Park

Rights and permissions

Reprints and permissions

About this article

Cite this article

Johnson, K.M., Davis, P.G. & Sieburth, J.M. Diel variation of TCO2 in the upper layer of oceanic waters reflects microbial composition, variation and possibly methane cycling. Mar. Biol. 77, 1–10 (1983). https://doi.org/10.1007/BF00393204

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00393204

Keywords

Navigation