Biomass distribution in marine planktonic communities

Patterns in primary production and carbon export from the euphotic zone suggest that the relative contribution of planktonic heterotrophs to community biomass should decline along gradients of phytoplankton biomass and primary production. Here, we use an extensive literature data survey to test the hypothesis that the ratio of total heterotrophic (bacteria + protozoa + mesozooplankton) biomass to total autotrophic biomass (H : A ratio) is not constant in marine plankton communities but rather tends to decline with increasing phytoplankton biomass and primary production. Our results show that the plankton of unproductive regions are characterized by very high relative heterotrophic biomasses resulting in inverted biomass pyramids, whereas the plankton of productive areas are characterized by a smaller contribution of heterotrophs to community biomass and a normal biomass pyramid with a broad autotrophic base. Moreover, open‐ocean communities support significantly more heterotrophic biomass in the upper layers than do coastal communities for a given autotrophic biomass. These differences in the biomass structure of the community could be explained by the changes in the biomass‐specific rates of phytoplankton production that seem to occur from ultraoligotrophic to eutrophic marine regions, but other factors could also generate them. The patterns described suggest a rather systematic shift from consumer control of primary production and phytoplankton biomass in open ocean to resource control in upwelling and coastal areas.

[1]  P. Rodhouse,et al.  Abundance of gelatinous carnivores in the nekton community of the Antarctic polar frontal zone in summer 1994 , 1996 .

[2]  P. Tortell,et al.  The role of heterotrophic bacteria in iron-limited ocean ecosystems , 1996, Nature.

[3]  G. Paffenhöfer,et al.  Composition and biomass of plankton in spring on the Cape Hatteras shelf, with implications for carbon flux , 1996 .

[4]  Francisco P. Chavez,et al.  Basin-wide distributions of living carbon components and the inverted trophic pyramid of the central gyre of the North Atlantic Ocean, summer 1993 , 1996 .

[5]  B. Riemann,et al.  Ecological importance of bacterivorous, pigmented flagellates (mixotrophs) in the Bay of Aarhus, Denmark , 1996 .

[6]  D. Stoecker,et al.  Micro- and mesoprotozooplankton at 140*W in the equatorial Pacific: heterotrophs and mixotrophs , 1996 .

[7]  P. Verity,et al.  Visualization and quantification of plankton and detritus using digital confocal microscopy , 1996 .

[8]  William K. W. Li,et al.  DNA distributions in planktonic bacteria stained with TOTO or TO‐PRO , 1995 .

[9]  D. Lindell,et al.  Ultraphytoplankton succession is triggered by deep winter mixing in the Gulf of Aqaba (Eilat), Red Sea , 1995 .

[10]  E. Haugen,et al.  Overestimation of heterotrophic bacteria in the Sargasso Sea: direct evidence by flow and imaging cytometry , 1995 .

[11]  J. Gasol,et al.  Biomass Distribution in Freshwater Plankton Communities , 1995, The American Naturalist.

[12]  M. Fasham Variations in the seasonal cycle of biological production in subarctic oceans: A model sensitivity analysis , 1995 .

[13]  Michael R. Roman,et al.  Spatial and temporal changes in the partitioning of organic carbon in the plankton community of the Sargasso Sea off Bermuda , 1995 .

[14]  K. Banse Zooplankton: Pivotal role in the control of ocean production I. Biomass and production , 1995 .

[15]  D. Caron,et al.  Mixotrophic nanoplankton in oligotrophic surface waters of the Sargasso Sea may employ phagotrophy to obtain major nutrients , 1995 .

[16]  R. Feely,et al.  Physical and Biological Controls on Carbon Cycling in the Equatorial Pacific , 1994, Science.

[17]  C. Duarte,et al.  The dependence of herbivory on growth rate in natural plant communities , 1994 .

[18]  M. Pace,et al.  Why does the relationship between sinking flux and planktonic primary production differ between lakes and oceans , 1994 .

[19]  D. Vaulot,et al.  Photosynthetic picoplankton community structure in the subtropical North Pacific Ocean near Hawaii (station ALOHA) , 1993 .

[20]  Nelson G. Hairston,et al.  Cause-Effect Relationships in Energy Flow, Trophic Structure, and Interspecific Interactions , 1993, The American Naturalist.

[21]  M. Veldhuis,et al.  Cell abundance and fluorescence of picoplankton in relation to growth irradiance and nitrogen availability in the red sea , 1993 .

[22]  Peter A. Jumars,et al.  Concepts in Biological Oceanography: An Interdisciplinary Primer , 1993 .

[23]  B. Monger,et al.  Flow Cytometric Analysis of Marine Bacteria with Hoechst 33342 , 1993, Applied and environmental microbiology.

[24]  C. Duarte,et al.  Self-regulation, bottom-up, and top-down control of phytoplankton communities : a reply to the comment by Kamenir , 1992 .

[25]  A. Wood,et al.  Biomass of bacteria, cyanobacteria, prochlorophytes and photosynthetic eukaryotes in the Sargasso Sea , 1992 .

[26]  A. Longhurst Role of the marine biosphere in the global carbon cycle , 1991 .

[27]  J. Cullen Hypotheses to explain high-nutrient conditions in the open sea , 1991 .

[28]  Donald A. Jackson,et al.  Ratios in aquatic sciences : statistical shortcomings with mean depth and the morphoedaphic index , 1990 .

[29]  D. Vaulot,et al.  Winter presence of prochlorophytes in surface waters of the northwestern Mediterranean Sea , 1990 .

[30]  P. Wassmann Relationship between primary and export production in the boreal coastal zone of the North Atlantic , 1990 .

[31]  Q. Dortch,et al.  Differences in biomass structure between oligotrophic and eutrophic marine ecosystems , 1989 .

[32]  D. Strayer On the limits to secondary production , 1988 .

[33]  Farooq Azam,et al.  Major role of bacteria in biogeochemical fluxes in the ocean's interior , 1988, Nature.

[34]  D. Stoecker,et al.  Large proportion of marine planktonic ciliates found to contain functional chloroplasts , 1987, Nature.

[35]  M. D. Keller,et al.  How important are oceanic algal nanoflagellates in bacterivory?1 , 1986 .

[36]  E. Laws,et al.  High phytoplankton growth and production rates in oligotrophic Hawaiian coastal waters1 , 1984 .

[37]  J. C. Goldman,et al.  Growth rate influence on the chemical composition of phytoplankton in oceanic waters , 1979, Nature.

[38]  Y. Sorokin The heterotrophic phase of plankton succession in the Japan Sea , 1977 .

[39]  R. W. Sheldon,et al.  The Size Distribution of Particles in the OCEAN1 , 1972 .

[40]  H. Odum,et al.  Fundamentals of ecology , 1954 .

[41]  J. Jellett,et al.  DNA distribut : ions in planktonic bacteria stained with TOT 0 or TO-PRO , 1999 .

[42]  R. Olson,et al.  Dynamics of picophytoplankton, ultraphytoplankton and bacteria in the central equatorial Pacific , 1996 .

[43]  F. Rassoulzadegan,et al.  Seasonal variations of mixotrophic ciliates in the northwest Mediterranean Sea , 1994 .

[44]  Roger I. Jones,et al.  Mixotrophy in planktonic protists as a spectrum of nutritional strategies. , 1994 .

[45]  S. Agustí Planktonic size structure and the photon budget of the euphotic ocean , 1994 .

[46]  W. Wiebe,et al.  Energy sources for microbial food webs , 1993 .

[47]  H. Ducklow,et al.  Stocks and dynamics of bacterioplankton carbon during the spring bloom in the eastern North Atlantic Ocean , 1993 .

[48]  M. Veldhuis,et al.  Growth and Fluorescence Characteristics of Ultraplankton on a North South Transect in the Eastern North-Atlantic , 1993 .

[49]  J. Dolan Mixotrophy in ciliates: a review of Chlorella symbiosis and chloroplast retention , 1992 .

[50]  P. Bienfang,et al.  The Role of Coastal High Latitude Ecosystems in Global Export Production , 1992 .

[51]  F. Azam,et al.  Significance of bacterial biomass in lakes and the ocean: comparison to phytoplankton biomass and biogeochemical implications , 1992 .

[52]  P. J. Hansen Quantitative importance and trophic role of heterotrophic dinoflagellates in a coastal pelagial food web , 1991 .

[53]  R. Sanders Mixotrophic Protists in Marine and Freshwater Ecosystems , 1991 .

[54]  G. Ærtebjerg,et al.  Picoalgae in Danish coastal waters during summer stratification , 1991 .

[55]  R. Psenner From image analysis to chemical analysis of bacteria: A long-term study? , 1990 .

[56]  F. Azam,et al.  Biogeochemical significance of bacterial biomass in the ocean's euphotic zone , 1990 .

[57]  H. Kaas,et al.  The structure of the pelagic food web in relation to water column structure in the Skagerrak , 1990 .

[58]  O. Holm‐Hansen,et al.  Microbial autotrophic and heterotrophic eucaryotes in Antarctic waters : relationships between biomass and chlorophyll, adenosine triphosphate and particulate organic carbon , 1990 .

[59]  J. Fuhrman,et al.  Dominance of bacterial biomass in the Sargasso Sea and its ecological implications , 1989 .

[60]  K.,et al.  Abundance of autotrophic, mixotrophic, and heterotrophic planktonic ciliates in shelf and slope waters. , 1989 .

[61]  D. Cushing A difference in structure between ecosystems in strongly stratified waters and in those that are only weakly stratified , 1989 .

[62]  Peter H. Wiebe,et al.  Functional regression equations for zooplankton displacement volume, wet weight, dry weight, and carbon : a correction , 1988 .

[63]  G. Paffenhöfer,et al.  Why is Acartia tonsa (Copepoda: Calanoida) restricted to nearshore environments? , 1988 .

[64]  K. Y. Bφrshiem Cell volume to carbon conversion factors for a bacterivorous Monas sp. enriched from seawatr. , 1987 .

[65]  S. C. M. O'Hara,et al.  The Biological chemistry of marine copepods , 1986 .

[66]  T. Packard,et al.  Measurement of electron transport activity of microplankton , 1985 .

[67]  M. Estrada,et al.  Particulate carbon and nitrogen and plankton biomass in oligotrophic and upwelling systems , 1985 .

[68]  N. Welschmeyer,et al.  Carbon‐14 labeling of phytoplankton carbon and chlorophyll a carbon: Determination of specific growth rates1 , 1984 .

[69]  G. Harris Phytoplankton productivity and growth measurements: past, present and future , 1984 .

[70]  P. Holligan,et al.  Vertical distribution and partitioning of organic carbon in mixed frontal and stratified waters of the English Channel , 1984 .

[71]  J. G. Field,et al.  The Ecological Role of Water-Column Microbes in the Sea* , 1983 .

[72]  L. Pomeroy,et al.  Heterotrophic-photoautotrophic index: a qualitative parameter of microbial interactions applied to a Gulf Stream intrusion , 1979 .

[73]  S. Chisholm,et al.  PARTICULATE ORGANIC MATTER IN SURFACE WATERS OFF SOUTHERN CALIFORNIA AND ITS RELATIONSHIP TO PHYTOPLANKTON. , 1977 .

[74]  Charles C. Elton Animal Ecology , 1927, Nature.