Microb Ecol (1994) 28:251-253
Controls of the Microbial Loop: Biotic Factors
MICROBIAL ECOLOGY © 1994Springer-VerlagNew York Inc.
Musings on the Microbial Loop: Twenty Years After T. Berman,1 L. Stone 2 1Israel Oceanographic & Linmological Research, Yigal Allon Kinneret Limnological Laboratory, P.O. Box 345, Tiberias, Israel 14102 2Department of Zoology, Tel Aviv University, Ramat Aviv, Israel 69978
Pomeroy's seminal paper [2] synthesized information then available on oceanic food webs and presented a more complete picture of pelagic ecosystems than that previously perceived. This paper laid the "ideological" foundation for the wealth of new information on the structure and function of microbial food webs that would be amassed in the subsequent 20 years. It took some years before others [1, 3], on the basis of new results and observations, examined in some detail Pomeroy's paradigm of oceanic food webs focusing on the "microbial loop." The new perception of bacterial and protist involvement both in terms of biomass and metabolic activity in pelagic ecosystems was made possible only by the development of new methodologies: epifluorescent microscopy and nucleic acid staining for direct counting of microbial cells, [3H]thymidine and [3H]leucine determinations of bacterial production, and radioactive and fluorescent tagging of bacteria and algal cells to follow grazing rates on these organisms. The implications of the new oceanic paradigm became, after a characteristic time delay, evident also to limnologists so that the emphasis towards understanding microbial food webs has also been felt in freshwater studies. Here we examine the extent to which some topics mentioned by Pomeroy [2] as largely unknown have remained so and, in contrast, we note some that are better understood 20 years later. The overwhelming contribution by picophytoplankton to the photosynthetic activities and biomass in oligotrophic waters is now recognized, and picocyanobacteria, prochlorophytes, and small eucaryotes have been observed in most aquatic ecosystems. However, although these organisms are the dominant phytoplankton in oligotrophic systems, as yet there has been no clear explanation of their role in mesotrophic and eutrophic water bodies where they may also be found in high numbers. Possibly these photosynthetic organisms may be an important food source for protist grazers, such as ciliates, tintinids, and heterotrophic dinoflagellates. Clarification of the links between the protista and picophytoplankton should have high priority in microbial food web research.
Correspondence to: T. Berman.
252
T. Berman, L. Stone
In 1974 Pomeroy wrote "We know much less about respiration in the ocean than about photosynthesis." Surprisingly, this statement still holds despite the fact that respiratory losses represent a major flux of carbon in lakes and oceans. There are few data on the magnitude of plankton respiration in the oceans or in lakes, although there seems to be little doubt that algal and bacterial respiration are by far the major contributors to the total. Better and more detailed measurement of planktonic respiration would seem an important research objective given the international concern with global carbon cycles. In his outline of microbial food webs, Pomeroy [2] indicated a presumptive link between protista and mesozoan zooplankton. The potential of protozoans to serve as food sources for zooplankton has been verified but is still not well quantified. Generally, the fate of protozoans within aquatic systems is largely undocumented. Recent studies have shown that larger phytoplankton are also to some extent liable to be fed upon by smaller protists, thus confusing any simple size-based trophic relationship. A further complication to the "simple" microbial food web outlined by Pomeroy [2] was the discovery that mixotrophic organisms are common and may be numerous in some aquatic ecosystems. Microorganisms in oceans and lakes are almost certainly not homogeneously dispersed in the water but rather may exist in microniches centered around phytoplankton, or be associated with inorganic and organic detrital aggregates such as marine and freshwater snow. Bacterial and protozoan involvement in particle formation and subsequent breakdown is increasingly studied, but understanding of these processes is still limited. Two further "twists" in microbial food webs include (1) the possible involvement of bacteriophage in promoting a mini-loop ("bacteria-phage-dissolved organic matter-bacteria"), the importance of which in oceans and lakes is, as yet, unclear; and (2) the capability of heterotrophic flagellates to grow on high molecular weight polysaccharides and thus to exploit some fraction of the large pool of dissolved organic compounds present in most natural water bodies. Over the past 20 years much detail of microbial food web function and structure has been revealed but there remains the question of how these microbial loops fit into the overall ecology of the aquatic environment. Theoretical ecologists have hardly begun to explore the implications of Pomeroy's "new paradigm" of aquatic food webs. An explanation for this lies in the difficulties of modeling systems that are of a truly complex nature. Nevertheless, initial progress has been made. For example, the unusual dynamics that might arise as a result of a rapidly cycling microbial loop have been examined recently. Since rapid recycling might be considered as a strong positive feedback loop, conventional ecological thinking would deem this to lead to system instability. However, for non-steady state systems (as frequently found in nature) such positive feedback loops may not necessarily be unstable and can lead to an efficient utilization of transient nutrient inputs. In the Bioscience paper [2], Pomeroy stressed that the new paradigm could eventually lead to applied benefits. In 1974, the emphasis was on fisheries management, but today understanding microbial food webs is also proving to be important for interpreting processes such as those controlling global warming, coastal pollution, or water quality in lakes and reservoirs. Future research in this field will benefit to the extent that we will be able to show the relevance of our results to questions of public concern.
The Microbial Loop after Twenty Years
253
References 1. Azam F, Fenchel T, Field JG, Gray JS, Meyer-Reil IA, Thingstad F (1983) The ecological role of water-column microbes in the sea. Mar Ecol Prog Ser 10:257-363 2, Porneroy LR (1974) The ocean's food web, a changing paradigm. Bioscience 24:499-504 3. Williams PJLeB (1981) Incorporation of microheterotrophic processes into the classical paradigm of the planktonic food web. Kieler Meerresforsch Sonderh 5:1-28 Note: Because of space limitations, we have given no detailed references. Most of the work mentioned is cited in the papers of this issue; an exact list is available from the authors.
Controls of the Microbial Loop: Biotic Factors
MICROBIAL ECOLOGY © 1994Springer-VerlagNew York Inc.
Musings on the Microbial Loop: Twenty Years After T. Berman,1 L. Stone 2 1Israel Oceanographic & Linmological Research, Yigal Allon Kinneret Limnological Laboratory, P.O. Box 345, Tiberias, Israel 14102 2Department of Zoology, Tel Aviv University, Ramat Aviv, Israel 69978
Pomeroy's seminal paper [2] synthesized information then available on oceanic food webs and presented a more complete picture of pelagic ecosystems than that previously perceived. This paper laid the "ideological" foundation for the wealth of new information on the structure and function of microbial food webs that would be amassed in the subsequent 20 years. It took some years before others [1, 3], on the basis of new results and observations, examined in some detail Pomeroy's paradigm of oceanic food webs focusing on the "microbial loop." The new perception of bacterial and protist involvement both in terms of biomass and metabolic activity in pelagic ecosystems was made possible only by the development of new methodologies: epifluorescent microscopy and nucleic acid staining for direct counting of microbial cells, [3H]thymidine and [3H]leucine determinations of bacterial production, and radioactive and fluorescent tagging of bacteria and algal cells to follow grazing rates on these organisms. The implications of the new oceanic paradigm became, after a characteristic time delay, evident also to limnologists so that the emphasis towards understanding microbial food webs has also been felt in freshwater studies. Here we examine the extent to which some topics mentioned by Pomeroy [2] as largely unknown have remained so and, in contrast, we note some that are better understood 20 years later. The overwhelming contribution by picophytoplankton to the photosynthetic activities and biomass in oligotrophic waters is now recognized, and picocyanobacteria, prochlorophytes, and small eucaryotes have been observed in most aquatic ecosystems. However, although these organisms are the dominant phytoplankton in oligotrophic systems, as yet there has been no clear explanation of their role in mesotrophic and eutrophic water bodies where they may also be found in high numbers. Possibly these photosynthetic organisms may be an important food source for protist grazers, such as ciliates, tintinids, and heterotrophic dinoflagellates. Clarification of the links between the protista and picophytoplankton should have high priority in microbial food web research.
Correspondence to: T. Berman.
252
T. Berman, L. Stone
In 1974 Pomeroy wrote "We know much less about respiration in the ocean than about photosynthesis." Surprisingly, this statement still holds despite the fact that respiratory losses represent a major flux of carbon in lakes and oceans. There are few data on the magnitude of plankton respiration in the oceans or in lakes, although there seems to be little doubt that algal and bacterial respiration are by far the major contributors to the total. Better and more detailed measurement of planktonic respiration would seem an important research objective given the international concern with global carbon cycles. In his outline of microbial food webs, Pomeroy [2] indicated a presumptive link between protista and mesozoan zooplankton. The potential of protozoans to serve as food sources for zooplankton has been verified but is still not well quantified. Generally, the fate of protozoans within aquatic systems is largely undocumented. Recent studies have shown that larger phytoplankton are also to some extent liable to be fed upon by smaller protists, thus confusing any simple size-based trophic relationship. A further complication to the "simple" microbial food web outlined by Pomeroy [2] was the discovery that mixotrophic organisms are common and may be numerous in some aquatic ecosystems. Microorganisms in oceans and lakes are almost certainly not homogeneously dispersed in the water but rather may exist in microniches centered around phytoplankton, or be associated with inorganic and organic detrital aggregates such as marine and freshwater snow. Bacterial and protozoan involvement in particle formation and subsequent breakdown is increasingly studied, but understanding of these processes is still limited. Two further "twists" in microbial food webs include (1) the possible involvement of bacteriophage in promoting a mini-loop ("bacteria-phage-dissolved organic matter-bacteria"), the importance of which in oceans and lakes is, as yet, unclear; and (2) the capability of heterotrophic flagellates to grow on high molecular weight polysaccharides and thus to exploit some fraction of the large pool of dissolved organic compounds present in most natural water bodies. Over the past 20 years much detail of microbial food web function and structure has been revealed but there remains the question of how these microbial loops fit into the overall ecology of the aquatic environment. Theoretical ecologists have hardly begun to explore the implications of Pomeroy's "new paradigm" of aquatic food webs. An explanation for this lies in the difficulties of modeling systems that are of a truly complex nature. Nevertheless, initial progress has been made. For example, the unusual dynamics that might arise as a result of a rapidly cycling microbial loop have been examined recently. Since rapid recycling might be considered as a strong positive feedback loop, conventional ecological thinking would deem this to lead to system instability. However, for non-steady state systems (as frequently found in nature) such positive feedback loops may not necessarily be unstable and can lead to an efficient utilization of transient nutrient inputs. In the Bioscience paper [2], Pomeroy stressed that the new paradigm could eventually lead to applied benefits. In 1974, the emphasis was on fisheries management, but today understanding microbial food webs is also proving to be important for interpreting processes such as those controlling global warming, coastal pollution, or water quality in lakes and reservoirs. Future research in this field will benefit to the extent that we will be able to show the relevance of our results to questions of public concern.
The Microbial Loop after Twenty Years
253
References 1. Azam F, Fenchel T, Field JG, Gray JS, Meyer-Reil IA, Thingstad F (1983) The ecological role of water-column microbes in the sea. Mar Ecol Prog Ser 10:257-363 2, Porneroy LR (1974) The ocean's food web, a changing paradigm. Bioscience 24:499-504 3. Williams PJLeB (1981) Incorporation of microheterotrophic processes into the classical paradigm of the planktonic food web. Kieler Meerresforsch Sonderh 5:1-28 Note: Because of space limitations, we have given no detailed references. Most of the work mentioned is cited in the papers of this issue; an exact list is available from the authors.
