Microb Ecol (1994) 28:303-319

Modeling the Microbial Loop

MICROBIAL ECOLOGYInc. © 1994Springer-Verlag New York

Modeling the Microbial Food Web H.W. Ducklow* Department of Chemistry, Woods Hole Oceanographic Institution, Woods Hole, Massachusetts 02543, USA

Abstract. Models of the microbial food web have their origin in the debate over the importance of bacteria as an energetic subsidy for higher trophic levels leading to harvestable fisheries. Conceptualization of the microbial food web preceded numerical models by 10-15 years. Pomeroy's work was central to both efforts. Elements necessary for informative and comprehensive models of microbial loops in plankton communities include coupled carbon and nitrogen flows utilizing a size-based approach to structuring and parameterizing the food web. Realistic formulation of nitrogen flows requires recognition that both nitrogenous and nonnitrogenous organic matter are important substrates for bacteria. Nitrogen regeneration driven by simple mass-specific excretion constants seems to overestimate the role of bacteria in the regeneration process. Quantitative assessment of the link-sink question, in which the original loop models are grounded, requires sophisticated analysis of size-based trophic structures. The effects of recycling complicate calculation of the link between bacteria or dissolved organic matter and mesozooplankton, and indirect effects show that the link might be much stronger than simple analyses have suggested. Examples drawn from a series of oceanic mixed layer plankton models are used to illustrate some of these points. Single-size class models related to traditional P-Z-N approaches are incapable of simulating bacterial biomass cycles in some locations (e.g., Bermuda) but appear to be adequate for more strongly seasonal regimes at higher latitudes.

Introduction For many of us, the modern era of microbial loop modeling began with "A simulation analysis of continental shelf food webs," by Pace, Glasser, and Pomeroy [39]. The history of attempts to model the microbial loop begins with the first quantitative models of plankton dynamics [49, 55]. These did not include microbial processes. But eventually they provided microbial ecologists with the conceptual apparatus with which to build models with microbial compartments, and just as importantly, with something to react against. In this paper I wish to address three objectives: I will (1) review some of the history leading up to the Pace et al., milestone; (2) discuss some of the essential components needed to model the microbial loop; and (3) present an overview of some of our recent work in the area. I use output from two versions of our model to illustrate the issues treated in part 2.

*New address: Virginia Institute of Marine Sciences, Box 1346, Gloucester Point, VA 23062. Intemet duck @ vims.edu.

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At the outset we should recognize the central role Larry Pomeroy has played in the development of the microbial loop paradigm. He was among the first to construct a plausible and convincing synthesis of supporting and conflicting observations, hypotheses, and speculations in a way that attracted the attention and curiosity of the community. The successful formulation of microbial processes in models, which signals acceptance of the paradigm, is partly the product of Larry's creative scientific imagination, and of the efforts of his colleagues and students at Georgia who helped to refine and support his ideas and carry the work forward to the wider community of marine scientists.

Establishing the Paradigm of the Microbial Loop Plankton modeling in the West derives essentially from the work of Gordon Riley at Woods Hole Oceanographic Institution, who was spurred by the need to understand quantitatively his observations on plankton cycles on Georges Bank, and by meeting Richard Fleming, of Scripps, in 1939 [35]. Fleming first wrote the differential equation describing the change of phytoplankton populations in time. By 1946, Riley had constructed a system of differential equations describing the dynamic behavior of phytoplankton, zooplankton, and nutrients, leading to the famous graphs depicting the production cycle at Georges Bank [49]. Riley realized that complete models would require bacteria [39, 50]. As pointed out by Pace et al. [39], future workers neglected Riley et al.'s recognition of the important phenomenon of phytoplankton not consumed by herbivores. Later, Pomeroy identified this resource as a key input to the microbial food web [45]. John Steele built the first modem compartmental model of plankton dynamics on the foundation laid by Riley [55]. Mills [35] identified Steele's major contribution as emphasizing the need to keep models simple, so the effects of single factors could be systematically explored. This necessitated consciously excluding many processes, including bacterial transformations in the water column. In constructing his later models, Steele was aware of the new results provided by Andrews and Williams [2] showing that bacterioplankton conversion of dissolved amino acids was a quantitatively significant process in coastal seas. He also discussed the possibility that protozoans could serve as a link between dissolved organic compounds and copepods--an early description of the microbial loop. However, Steele was concerned mainly with the problem of supporting observed fish yields from primary production, and based on the information available, he could not conclude for certain that the input of dissolved organic matter channeled into the copepods from microbes represented a previously unmeasured subsidy serving to increase the food available to fish. He included a bacterial compartment in the benthic food chain, but the pelagic chain proceeded from phytoplankton to herbivores (copepods) and on to fish and other carnivores. Steele's decisions about what compartments to include and which to neglect provided a clear statement about the marine ecosystem. Steele's model became identified as the "simple and neat," "classic" model of the aquatic food web [23]. It also became the paradigm view of the marine ecosystem to which microbial ecologists could react. At about the time Steele was finishing his book, Pomeroy was constructing a new synthesis of observations about the structure of marine ecosystems [44]. Pomeroy's

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concept seems to have been derived independently of similar work by Soviet microbiologists (e.g., [61]). If Steele's view represented the Classical (spare and elegant), then Pomeroy's was the Byzantine (filled with many complex and bizarre processes). This paper seems now to be remembered as the first to focus on the importance of small plankton--microbes in the production and respiration of the ocean. In a characteristic analogy, Pomeroy observed that "Far from being the grasses of the sea, net plankton appear to be the Sequoias... " ([44] p. 500). Just as important for future modelers, though, was his delineation of a multitude of food types including dissolved and particulate detrital forms, and the trophic pathways along which all these products of primary production could be consumed and transformed. The recognition of the magnitude of production and bacterial consumption of dissolved organic matter is of particular importance for our consideration of the microbial loop per se. Peter LeB. Williams also started from Steele's model in a later synthesis of the kinds of observations examined by Pomeroy [64]. He had the advantage of more data, including the first modem measurements of bacterial production [18, 24, 29]. Williams looked at the problem in a different way. Instead of presenting a new paradigm altogether, as Pomeroy did, he attempted to fit the new observations into the classical view. Williams showed how the new and high estimates of bacterial production could be explained by reasonable adjustments and additions to the classical model, while retaining the heavy grazing Steele postulated. In his budget, Williams routed 70% of the net primary production through the herbivores (i.e., 100% of the net particulate production), with 30% going into bacteria as primary dissolved photosynthate. Pomeroy suggested that around 25-50% of the particulate production remained unconsumed, adding more strands to the food web. Later, Fasham [15] identified the importance of recycling carbon through the microbial loop as a means of supporting reasonable fish yields and bacterial production. His model also introduced a simplified version of the expanded food web, amenable to the kinds of sensitivity analysis first explored by Steele. Besides providing the original synthesis and first comprehensive view of the microbial loop, Pomeroy was also comfortable with modeling approaches and understood their value and limitations early on. He noted the progress of ecosystem models in an early review of nutrient cycling [43], which first presented the elements of the new microbial loop paradigm. The next step to was to begin weaving in the complexity embodied in the loop paradigm to form a nonlinear compartmental simulation model. Depiction of the flows of energy and/or materials through plankton systems by means of aggregated compartmental flow diagrams was not new, even in the 1970s (e.g., [38, 61]). Pomeroy [45] began to formalize his earlier qualitative, descriptive models of plankton systems in a quantitative way. Starting again from Steele's simple model [55] of the North Sea plankton-benthos system, he added many of the compartments and processes identified earlier as elements of the new microbial loop paradigm. Pomeroy [45] presented steady-state carbon budget scenarios of continental shelf systems with a number of different assumptions. The emphasis is on the relative importance of the nanoplankton and detrital pathways. Pomeroy showed how the Steele model could be opened up to include high bacterial activity without violating Steele's assumptions, principally efficient ingestion of net plankton. But also, simply by rerouting most of the primary production through nano-

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Modeling the microbial food web.

Models of the microbial food web have their origin in the debate over the importance of bacteria as an energetic subsidy for higher trophic levels lea...
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