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Novel Interactions Between Phytoplankton and Microzooplankton: Their Influence on the Coupling Between Growth and Grazing Rates in the Sea

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Novel Interactions Between Phytoplankton and Microzooplankton: Their Influence on the Coupling Between Growth and Grazing Rates in the Sea Hydrobiologia 480: 41–54, 2002. 41 C.E. Lee, S. Strom & J. Yen (eds), Progress in Zooplankton Biology: Ecology, Systematics, and Behavior. © 2002 Kluwer Academic Publishers. Printed in the Netherlands. Novel interactions between phytoplankton and microzooplankton: their influence on the coupling between growth and grazing rates in the sea Suzanne Strom Shannon Point Marine Center, Western Washington University, 1900 Shannon Point Rd., Anacortes, WA 98221, U.S.A. Tel: 360-293-2188. E-mail: [email protected] Key words: phytoplankton, microzooplankton, grazing, stability, behavior, evolution Abstract Understanding the processes that regulate phytoplankton biomass and growth rate remains one of the central issues for biological oceanography. While the role of resources in phytoplankton regulation (‘bottom up’ control) has been explored extensively, the role of grazing (‘top down’ control) is less well understood. This paper seeks to apply the approach pioneered by Frost and others, i.e. exploring consequences of individual grazer behavior for whole ecosystems, to questions about microzooplankton–phytoplankton interactions. Given the diversity and paucity of phytoplankton prey in much of the sea, there should be strong pressure for microzooplankton, the primary grazers of most phytoplankton, to evolve strategies that maximize prey encounter and utilization while allowing for survival in times of scarcity. These strategies include higher grazing rates on faster-growing phytoplankton cells, the direct use of light for enhancement of protist digestion rates, nutritional plasticity, rapid population growth combined with formation of resting stages, and defenses against predatory zooplankton. Most of these phenomena should increase community-level coupling (i.e. the degree of instantaneous and time-dependent similarity) between rates of phytoplankton growth and microzooplankton grazing, tending to stabilize planktonic ecosystems. Conversely, phytoplankton, whose mortality in the sea is overwhelmingly due to microzooplankton grazing, should experience strong pressure to evolve grazing resistence. Strategies may include chemical, morphological, and ‘nutrient deficit’ defenses. Successful deployment of these defenses should lead to uncoupling between rates of phytoplankton growth and microzooplankton grazing, promoting instability in ecosystem structure. Understanding the comparat- ive ecosystem dynamics of various ocean regions will require an appreciation of how protist grazer behavior and physiology influence the coupling between rates of phytoplankton growth and microzooplankton grazing. Overview slowly emerged, and the consequences of this inter- play between bottom-up and top-down regulation are The evolution of thought on the regulation of phyto- still not always readily appreciated. plankton communities forms an important part of Bruce Frost’s research has contributed much to biological oceanographic history. While a few pres- the recognition of grazing as a process structuring cient thinkers have always espoused a holistic view phytoplankton communities. His work with copepods of phytoplankton regulation (Riley, 1946; Harvey et elucidated the predictable nature of these animals’ al., 1935; Johannes, 1964; Pomeroy, 1974), much feeding response to changing phytoplankton cell size early work framed problems of phytoplankton spe- and concentration (Frost, 1972, 1975). Such feed- cies succession and biomass change solely in terms of ing responses were quickly explored from a theor- resource availability and competitive interaction (i.e. etical viewpoint with colleagues including Lam and ‘bottom up’ factors). The view that grazing (a ‘top Steele (Lam & Frost, 1976; Steele & Frost, 1977). down’ factor) contributes equally to observed phyto- These papers and others from the same time period plankton community composition and size has only (Frost, 1980) clearly demonstrated the potential for 42 suspension-feeding copepods to regulate important as- corresponding elements of phytoplankton morphology pects of phytoplankton communities, including size and physiology that influence the same? Because the structure, overall biomass, and cell division rate study of planktonic protist grazers is in its infancy, (through grazer nutrient excretion). The relationship there are a number of exciting and largely unexplored between phytoplankton and grazer capabilities, and research areas germane to these questions. A central the consequent impact on phytoplankton community goal of this paper is to illustrate the potential import- dynamics, have since been used by Frost to illumin- ance of this research area, and by doing so to stimulate ate some of the major present-day problems in ocean inquiry into this little-known yet fascinating sector of plankton ecology. A particular focus has been the role plankton ecology. of grazing and its interaction with resource availab- ility in structuring the food webs of high nitrate–low Coupling between phytoplankton growth and chlorophyll (HNLC) regions (Frost, 1987, 1991, 1993; microzooplankton grazing Frost & Franzen, 1992; Loukos et al., 1997; Strom et al., 2000). Rates of phytoplankton growth (as intrinsic growth, In the spirit of the March 2001 symposium hon- or cell division rates) and microzooplankton grazing oring Frost’s contributions to plankton ecology, my may be coupled in both an instantaneous and a time- intent in this paper is to explore the influence of mi- varying sense. In the instantaneous sense, a coupled crozooplankton (phagotrophs <200 µm in size) on system is one in which cell- or biomass-specific rates phytoplankton communities. While Frost’s early ex- of growth and grazing are similar in magnitude; in perimental and theoretical work focused on copepods, highly coupled systems, rates might be equal. If the ‘microbial revolution’ that has swept biological equality persists over time and other accumulation oceanography since the early 1980s has indicated that or loss processes are inconsequential, phytoplankton microzooplankton, primarily protists, are the major biomass will remain constant, although phytoplank- grazers of phytoplankton at most times throughout ton production might be quite high. This situation is much of the world’s oceans (e.g. Burkill et al., 1993; thought to characterize the open subarctic Pacific, and Verity et al., 1993; Landry et al., 1997; Neuer & perhaps other HNLC regions (Miller, 1993; Landry Cowles, 1994; Sherr & Sherr, submitted). Further- et al., 1997). Conversely, in an uncoupled system, more, it is now widely recognized that the fate of most growth and grazing rates differ substantially, and large phytoplankton cells produced in the sea is to be eaten changes in phytoplankton standing stocks (e.g. blooms (Banse, 1992). This makes microzooplankton graz- or precipitous declines) are likely to ensue. Temper- ing a key process for the structuring of phytoplankton ate coastal waters represent this contrasting scenario, community composition, biomass, and activity, in pre- at least seasonally. The extent to which growth and cisely the conceptual sense envisioned by Frost and grazing are coupled in time affects the net response of others. the phytoplankton community to perturbations, such Phytoplankton cell division rates (i.e. the poten- as events that change light or nutrient availability, tial for phytoplankton cells to accumulate) and rates which in turn alter the phytoplankton growth rate. In of protist grazing can be either coupled or uncoupled a stable ecosystem, perturbations either initiate little in time. The nature and extent of this coupling, in change (high system resistance) and/or the changes concert with other loss processes such as cell sinking, that arise are short-lived (high system resilience sensu viral lysis, or advection, dictate the temporal evolution Pimm, 1984 and May, 2001). Phenomena that couple of the phytoplankton community. This view relates growth and grazing rates promote planktonic ecosys- directly to the widely employed ‘Frost equations’ for tem stability because event-driven changes in growth estimating grazing rates (specifically the coefficients rate, which might otherwise lead to changes in phyto- of phytoplankton growth (k) and zooplankton grazing plankton biomass and composition, are buffered by (g) therein) as well as to their first cousin, the dilu- corresponding changes in grazing. It is important to tion method of Landry and Hassett, which estimates note that phytoplankton biomass-specific grazing rates analogous coefficients of growth and microzooplank- are dependent on both the feeding rates of individual ton grazing for natural communities (Frost, 1972; grazers, and on grazer community biomass. Landry & Hassett, 1982). What are the attributes of In the remainder of the paper, I first explore fea- protists, as grazers, that influence coupling between tures of protist grazer behavior and physiology that phytoplankton growth rates and grazing? What are have the potential to couple phytoplankton growth and 43 protist grazing. These features involve both individual (per capita) grazing rate regulation, and regulation of grazer population size. Second I describe a related set of phytoplankton features that, in concert with prot- ist responses, could uncouple rates of phytoplankton growth and protist grazing. Throughout, the reader’s attention is directed to unanswered questions and out- standing research directions related to protist grazers and their interaction with phytoplankton. Figure 1. Comparative rates of phytoplankton growth
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