Self-regulation, bottom-up, and top-down control of phytoplankton communities: A reply to the comment by Kamenirl

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1 Comment 683 References AGUST~, S., C. M. DUARTE, AND D. E. CANFIELD, JR Phytoplankton abundance in Florida lakes: Evidence for the frequent lack of nutrient limitation. Limnol. Oceanogr. 35: AND J. KALFF Algal ccl1 size and the maximum density and biomass of phytoplankton. Limnol. Oceanogr. 32: BEGON, M., J. L. HARPER, ANDC. R. TOWNSEND Ecology. Individuals, populations and communities. V. 1. Mir. BIENFANG, P. K., AND M. TAKAHASHI Ultraplankton growth rates in a subtropical ecosystem. Mar. Biol. 76: HEMMINGSEN, A. M Energy metabolism as related to body size and respiratory surfaces, and its evolution. Rep. Steno. Mem. Hospital Nord. Insulinlab. 9: l JORGENSEN, B. B., N. B. REVSBECH, AND Y. COHEN Photosynthesis and structure of benthic microbial mats: Microelectrode and SEM studies of four cyanobacterial communities. Limnol. Oceanogr. 28: KAMENIR, Y. G Dimensional structure of cyclic systems: Interrelation of parameters [in Russian]. Ecol. Morya 24: Comparison of size spectra of living matter of three aquatic ecosystems. Syst. Anal. Model. Simul. 8: KHAILOV, K. M., AND Y. G. KAMENIR Photoassimilation surface of plants and its correlation with the respiratory surface of animals in size rows [in Russian]. J. Obshch. Biol. 49: KRUPATIUNA, D. K., A. S. LOPUKHIN, AND Y. G. KA- MENIR Size distribution of phytoplankton in the tropical Atlantic and its effect on the estimate of primary production and chlorophyll-a in waters at different trophic levels. Oceanology 27: MAY, R. M A cycling index for ecosystems. Nature 292: 105. ODUM, E. P Fundamentals of ecology. Saunders. PETERS, R. H The ecological implications of body size. Cambridge. SCHWINGHAMER, P Characteristic size distribution of integral benthic communities. Can. J. Fish. Aquat. Sci. 38: SHELDON, R. W., AND T. R. PARSONS A continuous size spectrum for particulate matter in the sea. J. Fish. Res. Bd. Can. 24: STOCKNER, J. G., AND N. J. ANTIA Algal picoplankton from marine and freshwater ecosystems: A multidisciplinary perspective. Can. J. Fish. Aquat. Sci. 43: WHITTAKER, R. H., AND P. L. MARKS Methods of assessing terrestrial productivity, p. 55-I 18. In R. H. Whittaker and G. E. Likens [eds.], Primary productivity of the biosphere. Ecol. Stud. 14. Limnol. Oceanogr., 37(3), 1992, , by the American Society of Limnology and Oceanography, Inc. Self-regulation, bottom-up, and top-down control of phytoplankton communities: A reply to the comment by Kamenirl In his comment Kamenir (1992) provides additional arguments supporting our demonstration (Agusti et al. 1990), based on the analysis of phytoplankton abundance and size in Florida lakes, of the importance of self-regulation and the frequent lack of nutrient limitation in limnetic phytoplankton communities. Kamenir regrets the scatter of the data we presented (Agusti et al. 1990) and suggests changes in data processing and variable selection that could improve the precision of our analysis. We welcome his constructive comment and support of our arguments, but find operational difficulties I Submitted: 23 October in implementing one of his main recommendations. Here we discuss these difficulties and the relevance of his suggestions and our own conclusions for the current debate on the importance of top-down vs. bottomup control of limnetic phytoplankton. We agree that both of Kamenir s main recommendations would increase the accuracy of our analysis. First, that inclusion of picoplankton, excluded from our analysis due to methodological limitations (Agusti et al. 1990), should bring the phytoplankton communities of oligotrophic lakes dominated by small algae, which were those showing the broadest differences between predicted maximal densities and realized densities (Agusti et al. 1990), closer to the

2 684 Comment predicted maximal density. Second, that the integral surface of organisms (i.e. the areal integral of phytoplankton surface area, m2 m-2) should be a more appropriate descriptor of phytoplankton abundance than the volumetric density or biomass (i.e. n mm3 or g m-3) when the irradiance reaching the lake s surface, which has units PEinst m-2, is believed to be the ultimate factor limiting the abundance of phytoplankton. The data used in our analysis (Agusti et al. 1990) were collected as part of a largescale project to characterize the regional limnology of Florida lakes (Canfield and Hoyer 1988). This project was completed a decade before our work in the laboratory produced models allowing estimates of the maximal algal density possible (Agusti et al. 1987; Agusti and KallI 1989). Thus, data collection and processing were not specifically designed to test the proximity of the algal communities in Florida lakes to the maximal achievable densities, which would be best achieved, as pointed out by Kamenir, if planktonic autotrophs across the full size spectrum were enumerated. The measurement of the integral surface of autotrophs, while relatively straightforward in macrophytes and terrestrial plants (i.e. the leaf area index), poses serious problems in aquatic ecosystems. Samples should integrate the fraction of the water column inhabited by active planktonic autotrophs, which is often represented by the water column within the euphotic layer, as suggested by Kamenir. This procedure would, however, underestimate the integral surface of autotrophs in systems where mixing extends below the euphotic zone, as occurs in many nonstratified Florida lakes. In addition to those methodological difficulties, there are, to our knowledge, no available estimates of the maximal integral phytoplankton surface area against which measured values can be compared. There are published estimates of the maximum areal chlorophyll concentration possible for phytoplankton that range from 0.4 to 0.8 g of Chl mm2 (Steemann Nielsen 1962), depending on whether diatoms or green algae dominate the plankton. These estimates assume a constant Chl a-specific absorption coefficient (Steemann Nielsen 1962), where- as the Chl-specific absorption coefficient of phytoplanktonic algae varies from to 0.05 m2 (mg Chl)-. Because the communities studied varied widely in species composition (Duarte et al. 1992) use of an average Chl-specific absorption coefficient would introduce substantial error to estimates of the maximal areal chlorophyll content of planktonic communities. In contrast, the model by Agusti et al. (1987) provides conservative estimates of the maximal volumetric densities achievable by phytoplankton against which volumetric data, such as those of Agusti et al. (1990) can be compared. Whether volumetric or areal estimates of phytoplankton abundance should be used depends on the goals of the study. Areal estimates, such as the integral areal phytoplankton surface should be preferred when the importance of light as the ultimate resource limiting phytoplankton abundance is being assessed (Steemann Nielsen 1962; Kamenir 1992) and when the total phytoplankton crop of a lake ecosystem is being characterized. Volumetric estimates of phytoplankton abundance should be favored, however, when the importance of phytoplankton control mechanisms that operate volumetrically (e.g. nutrient availability and grazing pressure) is being assessed. Volumetric estimates are also more relevant to those concerned with the noxious effects of phytoplankton accumulation, which depend on concentration rather than integrated abundance in the water column. At any rate, our conclusion that many (w 30 %) of the phytoplankton communities examined were at, or close to, the maximal achievable densities is conservative, because, as pointed out by Kamenir, implementation of his recommendations would raise the number of communities estimated to be near or at the maximal achievable density. His contention that the predicted maximum vol.umetric densities based on Agusti et al. (1987) should increasingly overestimate the maximal volumetric density as lakes become deeper follows the empirical and theoretical analysis of the influence of lake depth on phytoplankton yield by Sakamoto (1962). Sakamoto developed a model predicting the maximal phytoplankton yield of lakes with mean depth

3 Comment m to be only -0.5 mg Chl a rnd3, whereas communities growing in lakes with mean depth of - 5 m can achieve up to 300 mg Chl a mv3 (figure 11, Sakamoto 1962). These calculations, however, assume the water column to have remained completely mixed during development of the phytoplankton population, which is difficult to test. Kamenir also raises the important point that values of integral phytoplankton surface area show little variability in systems ranging from eutrophic reservoirs to the world ocean, despite orders of magnitude differences in nutrient loading. This observation supports our contention that there must be mechanisms of self-regulation by which phytoplankton compensate lack of nutrients, such as changes in their size spectrum, with the associated changes in nutrient use efficiency (Smith and Kalff 1982). Thus, changes in nutrient supply may alter the vertical distribution of phytoplankton, concentrating the cells within a shallow photic layer when nutrients are abundant or diluting them over a deep photic layer when nutrients are scarce, without substantially altering the areal abundance of the planktonic community. These changes in the vertical distribution of phytoplankton lead, in turn, to self-regulation of the light climate by phytoplankton (Talling 197 l), because changes in cell size distribution, growth form (i.e. colonial vs. single cells), and intracellular Chl a concentration yield changes in the absorption of light per unit Chl a and, therefore, on the extinction of light by phytoplankton (Agusti a, b; Agusti and Phlips 1992). There are, however, shallow, oligotrophic lakes in Florida (Canfield et al. 1983) and elsewhere (e.g. Carrillo et al. 1990) that support integral phytoplankton crops orders of magnitude below the average values. These lakes are shallower than the photic depth, where phytoplankton abundance must be regulated by mechanisms that operate volumetrically, such as nutrient supply or grazing pressure, and not light. There are, therefore, three main mechanisms regulating phytoplankton abundance and metabolism: bottom-up control, which involves regulation by physical-chemical factors and is the dominant regulatory agent in nutrient-limited populations; top-down control, which involves regulation by predators; and self-regulation, which involves changes at the community (e.g. shifts in size spectrum, species replacements, and biomass distribution across taxa) and cellular (e.g. changes from isolated to colonial growth form, changes in size and biochemical composition) level and becomes particularly important when algal crops have reached the ceiling imposed by physical-chemical constraints (notably light limitation). These three processes are linked through feedback mechanisms and operate in concert in all phytoplankton communities, although their relative contribution varies. Patterns derived from comparative analyses of changes in Florida phytoplankton communities help to clarify how their relative importance changes across a trophic gradient. These patterns include, first, patterns indicative of a reduction in the importance of phytoplankton regulation by grazing toward eu- trophic lakes. These are a tendency for algal size to increase from oligotrophic to eutrophic Florida lakes, both at the community (Agusti et al. 1990) and genera (Duarte et al. 1990, 1992) level, dense communities being dominated by colonial algae; a shift in phytoplankton community structure in Florida lakes from dominance of green algae in oligotrophic lakes and blue-greens in eutrophic lakes, diatoms having their greatest contribution at intermediate biomasses (Duarte et al. 1992); and a reduction in the rate of increase in zooplankton abundance with increasing phytoplankton biomass (i.e. slope of log zooplankton abundance vs. log phytoplankton biomass < 1, Canfield and Watkins 1984). Second, a change in the strength and the relative rate of increase in phytoplankton biomass with increasing nutrients from low in oligotrophic lakes to high in mesotrophic lakes and low in eutrophic lakes (Canfield 1983; Prairie et al. 1990), suggesting phytoplankton abundance to be most dependent on nutrients in mesotrophic lakes. Third, patterns indicative of an increased importance of self-regulation as populations become increasingly dense toward eutrophic lakes. These are a shift in the biomass partitioning in Florida phytoplankton com-

4 686 Comment munities from biomass being more equally distributed among many taxa in sparse communities to the accumulation of rnost of the biomass in one or a few taxa in dense communities (Agusti et al. 199 l), reflecting increased competition among phytoplankton taxa in dense communities; and an increased proportion of phytoplankton communities near or at the maximal achievable density toward eutrophic lakes (Agusti et al. 1990). The contention that nutrient limitation may not be the dominant regulatory agent in oligotrophic lakes appears paradoxical, but is consistent with existing evidence that phytoplankton in oligotrophic oceans is growing at, or close to, the maximal intrinsic rates (Goldman et al. 1979; Goldman 1980), grazing pressure being the volumetric mechanism maintaining the sparse populations and efficient recycling necessary to avoid nutrient limitation in these waters (Goldman 1984; Harris 1986). As nutrient supply increases toward mesotrophic lakes, gra:zing pressure should be less efficient in maintaining low volumetric phytoplankton biomass and, therefore, fails to provide efficient recycling, yielding increasingly nutrient-limited phytoplankton communities. In eutrophic lakes, zooplankton populations are unable to clear phytoplankton fast enough to prevent the high phytoplankton biomass characteristic of these systems. Accumulation of phytoplankton biomass in these lakes results in strongly self-shaded populations near or at the maximum achievable density (Agusti et al. 1990) and triggers self-regulatory processes (Tailing 1971). The interplay of regulatory mechanisms described above involves feedback effects that render arguments to identify cause and effect circular, requiring redefinition of what the dependent and independent factors in models of phytoplankton regulation are. The lack of such models is probably explained by the fact that research interest has shifted with time from a dominance of the consideration of physical-chemical mechanisms of phytoplankton regulation to an expanding interest on the importance of grazing and food-web structure (Carpenter et al ). Consideration of both sets of factors in concert has proven to substantially ameliorate our ability to predict phytoplankton abundance (Carpenter et al ). Similarly, we hope that Kamenir s and our own advocacy of the importance of self-regulation in phytoplankton ecology may encourage consideration of self-regulatory processes, and thereby lead to a more balanced interplay of the consideration of bottom-up, top-down, and self-regulatory mechanisms in phytoplankton ecology.. Susana Ag-usti Carlos M. Duarte Centro de Estudios Avanzados Camino de Santa Barbara Blanes, Gerona Spain de Blanes Daniel E. Canfield, Jr. Department of Fisheries and Aquaculture University of Florida 7922 NW 7 1st St. Gainesville References AGWST~, S. 199 la. Allometric scaling of light absorption and scattering by phytoplankton cells. Can. J. Fish. Aquat. Sci. 48: p b. Light environment within dense algal populations: Cells size influences on self-shading. J. Plankton Res. 13: ,C. M. DUAWE,AND D.E. CANFIELD, JR Phytoplankton abundance in Florida lakes: Evidence for the frequent lack of nutrient limitation. Limnol. Oceanogr. 35: 18 l-l ,AND-. I99 1. Biomass parti- tioning within Florida phytoplankton communities. J. Plankton Res. 13: AND J. KALFF Algal cell size and the maximum density and biomass of phytoplankton. Limnol. Oceanogr. 32: , AND J. KAIIF The influence of growth conditions on the size dependence of maximal algal density and biomass. Limnol. Oceanogr. 34: 1104-l , AND E. J. PHLIPS Light absorption by cyanobacteria: [mplications of the colonial growth form. Limnol. Oceanogr. 37: CANFIELD, D. E., JR Prediction of chlorophyll a concentration in Florida lakes: The importance of phosphorus and nitrogen. Water Resour. Bull. 19: , AND M. V. HOYER Regional geology and the chemical and trophic state characteristics of Florida lakes. Lake Reservoir Manage. 4: , M. J. MAC:EINA, L. M. HODGSON, AND K. A.

5 Comment 687 LANGELAND Limnological features of some In Flows of energy and materials in marine eco- Northwestern Florida lakes. J. Freshwater Ecol. 2: systems. NATO Conf Ser. 4, Mar. Sci. V Plenum. AND C. E. WATKINS II Relationships -, J.J. MCCARTHY, AND D. G. PEAVEY beiween zooplankton abundance and chlorophyll Growth rate influence on the chemical composia concentration in Florida lakes. J. Freshwater Ecol. tion of phytoplankton in oceanic waters. Nature 2: : CARPENTER, S. R., AND OTHERS Patterns of primary production and herbivory in 25 North American lake ecosystems, p In J. J. Cole, et al. [eds.], Comparative ecology of ecosystems: Patterns, mechanisms, and theories. Springer. CARRILLO, P., L. CRUZ-PIZARRO, AND P. SANCHEZ- CASTILLO Analysis of phytoplankton- HARRIS, G. P Phytoplankton ecology. Structure, function and fluctuation. Chapman and Hall. KAMENIR, Y Further evidence of nonnutrient constraints on phytoplankton abundance. Limnol. Oceanogr. 37: PRAIRIE,~. T., C. M. DUARTE, AND J. KALFF Unifying nutrient-chlorophyll relationships in zooplankton relationships in an oligotrophic lake under natural and manipulated conditions. Hydrobiologia 200/201: DUARTE, C. M., S. AGUST~, AND D. E. CANFIELD,JR Size plasticity of Florida phytoplankton: Implications for phytoplankton community structure. Limnol. Oceanogr. 35: 1846-l ,AND Patterns in phytoplankton community structure in Florida lakes. Limnol. Oceanogr. 37: 155-l 61. GOLDMAN, J. C Physiological processes, nu- trient availability, and the concept of relative growth rate in marine phytoplankton ecology, p In Primary productivity in the sea. Brookhaven Symp. Biol. 31. Plenum Oceanic nutrient cycles, p lakes. Can. J. Fish. Aquat. Sci. 46: 1176-l 182. SAKAMOTO, M Primary production by the phytoplankton community in some Japanese lakes and its dependence on lake depth. Arch. Hydrobiol. 62: l-28. SMITH, R. E. H., AND J. KALFF Size-dependent phosphorus uptake kinetics and cell quota in phytoplankton. J. Phycol. 18: STEEMANN NIELSEN, E On the maximum quantity of plankton chlorophyll per surface unit ofa lake or the sea. Int. Rev. Gesamten Hydrobiol. 47: TALLING, J. F. 197 I. The underwater light climate as a controlling factor in the production ecology of freshwater phytoplankton. Mitt. Int. Ver. Theor. Angew. Limnol. 19, p