We present an analysis of the global impact of microplanktonic grazers on marine phytoplankton and its implications for remineralization processes in the microbial community. The data were obtained by an extensive literature search that yielded 788 paired rate estimates of autotrophic growth (µ) and microzooplankton grazing (m) from dilution experiments. From studies in which phytoplankton standing stock was measured in terms of carbon equivalents, we show that the production estimate from dilution experiments is a reasonable proxy (r = 0.89) for production determined by the standard ¹⁴C method. The ratio m: µ, the proportion of primary production (PP) consumed by micrograzers, shows that microzooplankton consumption is the main source of phytoplankton mortality in the oceans, accounting for 67% of phytoplankton daily growth for the full data set. This ratio varies modestly among various marine habitats and regions, with data averages ranging from 60% for coastal and estuarine environments to 70% for the open oceans, and from ~59% for temperateߚsubpolar and polar systems to 75% for tropicalߚsubtropical regions. Given estimates for the metabolic requirements of micrograzers and assuming they consume most bacterial production, regionally averaged estimates of the protistan respiration are 35ߚ43% of daily PP for the first level of consumer or 49ߚ59% of PP for three trophic transfers. The estimated contributions of microbial grazers to total community respiration are of the same magnitude as bacterial respiration. Consequently, potential ecosystem differences in micrograzer activity or trophic structure are a large uncertainty for biogeochemical models that seek to predict the microbial community role in carbon cycling from bacterial parameters alone.

11 pages, 3 figures, 3 tablesWe show the results of a comparative, cross-ecosystem, analysis of the relative importance of ciliates as carbon sources for copepod, and, specifically, evaluated the strength of the ciliate-copepod trophic link. Although phytoplankton represent, globally, a far higher biomass than ciliates (>1 order of magnitude), the consumption of the latter nevertheless comprises, on average, 30 % of copepod daily carbon rations (ciliates + phytoplankton). The relative importance of ciliate consumption by copepods clearly depends on the trophic state of the system. In regions where phytoplankton concentrations are low (< 50 μgC l-1), ciliate and phytoplankton contribution to the diet are equivalent. In richer environments this value declines, with ciliates accounting for only 25 and 22 % of diet in environments characterized by phytoplankton concentrations of 50-500 and > 500 μgC l-1, respectively. From a biogeochemical point of view, our carbon budget estimates indicate that copepods process, on a global scale, 5.5 to 8.1 gigaton (Gt) phytoplankton-derived C yr-1; from the heterotrophic side, this flux would represent 2.0 to 2.4 Gt ciliate-derived C yr-1 and, probably, a higher value would be obtained if other microheterotrophs, like heterotrophic dinoflagellates, were included. Hence, the flux of carbon from ciliates, and other microzooplankton, towards upper trophic levels should definitely be considered in oceanic biogeochemical cycles and pelagic food web models. © Inter-Research 2005This work was supported by projects ZOOTRANSFER (REN2001–1693) and PETROZOO (VEM2003-20037), and by program Ramón y Cajal from the Ministry of Science and Technology of Spain. We also acknowledge the OMEX grant (MAS3-CT97-0076) to S. BattenPeer Reviewe

The traditional view of the planktonic food web describes consumption of inorganic nutrients by photoautotrophic phytoplankton, which in turn supports zooplankton and ultimately higher trophic levels. Pathways centred on bacteria provide mechanisms for nutrient recycling. This structure lies at the foundation of most models used to explore biogeochemical cycling, functioning of the biological pump, and the impact of climate change on these processes. We suggest an alternative new paradigm, which sees the bulk of the base of this food web supported by protist plankton communities that are mixotrophic – combining phototrophy and phagotrophy within a single cell. The photoautotrophic eukaryotic plankton and their heterotrophic microzooplankton grazers dominate only during the developmental phases of ecosystems (e.g. spring bloom in temperate systems). With their flexible nutrition, mixotrophic protists dominate in more-mature systems (e.g. temperate summer, established eutrophic systems and oligotrophic systems); the more-stable water columns suggested under climate change may also be expected to favour these mixotrophs. We explore how such a predominantly mixotrophic structure affects microbial trophic dynamics and the biological pump. The mixotroph-dominated structure differs fundamentally in its flow of energy and nutrients, with a shortened and potentially more efficient chain from nutrient regeneration to primary production. Furthermore, mixotrophy enables a direct conduit for the support of primary production from bacterial production. We show how the exclusion of an explicit mixotrophic component in studies of the pelagic microbial communities leads to a failure to capture the true dynamics of the carbon flow. In order to prevent a misinterpretation of the full implications of climate change upon biogeochemical cycling and the functioning of the biological pump, we recommend inclusion of multi-nutrient mixotroph models within ecosystem studies.

Arranging organisms into functional groups aids ecological research by grouping organisms (irrespective of phylogenetic origin) that interact with environmental factors in similar ways. Planktonic protists traditionally have been split between photoautotrophic "phytoplankton" and phagotrophic "microzooplankton". However, there is a growing recognition of the importance of mixotrophy in euphotic aquatic systems, where many protists often combine photoautotrophic and phagotrophic modes of nutrition. Such organisms do not align with the traditional dichotomy of phytoplankton and microzooplankton. To reflect this understanding, we propose a new functional grouping of planktonic protists in an eco-physiological context: (i) phagoheterotrophs lacking phototrophic capacity, (ii) photoautotrophs lacking phagotrophic capacity, (iii) constitutive mixotrophs (CMs) as phagotrophs with an inherent capacity for phototrophy, and (iv) non-constitutive mixotrophs (NCMs) that acquire their phototrophic capacity by ingesting specific (SNCM) or general non-specific (GNCM) prey. For the first time, we incorporate these functional groups within a foodweb structure and show, using model outputs, that there is scope for significant changes in trophic dynamics depending on the protist functional type description. Accordingly, to better reflect the role of mixotrophy, we recommend that as important tools for explanatory and predictive research, aquatic food-web and biogeochemical models need to redefine the protist groups within their frameworks.

Calbet, A. 2008. The trophic roles of microzooplankton in marine systems. – ICES Journal of Marine Science, 65: 325–331. Microzooplankton (here defined as <200 µm grazers) are key components of marine foodwebs. Their grazing significantly affects primary producers and usually exceeds that of mesozooplankton. However, our knowledge of the detailed roles that microzooplankton taxa play in marine ecosystems is surprisingly limited. Here, I identify the main protists responsible for most of the grazing impact on phytoplankton in two contrasting marine ecosystems: oligotrophic waters and productive waters, such as upwelling systems, spring blooms, and other blooms in nearshore and estuarine systems. Evidence indicates that pico- and nano-sized flagellates, which are routinely included with the microzooplankton size class of protists, appear to be the main grazers of phytoplankton in oligotrophic habitats, whereas heterotrophic and mixotrophic dinoflagellates are candidates for the dominant grazing impact in upwelling and other productive ecosystems. Microzooplankton are also important contributors to mesozooplankton diet, especially in oligotrophic areas, although the strength of the mesozooplankton–microzooplankton link is traditionally overlooked in plankton studies. As a final remark, this review emphasizes the need to develop suitable methods for studying the role of microbial grazers in the dynamics of marine ecosystems.

A comparative analysis of the importance of mesozooplankton (200–20,000 µm) as grazers of the phytoplanktonic primary production (PP) across a wide spectrum of marine ecosystems revealed mesozooplankton ingestion rates to increase nonlinearly with increasing PP. The slope of the log‐log relationship between ingestion rates and PP was significantly ,1, indicating a decline of relative importance of mesozooplankton grazing with increasing PP. The effect of mesozooplankton on PP (as the percent PP consumed per day) is moderate in most of the studies (mode 6%, mean 22.6%) and decreases exponentially with increasing productivity. Contrary to the common assumption, the size barrier imposed by dominant picoautotrophs does not always result in a lower grazing pressure in unproductive communities (we consider here those with PP < 250 mg C m⁻² d⁻¹). Yet, the amount of phytoplanktonic carbon ingested per unit of mesozooplankton biomass is lower in unproductive than in moderate (250 to 1,000 mg C m⁻² d⁻¹) and highly productive communities (>1,000 mg C m⁻² d⁻¹). This observation, together with the generally low values of daily biomass‐specific ingestions, suggests that alternative food sources (e.g., protozoans) must represent an important component of mesozooplankton diet in unproductive ecosystems. The relationships obtained in the study yield an estimate of 5.5 Gt phytoplanktonic C consumed per year in the global ocean, which represents ~12% of the oceanic PP.