AQUATIC MICROBIAL ECOLOGY Vol. 9: 33-39,1995 Published April 28 Aquat microb Ecol

Some comments on and its importance in the pelagic ecosystem

G. E. Fogg

School of Ocean Sciences (University of Wales, Bangor), Marine Science Laboratories, Menai Bridge. Anglesey, Gwynedd LL59 5EY. United Kingdom

ABSTRACT. Picoplankton is an integral component of a microbial community, termed the ultraplank- ton, which seems to be ubiquitous in all seas and lakes. The picophytoplankton and heterotrophic bac- terioplankton produce the bulk of the in the community and their consumption by predators with matching growth rates results in a highly dynamic and self-contained system with efficient recy- cling of mineral nutrients and dissolved organic matter. Given adequate radiant energy the population levels of the component organisms are largely determned by the internal dynamics of the community rather than by external factors. Only when concentrations of mineral nutrients rise above those set by dynamics of the ultraplankton can larger compete effectively and multiply. There is a sharp distinction in form and dynamics between ultra- and microplankton. The metabolism of the ultra- commonly dominates in pelagic ecosystems, although it seems to contribute little organic matter to higher trophic levels, and must be taken into account in the determination of primary pro- ductivity.

KEYWORDS: Picoplankton . Ultraplankton . Microplankton . . Recycling .

INTRODUCTION COSMOPOLITAN NATURE AND STABILITY IN COMPOSITION OF PICOPLANKTON Picoplankton includes all those organisms, both phototrophic and heterotrophic, which fall into the size Numerous studies suggest that picoplankton is cos- class 0.2 to 2.0 pm. In this paper I propose to comment mopolitan in distribution in the surface waters of both on some aspects of the ecology of these micro-organ- freshwater lakes and the sea, with numbers of organ- isms, elaborating a point of view already advanced by isms commonly around 106 ml-' for heterotrophic bac- Sieburth (1984). My object will be to emphasize the teria, 104 ml-' for (Fogg 1986a, 1987, remarkable characteristics of the marine microbial Nagata 1988, Stockner 1988, Kudoh et al. 1990, Caron community of which the picoplankton forms an inte- et al. 1991), 103 ml-' for eukaryotes and up to 105 rnl-' gral part. This community has been called the 'micro- for prochlorophytes (Campbell & Vaulot 1993). This is litersphere' by Sieburth & Davis (1982) but I prefer to so for Mediterranean waters as for other seas (Maugeri use the older term 'ultraplankton'. The upper size level et al. 1992, Wood et al. in press). Population densities of this, put between 10 and 20 pm so as to include do not usually vary very much but fluctuations of sev- nanoplankton (but see Shapiro & Guillard 1986), eral orders of magnitude have been reported, e.g. for a seems, as I hope to show, to mark a natural discontinu- Welsh lake (Happey Wood 1991) and for Lakes Faro ity between it and the microplanktonic community and Ganzirri near Messina (Acosta Pomar et al. 1988, familiar from the textbooks. A community related to Bruni et al. 1990), but these are relatively small water the ultraplankton is to be found in (Silver bodies subject to abrupt changes in water quality and et al. 1986) but, although it undoubtedly has important may be regarded as special cases. Another component interactions with both the free-living ultraplankton of the ultraplankton, the nanoplanktonic phagotrophic and the microplankton, this will not be dealt with here. , also shows a relative stability of population

Q Inter-Research 1995 Resale of full artjcle not permitted 34 Aquat microb Ecol9: 33-39, 1995

density at around 103 ml-' (Sherr & Sherr 1984), as per- occur at progressively greater depths, a separation haps virus particles at up to 108 ml-' do as well (Bergh which seems to be explained by the respective effi- et al. 1989, Proctor & Fuhrman 1990). ciencies of their photosynthetic pigments in utilizing Types, if not species, of picoplankton seem to be the wavelengths which penetrate to these depths (Li cosmopolitan. spp. seem ubiquitous in & Wood 1988, Lande et al. 1989, Wood 1990, Campbell open waters, whether fresh or salt. Kennaway (1989) & Vaulot 1993).Orientated motility may contribute isolated from a Welsh lake a Synechococcus which was to the positioning in the water column of the small morphologically similar to the Type 1 described by eukaryotes (Lande et al. 1989). Johnson & Sieburth (1979) from . On the other Population densities of both phototrophic and het- hand, considerable genetic and biochemical differ- erotrophic picoplankton have been found to increase ences have been found between morphologically iden- by perhaps an order of magnitude between oligo- tical strains of marine Synechococcus (Glibert et al. trophic and moderately eutrophic waters (see e.g. El 1986, Glibert & Ray 1990, Wood & Townsend 1990). Hag & Fogg 1986 for the marine situation and Bern- Picoplanktonic prochlorophytes (with which can prob- inger et al. 1991 for freshwaters). Otherwise the popu- ably be included the 'very small red fluorescing bod- lation characteristics seem little affected by nutrient ies' referred to by several authors) were reported as availability or hydrographic features. abundant in North Atlantic waters by Chisholm et al. The impression is that these characteristics of (1988) and are evidently widely distributed. They are picoplankton populations depend more on the inter- present in the coastal waters of Italy (Li et al. 1991) and nal dynamics of the ultraplanktonic community than in the northwestern (Vaulot & Partensky 1992) and on environmental factors. This idea is supported by eastern Mediterranean Sea (Wood et al. in press). It is what we know of the growth kinetics and trophic uncertain as yet whether there is any floristic similarity relationships of the component organisms, which in prochlorophyte or eukaryotic picophytoplankton seem essentially the same in freshwaters and the sea from freshwaters and the sea. The (Berninger et al. 1991).There are considerable differ- flora is still largely uncharacterized, evidently because ences in estimates of population growth rates accord- it has so far evaded isolation in culture. Analysis of ing to the methods used (Sheldon et al. 1992) but the bacterial 16s ribosomal genes from natural popula- general position seems clear. Heterotrophic tions in the Sargasso Sea shows the presence of many and the picophytoplankton have doubling times of a undescribed and so far uncultivated species (Giovan- few hours (Van Es & Meyer-Reil 1982) and around noni et al. 1990). 16 h (Stockner & Antia 1986) or 12 h (Sheldon et al. There are striking variations, however, in the compo- 1992) respectively. The principal predators on both sition of the picophytoplankton as seen in the relative these types of micro-organism, the phagotrophic fla- numbers of the prokaryotic and eukaryotic compo- gellates and , have doubling times of the order nents in relation to temperature and irradiance. In both of 24 h (Goldman & Caron 1985, Berninger et al. Lake Ontario (Caron et al. 1985) and the Irish Sea 1991, Sheldon et al. 1992). Since do not (Fogg 1986b) a logarithmic increase in cell numbers of grow during the night, growth rates of predator and picoplanktonic cyanobacteria with temperature, corre- prey are effectively equal (Sheldon et al. 1992). There sponding roughly to a doubling for every 2.5"C rise, is thus a rapid response of predator to increase in has been reported. On a transect between Australia prey and equilibrium is established rapidly, as has and Antarctica cyanobactenal picoplankton decreased been demonstrated, for example, in laboratory exper- with increasing latitude in a manner which suggested iments by Johnson et al. (1982) and by Caron et al. that temperature was the determining factor, a mini- (1991), biomass of prey and predator being thus mum concentration of 1C cells ml-' being found at tightly coupled (Kudoh et al. 1990). In -1°C (Marchant et al. 1987). It should be noted, how- (Hagstrom et al. 1988) and freshwaters (Berninger et ever, that strains of marine picoplanktonic cyanobacte- al. 1991) bacterial production and consumption have ria tolerant to low temperature do exist (Neuer 1992). sometimes been found to be nearly equal but some Heterotrophic picoplankton shows a less marked de- investigators have observed that rates fall crease in population density with decreasing tempera- appreciably short of estimated total mortalities (e.g. ture (Egan & Floodgate 1985) and eukaryotic numbers Lochte & Turley 1985). A steady state model based on tend to increase at lower temperatures (Murphy & the assumption that bacterial losses are caused by Haugen 1985). grazing, sinking and turbulent mixing gives predic- Variations in composition in relation to irradiance tions which match well with actual observations save are seen as one goes down the water column. Towards that it consistently and substantially overestimates the bottom of the euphotic zone maxima of cyano- bacterial biomass (Taylor & Joint 1990). It has been bacterial, eukaryotic and prochlorophyte populations suggested that lysis by viral action, to which Fogg: Importance of p~coplanktonin the pelagic ecosystem

cyanobacteria as well as eubactena are susceptible, speeds of the nanoplanktonic flagellates enable them may account for such discrepancies (Bergh et al. to encounter their prey sufficiently frequently to sup- 1989). Viral particles must have high production rates port their high growth rates (for references see Fogg and correspondingly high decay rates have been 1986a). demonstrated in coastal and lake waters (Heldal & Growth and predation in the ultraplanktonic com- Bratbak 1991). munity involve considerable turnover in organic mat- The total picture is thus one of a highly dynamic and ter. Release of organic carbon from picophytoplankton responsive system tending towards equilibrium. The during is appreciable (Wood et al. effect of temperature noted above is presumably due 1992). Phagotrophic flagellates are generally 'sloppy to differential effects on rates of production and preda- feeders', releasing free amino acids and, presumably, tion of cyanobacteria and eukaryotic picophytoplank- other soluble organic substances, perhaps amounting ton. The effects of irradiance are due to differential to as much as half of the ingested carbon, whilst graz- effects on the growth rates of different types of photo- ing on bacteria (Andersson et al. 1985, Hagstrom et al. trophs combined with migration to favourable levels in 1988). Many nanoflagellates, being capable of both the water column by motile forms. photosynthesis and phagotrophy, presumably con- tribute dissolved organic matter by either of these routes as circumstances dictate. Viral lysis of bacteria TURNOVER OF MATERIALS IN THE and cyanobacteria also, of course, releases dissolved ULTRAPLANKTONIC COMMUNITY organic matter. Heldal & Bratbak (1991), who found that 'phages may lyse 2 to 24 % of the bacterial popula- This rapid turnover of populations of the various tion per hour in coastal and lake waters', consider that microbial components must be paralleled by rapid this provides a major pathway for carbon flow back cycling of nutrient elements and rapid flow of energy into the bacteria. Viral particles themselves are subject through the system. To understand this we must first to rapid decay (Heldal & Bratbak 1991) and the protein look at the physical background. The linear dimen- and nucleic acids from them must enter the general sions of all the organisms which we are considering pool of dissolved organic matter. Bacterioplankton is and the spacing between them lie in the domain of able to utilize effectively the low concentrations of sub- very low Reynolds number in which molecular diffu- strates available in natural waters (Ammerman et al. sion, rather than eddy diffusion, is the predominant 1984) and turnover times may be very short (Table 1). agency for transfer of materials. Inertia is irrelevant so Mineral cycling is coupled to this traffic in organic car- that the motility of organisms is of a different kind from bon and turnover times of nitrogen and phosphorus that of the microplankton and macroscopic forms of life are correspondingly short. For example, Suttle et al. (Purcell 1977).The small radius of curvature of the sur- (1980), using the sensitive tracer l3N in studies of faces of the individual organism effectively steepens ammonium uptake by natural phytoplankton popula- concentration gradients, the total steady state flux tions in Long Island Sound, found turnover times of becoming inversely proportional to the square of the tens of hours in April to early June falling to a fraction radius (Pasciak & Gavis 1974). Episodic concentration of an hour between mid-June and late July. Similar gradients are dissipated in milliseconds. Together with results were obtained in parallel studies on phospho- the high surface area available for exchange relative to rus uptake. The implication of picoplankton in this flux volume of protoplasm this results in the potential flux was shown by the observation that up to 50% of the of nutrient ions or molecules from concentrations such flux of 13N from ambient ammonium concentrations as are usually encountered in natural waters into was into particles of less than 1 pm size. However, it picoplankton cells being much in excess of what is begins to appear that the nanoplanktonic required to maintain maximum growth rates (Raven 1986).In natural populations high specific growth rates Table 1. Turnover times of dissolved organic substances in the are maintained even under poor nutrient conditions of the sea (Kudoh et al. 1990). Surrounded as it is by a cloud of efficientlyabsorbing picoplankton cells, a rnicroplank- Substance Time (d) Source tonic organism with much less efficient uptake is poorly situated and can presumably survive only when Glucose 0.4-100 Andrews & Williams (1971) nutrient concentrations are in excess of those required Acetate 0.34-69 Billen et al. (1980) by the picoplankton. Most planktonic bacteria are Lactate 2.1-104 Billen et al. (1980) Glycollate 0.04-37 Edenborn & Litchfield (1987) motile and their swimming speeds are such that they Free amino ca 0.02 Fuhrman (1987) can move into the vicinity of a cell releasing organic acids material in a few seconds. Likewise the swimming 36 Aquat rnicrob Ecol9: 33-39, 1995

fraction is the main agent in mineralization, not bacte- through this number of levels inevitably implies that ria as classically supposed. Thus Van Wambeke & only a small proportion of the original production can Bianchi (1985a, b) found rates of ammonium regenera- reach the highest level. tion to be nearly 4 times as great per unit dry mass of micro-organism for heterotrophic flagellates as for bacteria. Similarly, Anderson et al. (1986) found in RELATIONSHIP OF THE ULTRAPLANKTONIC AND grazing experiments in batch cultures of a marine fla- MICROPLANKTONIC COMMUNITIES gellate that this was responsible for the bulk of phos- phate regeneration, bacteria making a negligible con- From all this emerges a picture of the ultraplankton tribution. as a dynamic system, approaching equilibrium, within which materials are tightly cycled so that given the necessary light for photosynthesis it can maintain itself INPUT FROM THE ULTRAPLANKTONIC indefinitely. There are parallels here with the coral COMMUNITY INTO HIGHER TROPHIC LEVELS reef and the tropical rain forest. Losses by sedirnenta- tion are minimal and any material lost to higher trophic The extent to which the ultraplanktonic community levels can be regained from the excretory or decompo- contributes to the sustenance of larger organisms has sition products of the larger organisms. Phenotypic been a matter for controversy. Picophytoplankton are adaptation is rapid, as, for example, in the response of responsible for most of the primary production in oligo- a marine Synechococcus to a transient nanomolecular trophic waters and a substantial proportion of that in increase in surface layer nitrate concentration (Glover eutrophic waters (see Fogg 1986a). It was supposed by et al. 1988). Picoplankton also has the advantage that Gray et al. (1984) that, additionally, the 'microbial loop' the large population sizes, short generation times and as it is often called in this connexion, is important in asexual propagation enable fast evolutionary response returning energy and materials to the classical pelagic to environmental change (Lynch et al. 1991). Rare food chain via the heterotrophic bacterioplankton. genotypes may become dominant within weeks or Separation of the microbial loop from other ultraplank- days if generation times are short and selection pres- tonic processes now seems artificial; cyanobacteria sures high (Wood 1990) and the genetic structure of may contribute almost as much as heterotrophic bacte- the ultraplankton is likely to be in constant flux. ria to the sustenance of bacterivores (Caron et al. 1991) The small size and adaptability of the picoplankton and remineralization, as we have just seen, is probably endow it with a superior capacity for uptake of dis- more actively carried out by flagellates and solved materials so that in this respect it can out- than by bacteria. The importance of the microbial loop compete larger organisms. The microplankton can only in providing energy for higher levels of the food chain exist when concentration of nutrients are above those was questioned by, amongst others, Ducklow et al. set by the internal dynamics of picoplankton. Ample (1986),who found that in an enclosed seawater column evidence of this is seen in the dominance of pico- in which the bacterioplankton was labelled with 14C, phytoplankton in oligotrophic seas but is also forthcom- only 2% of the label was present in larger organisms ing from experiment. Takahashi et al. (1982) deter- after 13 d although about 20% remained in particles, mined photosynthetic rates in different size fractions of presumably bacteria, of less than 1 pm size. Their con- plankton in enclosed columns in the CEPEX Foodweb 1 clusion that the microbial loop did not contribute experiment at Saanich Inlet, British Columbia, and appreciably to higher order consumers in the plank- found that under nutrient-poor conditions most photo- tonic food web was contested by Sherr et al. (1987) on synthesis was carried out by the size fraction less than various grounds but principally because one should 3 pm. With added nutrients the picture changed, the not generalize from a single experiment done under biomass and photosynthesis of the less than 3 pm frac- somewhat artificial conditions. However, the consen- tion remaining about the same but those of fractions be- sus which seems to be emerging is that the contribu- tween 35 and 202 pm increasing greatly. It is to be tion is generally slight. Hagstrom et al. (1988) from an noted that the 3-55 pm fraction gained little from the attempt to quantify organic fluxes in oligotrophic increased nutrient supply. Evidence of a different sort Mediterranean water using the minicell recapture came from the experiments, already mentioned, of technique concluded that only 6% of the total auto- Suttle et al. (1990) with 13N as a tracer of ammonium trophlc production reaches the higher trophic levels, uptake. A slight increase of ammonlum concentration Wikner & Hagstrom (1988) using the same technique over the ambient level resulted in uptake in the partic- demonstrated a predator-prey link between flagellates ulate fraction retained by a 3 pm filter increasing from of 1 to 3 pm size and bacteria which was tightly con- 33 to 80% of the total accompanied by more carbon trolled through a chain of 4 trophic levels. Passage being transferred to the higher level consumers. Fogg. Importance of plcoplankton in the pelaglc ecosystem

Table 2. Comparison of the characterist~csof ultraphytoplankton and micl-ophytoplankton

Ultraplankton M~croplankton - P P P P P P P P Slze 0 2-20 pm 20-200 pm hla~nphysical plocess determining nutrient supply Molecular dlffuslon TUIbulence, motion relative to water Form Simple unicellular Elaborate, often colonial Gas vacuoles ~ncyanobacteria Absent Present Generat~ontime Houl s Days Relatlve generation tune of predators Equal Much longer Variations ~nnatural population densities 10-10L 10'-105

The larger phytoplankton escape the predation by of magnitude. The microplanktonic community is thus the nanoflagellates which limits the picoplankton but non-equilibrium in its dynamics, a conclusion to which achieve this at the expense of becoming less efficient the late G. E. Hutchinson was forced in resolving the in nutrient uptake and more liable to sedimentation so '' (1961). that remaining in the water column becomes a prob- lem. They also have to exist in a different domain, in which turbulence rather than viscous flow becomes the CONCLUSIONS controlling physical factor. The thought occurs that it may be biologically disadvantageous to live in the no- I suggest therefore that the picoplankton should be man's-land between the regimes of viscous flow and considered as an integral component of a basic, ubiq- turbulence. Bimodal distributions of biomass, with a uitous and nearly self-contained pelagic community. trough in the 10-55 pm region, which have been Especially in oligotrophic waters but to a considerable reported by several observers (for references see Fogg extent under eutrophic conditions too, its metabolism 1991),seem to support this idea. There are examples in is dominant and that of larger organisms is merely which there clearly is not such a trough in the biomass superimposed on it. This has to be taken into account, distribution curve (e.g. Li & Wood 1988, Sheldon et al. for example, when interpreting determinations of pri- 1992) but these are from oligotrophic waters in which mary production. The use in the radiocarbon technique the concentrations of organisms of size greater than of filters which do not retain picophytoplankton will 20 pm would be expected to be low. Takahashi et al. result in an underestimate of total primary productivity (1982) found in experimental enclosures that there was but will give a more realistic estimate of the proportion a gap in the distribution of photosynthetic activity and which is available for the higher trophic levels. according to particle size between 3 and Another practical point is that the ultraplanktonic com- 30 pm and that addition of nitrate increased the growth munity, being a highly dynamic system in which some of phytoplankton of the larger size classes, accentuat- of the conlponents, for example the nanoflagellates, ing the bimodal distribution. There is certainly a radi- are extremely fragile, may be profoundly disturbed cal change in passing from one regime to the other and its metabolism altered by manipulative proce- (Fogg 1991) and, as others before me (e.g. Sournia dures. Enclosure of a sample in a bottle, or a change in 1982) have pointed out, ultraphytoplankton and temperature, sometimes produce effects which seem microplankton differ in many important respects explicable only on such a basis (Fogg & Bajpai 1988, (Table 2). As we have just seen, the microphytoplank- Fogg & Calvario-Martinez 1989, Kudoh et al. 1990). ton can only grow when nutrient concentrations are Beyond this, as pointed out by Smith et al. (1984), the above a minimum level set by the ultraplanktonic com- presence of a large heterotrophic component - the munity. This means that their multiplication is oppor- bacteria - in oceanic waters has a profound regula- tunistic with different species being favoured accord- tory effect on the metabolism of the whole plankton ing to circumstances. Because the which system, as judged by both the oxygen and carbon diox- graze on them are larger and more complex than the ide fluxes. Failure to recognize this when making com- single-celled phagotrophic flagellates and ciliates, parisons between in vjtro carbon uptake and oxygen their development is slower and generation times evolution will severely limit the value of information much longer. Thus there is a considerable lag between about productivity in the sea. the development of a microphytoplankton population and that of the zoo~lanktonpredators so that Acknowledgements, I am extremely grateful to Dr A, tion densities are less tightly controlled than those of Michelle wood for her constructive criticism of an earlier the picoplankton and variations may be up to 5 orders version of thls paper. 38 Aquat microb E

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