On the Importance of Planktonic Protozoans in the Eutrophication Process of the Baltic Sea

1 Int. Revueges. Hydrobiol. 1 76 1 1991 I 3 1 387-396 1 __

HARTMUT ARNDT

Institut fur Geographie and.Geookologie, Abt. Aquatische Okosysteme, Berlin, Germany, and Institut fur Limnologie, Osterreichische Akademie der Wissenschaften, Mondsee, Austria

On the Importance of Planktonic Protozoans in the Eutrophication Process of the Baltic Sea

key words: zooplankton, ciliates, flagellates, Baltic, eutrophication

Abstract

Analysing the results of various authors recent studies in the pelagic region of the Baltic revealed that protozoan biomass is in the same range or even higher than metazooplankton biomass. The dominant groups of planktonic protozoans are heterotrophic pico- and nanoflagellates (various taxonomic groups), large heterotrophic flagellates (mainly dinoflagellates) and ciliates. Regularly the spring bloom of phytoplankton is accompanied by a maximum of protozoan biomass which declines in early summer as a result of intensive grazing pressure by metazooplankton and changing food conditions. The analysis of results from different stations indicated that biomasses of protozoans increase with an increasing degree of eutrophication. Several trophic levels within the microbial web should be added to the traditional view on the pelagic food web of the Baltic. Our knowledge regarding the quantitative aspect of the microbial matter flux of the Baltic is very limited up to now and complex ecological (and taxonomicat) studies using standardized methods including all protozoan components are necessary. Protozoans (various trophic groups and levels), besides bacteria, should be viewed as the metabolically most active heterotrophic component in the pelagic region of the Baltic, their activity should increase with an increasing degree of eutrophication.

1. Introduction

Though the role of protozooplankton cannot be ignored according to our present state of knowledge within this volume on “Eutrophication of the Baltic Sea” our data base on protozoans in the Baltic ecosystem is very limited up to now. As early as 1894 LEVANDER provided us with a species list of the Baltic protozoans from the area around Helsinki. LOHMANN (1908) gave already quantitative estimations of the biomass of planktonic ciliates, which accounted for about 13 % of the total zooplankton in Kiel Bight. However, until the last 15 years investigators of zooplankton included generally only loricated ciliates. It were the well-known studies by FENCHEL in the Baltic and Kattegat area in the late 60’s which completely changed our opinion regarding the role of benthic and- later on-pelagic protozoans in marine ecosystems (cf. FENCHEL 1987). According to the concept of the “microbial loop” (AZAM et al. 1983) DOC released by different trophic levels (mainly by algae) is returned to the main food chain via bacteria, heterotrophic nanoflagellates and other microzooplankton. Heterotrophic flagellates and small ciliates should be the metabolically most active part of marine zooplankton. But both of these groups have only been sporadically considered in zooplankton research of the Baltic. Due to this lack of sufficient data the aim of this short contribution is rather to stimulate future attention on these important zooplankton groups than to analyse long term changes of protozooplankton in the Baltic.

388 H. ARNDT

2. Composition of Protozooplankton

The most well-known forms among protozooplankton of the Baltic are ciliates. Among ciliates mostly only tintinnids have been recorded in plankton samples due to their often large and hard loricae, which can be detected even in net samples. But mostly the biomass of these forms should have been incorrectly estimated due to a loss of significant parts of the individuals. Own investigations revealed that a large percentage (up to 80% depending on the species composition) of loricae passes the common used gazes (250 pm mesh size), in additon significant numbers of individuals leave the loricae during the process of filtration and pass the net. On the other hand GILRON and LYNN (1989) found that the ratio between the volume of loricae and the animals was mostly overestimated when calculating tintinnid biomass. Nevertheless, tintinnids can compose a significant part of protozooplankton biomass during certain periods in the Baltic, esp. during spring. Naked oligotrichs (e.g. Strombidium, Lohmanniella, Hulteria) are often of much higher importance than tintinnids, though their biomass have only recently been estimated quanti- tatively in the Baltic. Other important ciliate groups are scuticociliates (e.g. Cyclidium, Uronema) and gymnostomes (e.g. Mesodinium, Didinium, Lacrymaria).

Up to our present knowledge rhizopods play only a minor role among Baltic protozooplankton. However, recent live counts (cf. Fig. 2B) in inner coastal waters of the Baltic revealed that .at least small heliozoans can be a significant component during certain periods acting as voracious predators on flagellates and ciliates (ARNDT unpubl.). In shallow coastal waters naked amoebae and testates sometimes occur in plankton samples.

The most .numerous protozooplankton component are the groups of heterotrophic flagellates. Their significant contribution to protozooplankton biomass has only recently been recognized (e.g. FENCHEL 1982, SMETAEEK 198 1). Many diverse taxonomic groups of flagellates contain phagotrophic forms, most important among them are choanoflagellates, bicoecids, bodonids, chrysomonads, cryptomonads and dinoflagellates. One can differ between picoflagellates (< 2-3 pm) and nanoflagellates (< 10-12 pm) feeding mainly on picoplankton as well as microflagellates (<200pm, sometimes found as part of the netplankton like some dinoflagellates or Ebriu) feeding on a large range of phytoplankton, bacteria as well as on other heterotrophic flagellates. In addition there are also mixotrophic forms which contain pigments but are also able to feed as phagotrophs (cf. SANDERS & PORTER 1988).

Our knowledge regarding the species composition of Baltic protozooplankton is poor (e.g. LEVANDER 1984, VALIKANGAS 1926, SCHWARZ 1961, AGAMALIEV 1983, BOIKOVA 1989, MACKIEWICZ 1989), esp. regarding the nano- and picoplankton.

The comparison between the relative contribution of the different protozooplankton groups suffers from the lack of simultaneous sampling of all groups with appropriate methods at the same time. It is clear now that each group requires special methods: small forms have to be counted in small volumes, larger one in larger volumes, picoplankton can only be analysed by fluorescent staining, in most cases parallel live counts are indispensable, epifluorescent techniques are generally necessary to differentiate between pigmented and unpigmented forms. Some data are available from the Baltic (summarized in Fig. 2 and 3). Roughly estimated ciliates, large heterotrophic flagellates and nanoflagellates seem to compose each about one third of the protozooplankton biomass on an annual basis, with significant local (e.g. GEORGI pers. comm., BOIKOVA 1984, SETALA 1989, cf. Fig. 3 0 , E ) and temporal differences (cf. Figs. 1 and 2). The total protozooplankton biomass seems to range from <0.1 to 1 mg fresh weighM for open waters and from < 0.5 to 5 mg fresh weight/l for inner coastal waters. This indicates that protozooplankton biomass is in the same range as metazooplankton biomass (and may be even higher).

Planktonic Protozoans in Eutrophication 389

0 20 40 d

Figure 1. Short-term fluctuations of the biomass of dominant ciliates in the plankton of an enclosure exposed in Zingster Strom (Darss-Zingst estuary, southern Baltic; June/July 1986; 3.1 m3;

ARNDT orig.) I Stromhidium sp., 2 Halieria sp., 3 Tiniinnidium sp., 4 cf. Enchelys. 5 Mesodinium sp.,

6 Monodiniurn halhiani, 7 Didiniwn nasutum, 8 Cyclidium sp.

3. Seasonal Aspects

Due to short generation times (from 1-2 hours to a few days) the protozooplankton is characterized by short-term changes of protozoan groups (e.g. BOIKOVA 1984, ANDERSEN & WRENSEN 1986) as well as protozoan species (see Fig. 1). On the other hand, mean protozooplankton biomass changes considerably in the course of a year. Figure 2 sum- marizes annual data sets by different authors from the eutrophic Darss-Zingst estuary (southern Baltic), the Bay of Gdansk, the Gulf of Riga, off Ask0 (Sweden), and from Kiel Bight. One distinct maximum in protozooplankton biomass occurs in spring and a second not as pronounced maximum often appears in autumn. Mostly data are only available for ciliates. Their biomass increases when the phytoplankton spring bloom reaches its maximum and decreases with increases in metazoan biomass (Fig. 2, KRANEIS 1974, STEGMANN & PEINERT 1984). It was found that this decrease in summer is caused by the grazing pressure of metazoans (esp. copepods and Synchaeta) on ciliates (ARNDT et al . 1989a), if these metazoans are of reduced importance carnivorous ciliates can act as predators (KOPACZ 1989, ARNDT et al. 1989a, b). In addition food availability should play a significant role (PRENA 1989, ARNDT et al. 1990a).

Regarding heterotrophic flagellates only little information is available up to now. In Kiel Bight large heterotrophic flagellates showed a high biomass in spring and autumn (SMETACEK 1981, see Fig. 2 F ) , whereas in the Gdansk Bay maximum values of these forms occurred during summer; choanoflagellates reached highest values during spring (MACKIEWICZ 1989). In the Gulf of Riga mean biomass of flagellates can vary significantly, high values occur in early summer (BOIKOVA 1984, see Fig. 2 0 ) . Large heterotrophic flagellates were found to depend on phytoplankton prey and seems to be grazed by copepods (KLEIN BRETELER 1980, SMETA~EK 198 I), whereas nanofl agellates 26 Int. Revue ges. Hydrobiol. 76 (1991) 3

390 H. ARNDT

1986 I 1988 A

.4

I .2

0 D

Figure 2. Seasonal changes in the biomass of protozooplankton in various regions of the Baltic according to different authors: A ciliate fc) and metazooplankton (m) biomass in Zingster Strom, southern Baltic (ARNDT et ul. 1989a); B composition of protozooplankton in Zingster Strom in July and October 1988 (hn: heterotrophic nanoflagellates, hm: heterotrophic microflagellates 2 15 pm, h: heliozoans; ARNDT orig.); C biomass of heterotrophic ciliates (hc) and Mesodinium ruhrum (hatched area), and metazooplankton in the Bay of Gdansk (KOPACZ 1989); D biomass of ciliates and heterotrophic flagellates (hf) in the Gulf of Riga (BOIKOVA 1984); E biomass of ciliates and metazooplankton off Ask0 (Northern Baltic; HAGSTR~M & LARSSON 1984); F biomass of ciliates,

large heterotrophic flagellates, and metazooplankton in Kiel Bight (SMETACEK 198 1).

should mainly depend on bacteria and are grazed by protozoans (FENCHEL 1982, ANDER- SEN & WRENSEN 1986) and most probably by all other planktonic components which are known to feed on nanophytoplankton.

The relative contribution of protozoans to total zooplankton biomass changes from high values during autumn till spring to low values during summer (Fig. 2).

4. Protozooplankton along a eutrophication gradient

Since comparative data on protozooplankton during the eutrophication process of the Baltic (LARSSON et al. 1985, SCHIEWER this volume) are lacking the idea about the function of protozoans within this process have to be derived from the analysis of waters with a different degree of eutrophication. One of the best studied areas in this respect are the Schlei estuary and the Darss-Zingst estuary. Up to tenfold increases in the biomass of protozooplankters occur from the outer parts of the estuaries with low phyto- and bacte-

Planktonic Protozoans in Eutrophication 39 1

Figure 3. Microzooplankton distribution along eutrophication gradients in the Baltic according to different authors: A changes in microzooplankton biomass (>3 ptn) in the Schlei estuary in August 1982 (GAST 1983); B changes in ciliate biomass in the Darss-Zingst estuary in August 1962 (SCHWARZ 1975); C ciliate biomass at 2 stations of the Darss-Zingst estuary (indicated by circles) in spring 1987 (ARNDT orig.); D biomass of ciliates (ci), Mesodinium ruhrum (Mr) , and heterotrophic dinoflagellates (hd) at different stations (crosses) of the Baltic a t 0-10 m depth (a) and at 40 m depth (h) in June 1988 (SETALA 1989); E biomass of ciliates and heterotrophic flagellates at differ-

ent regions (pooled data) of the Baltic (BOIKOVA 1989).

rioplankton biomasses to the eutrophicated inner parts (e.g. GAST 1983, SCHWARZ 1975, ARNDT unpubl.; Fig. 3A-C). Though the biomass of metazooplankton increases, too, the increase is not as pronounced as that for protozoans indicating an increase in the relative importance of protozoans. However, these comparisons over a eutrophication gradient suffer from a corresponding change in salinity which has a considerable influence on species composition of protozooplankton, e.g. tintinnids (SCHWARZ 1961). But, also studies from areas of similar salinity but different eutrophic status showed a significant increase of protozooplankton biomass with increasing eutrophication. For example, protozooplankton biomasses were much higher in the Gdansk Bay compared to the Gdansk Basin (MACKIEWICZ 1989, KOPACZ pers. comm.). BOIKOVA (1989) found much higher biomasses at stations (pooled values) characterized by higher eutrophy (see Fig. 3E). She was able to distinguish water masses by an analysis of protozooplankton. A comprehensive overview on protozoans as biomonitors in the Baltic was given by BOIKOVA (1989).

Increasing amounts of protozoans in eutrophicated waters were also found by ANDER- SEN & SORENSEN (1986) comparing marine studies as well as by BERNINGER et a / . (1988) and BEAVER & CRISMAN (1989) comparing studies of limnetic waters.

Thus, it has to be assumed that eutrophication processes in the Baltic are connected with an increasing biomass (and activity) of protozooplankton. Artificial eutrophication in enclosure experiments with Baltic communities using anorganic nutrient supplies revealed significant short-term increases in protozoan biomass (e.g. SCHARF et al. 1984), however, long-term investigations over several weeks revealed only slightly higher protozoan biomasses compared to the control enclosures (e.g. KUUPPO-LEINIKKI 1989, ARNDT et al. 1989b, 1990a). Changes in species composition of ciliates followed changes in the 7.6.

392 H. ARNDT

composition of food particles (bacteria, nanoplankton), at high concentrations of protozoans carnivorous grazing by ciliates (as regulators) should be of significance (ARNDT ef al. 1989b, 1990a). An overview about experimentally induced changes in the microbial web will be presented in other chapters of this volume (e.g. TAMMINEN & KAITALA, SCHIEWER & JOST).

5 . Protozoans’ function

Marine planktonic protozoans are viewed now as the central part of the “microbial loop” (AZAM et al. 1983) controlling bacterial production and transferring energy from picoplankton to mesozooplankton. Most parts of this concept have been proved to be true also for the Baltic pelagic ecosystem. As can be derived from the available data the mean annual biomass of total protozooplankton should be the same or even higher than that of metazooplankton, their metabolic activity, however, should be several times higher. Besides net and nanophytoplankton picoautotrophs can amount for up to 25 per cent of phytoplankton biomass (e.g. LARSSON & HAGSTR~M 1982). A significant part of primary production is released as DOC which is largely consumed by bacteria (e.g. LARSSON & HAGSTR~M 1979, KUPARINEN 1985). A large part of the picoplankton production is grazed by heterotrophic protozooplankton (e.g. KUOSA & MARCUSSEN 1988, KUUPPO-LEINIKKI 1989). Large heterotrophic flagellates and ciliates should also be considered as significant herbivores (e.g. SMETACEK 1981). Protozoans in turn are known as a food source for many metazoans (cf. BURCKHARDT & ARNDT 1987). The autotrophic ciliate Mesodi- nium ruhrum~containing endosymbiotic algae significantly contributes to ciliate biomass (Fig. 2, shadded areas). LEPPANEN and BRUUN (1986) estimated that this ciliate produces about 10 % of total primary production in the Nothern Baltic during spring. Due to their very short generation times protozoans in contrast to most metazoans are able to respond very closely to changes in phyto- and bacterioplankton.

However, up to now we are not able to draw a comprehensive picture of the quantitative aspects of fluxes within the microbial web and its quantitative link to the traditional food chain. Quantitative studies of all major fluxes have seldom been made at the same time. Such studies are reserved for future international and interdisciplinary co-operative work.

In order to stimulate quantitative studies representatives of different functional groups of the pelagic cummunity of the Baltic have been figured, but with no regard to fluxes (Fig. 4). Dotted lines (to the right and below the organisms) should indicate the food spectrum. Most organisms are able to consume a wide range of trophic groups. Auto- trophs are represented by very different size classes from pico- to net plankton; mixotrophs capable of autotrophy and phagotrophy are known e.g. among nanoflagellates, ciliates, and dinoflagellates. Heterotrophic flagellates differ significantly in size, too, ranging from picoflagellates to Nocfiluca. Most pico- and nanoflagellates feed on bacteria and other picoplankton (e.g. KUOSA & MARCUSSEN 1988), whereas larger flagellates are voracious feeders also of phytoplankters (and most probable of small protozoans) often of the same size as theyself (e.g. SMETA~EK 1981). The ciliate plankton is composed of forms like some scuticociliates feeding preferably on picoplankton, others like some oligotrichs which feed on both, pico- and nanoplankton (most probably also on zooflagellates), and omnivorous or carnivorous forms of ciliates (or heliozoans among rhizopods) feeding on a wide range of food organisms. Also among metazoans there are forms feeding on pico- and nanoplankton like some rotifers and copelates, others like Synchaeta feed on phytoplankters and protozoans (e.g. ARNDT eral. 1990b), and copepods are able to feed on a wide range of food particles. Some larger invertebrates (BURCKHARDT & ARNDT 1987) as well as fish larvae (KENTOURI & DIVANACH 1986, SPITTLER er al. 1990) are able


to feed on organisms in the size down to protozoans, large coelenterates can be final points within the food chain. Adult planktivorous and piscivorous fish seems to be the only components which are not able to feed directly on protozoans.

Figure 4. Scheme of the dominant functional groups of the pelagic region of the Baltic (dotted lines indicate the expected food spectrum; for explanations see text)

Theoretically a carbon atom fixed as part of a carbohydrate by an algae can pass, if not lost via respiration, by four steps (e.g. nanoflagellate-copepod-fish) as well as by at least eight steps (e.g. picoplankton-nanoflagellate~ligotrich~idiniid-copepod-mysid-fish) and even a longer chain (if it passes the DOC-pool) to piscivorous fish. Generally only about 5 trophic levels are assumed (e.g. ELMGREN 1989) due to the about 10% trophic level efficiency. There are some reasons why more trophic levels are possible from the energetic viewpoint: e.g. higher primary production due to DOC release and picoplankton production, excreted compounds from all trophic levels which are not respired are introduced via bacteria into the food web again, gross growth efficiencies in protozoans are generally much higher than in the traditional food chain. On the other hand respiration rate by bacteria is high, however, there are data suggesting that coupling between bacteria and heterotrophic flagellates (as their main grazers) and between heterotrophic flagellates and other protozoans (as their main grazers) is very close (ANDERSEN & SORENSEN 1986, KUUPPO-LEINIKKI 1989). And also a significant part of ciliate production seems to be consumed by metazoans (ARNDT et al. 1989a). Probably a large part of the production of each trophic level within the microbial web is transfered to the next level, thus reducing the respirative losses on each level.

Closely connected with the carbon flux is the flux of limiting nutrients. Since protozoans are-besides bacteria (which sometimes compete with algae for nutrients)-the most active heterotrophic respirators, they are very important mineralizers of nutrients (e.g. CARON etal. 1988, SHERR etal. 1983). Generally the distribution of protozoans is similar to primary producers with maxima in the upper layers and thus providing the excreted

394 H. ARNDT

nutrients soon to phytoplankters. This short and rapid way of nutrient recycling should play a significant role for plankton primary production in the epipelagic region of the Baltic. On the other hand, high protozooplankton concentrations were also found below the halocline (e.g. SETALA 1989), where excretion by protozoans besides bacterial and benthic remineralization should be responsible for the observed nutrient accumulation in the depth.

Many questions regarding protozoans’ function are open for future research.

6 . Perspectives of Protozooplankton Research in the Baltic

Though we know something about the protozooplankton composition in coastal areas only sporadic informations are available from the central parts. Not only protozoan biomass is of interest, but the trophic interactions, too (see above). We have to be aware of the fact that even within the protozooplankton there are several trophic groups which have to be considered. To analyse the role of protozooplankton within the eutrophication process much more informations regarding the capacity and effect of nutrient remineralization by protozoans are necessary from field studies.

Since there is no doubt today that the microbial web significantly effects the functioning of the Baltic pelagic ecosystem the analysis of protozooplankton should be included within the Baltic monitoring programs. Up to now even distribution patterns of protozoans are still unclear. Guidelines should be prepared which allow comparisons of studies by different authors in different regions of the Baltic. Since protozoology is a fast developing field care should be taken that studies during different years are comparable. It should be considered that there are very different groups of important protozoans (pico- and nanoflagellates, large heterotrophic flagellates, very small to large ciliates, probably rhizopods) each of them requires special methods. Besides counts of fixed samples life counts are mostly indispensable. Calculations of biovolumes should be bas- ed on length measurements of living animals (where possible), geometric forms and calculations should be recommended as it was done for phytoplankters (cf. EDLER 1979).

An open field for future research of protozooplankton are parasitic protozoans which play probably a much larger role for the ecosystem functioning than we believe now.

7. Acknowledgements

I’m very thankful for valuable discussions with many members of the Baltic Family. Especially, I acknowledge the help by MARIA KOPACZ (Gdansk), ANETT PRENA (Rostock), OUTI SETALA (Hel- sinki), FRANK GEORGI (Warnemiinde) and THOMAS MACKIEWICZ (Gdynia) who provided me with their in press-results, and by MAREN VOSS (Kiel) who helped with some literature.

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Dr. HARTMUT ARNDT Institut fur Limnologie Osterreichische Akademie der Wissenschaften Gaisberg 116 A - 5310 Mondsee, Austria

Documents

On the Importance of Planktonic Protozoans in the Eutrophication Process of the Baltic Sea