MARINE ECOLOGY PROGRESS SERIES Vol. 152: 13-25, 1997 Published June 26 Mar Ecol Prog Ser

Tintinnids and rotifers in a northern Mediterranean coastal lagoon. Structural diversity and function through biomass estimations

Thong Lam-Hoai*, Claude Rougier, Gerard Lasserre

Laboratoire dlHydrobiologie - Unite Mixte de Recherche (UMR-CNRS 5556),Universite de Montpellier 11, Case 093, Place E. Bataillon, F-34095 Montpellier Cedex 05, France

ABSTRACT: Daily zooplankton samples were obtained from the Etang de Thau, France, a 70 km2 coastal lagoon of the northwestern Mediterranean Sea. The survey was monitored at 2 stations inside the lagoon and at 1 station on the seaside during 4 periods in 1994. The microzooplankton, towed with a 40 pm mesh size net, included tintinnids, rotifers, anthozoan larvae, and crustacean and mollusk lar- vae. The tintinnids and rotifers have not been studied in the lagoon yet. Over all the sampling periods, their mean biomass represented between 26 and 45 YO of the net collected mlcrozooplankton biomass, which was estimated by image analysis. Their biomass in the central part of the lagoon free of anthropic activity was close to the level observed at the nearby seaside. However, at the shellfish culture area, the occurrence of oysters and of epibiotic fauna resulted in a drastic biomass reduction of these taxo- coenoses by a factor of 10 compared to values measured in the middle of the lagoon. Samples collected during the fall indicated well-developed tintinnid and rotifer populations in this season. lnside the lagoon these populations seemed to be already abundant in early spring (March and June samples).An ordination of taxa biomasses showed 2 main factors which might have contributed to the organization of the tintinnid and rotifer assemblages: the geographical position and the thermal period. The geo- graphical position integrated the lagoon-sea water exchange. The thermal period reflected both the populations' development cycles and the env~ronmentalconstraints. The resulting effects appeared in assemblages structured in a space and time gradient. The capacity of the tintinnids and rotifers to quickly colonise the habitat (reproduction modes, resistance forms) and to use a wide range of food resources (organic matter, bacteria, pico- and nanoplankton) likely enhances their ability to serve as trophic links between primary and secondary producers. Hence, their function in the lagoon ecosystem is not minor.

KEY WORDS: Net microzooplankton Biomass structures - Environmental impact . Image analysis Mediterranean coastal lagoon

INTRODUCTION study in the Etang de Thau, FI-ance, a 70 km2 coastal lagoon of the northwestern Mediterranean Sea. They Besides dependencies and interactions related to have never been studied on this site, and have often their location between land and sea, lagoons are sub- been absent from studies related to the marine or jected to internal and irregular variations, through lagoon environments because collection was made which the biocoenosis may be submitted to abrupt and with a mesh size greater than 100 pm. The summarised undamaged evolution (Amanieu & Lasserre 1982). qualitative fauna observations of Mathias & Tchern- Thus they appear to be original entities compared to iakofsky (1932) and Mathias & Euzet (1951, 1962) adjoining ecosystems. Tintinnids and rotifers were the included 7 species of tintinnids (Tintinnopsis beroidea, 2 microzooplankton groups surveyed in the present T campanula, Stenosemella ventncosa, Favella ehren- bergii, F. serrata, Petalotncha ampulla and Eutintinnus fraknoii) and 2 species of rotifers (Synchaeta neapoli- tana and S. triophfalrna). More recent studies of the

O Inter-Research 1997 Resale of full article not permitted Mar Ecol Prog Ser 152: 13-25. 1997

zooplankton (Lam-Hoai 1985, Jouffre 1989, Lam-Hoai The survey was performed daily during 4 sampling & Amanieu 1989) dealt only with the mesozooplank- periods in 1994. (1) from 21 to 25 March, (2) from 20 to ton. Contribution estimates of the populations to the 24 June, (3) from 26 to 30 September, and (4) from Shannon's diversity index already allowed typi.ca1 28 November to 2 December. They corresponded assemblages of the lagoon or of the coastal zone to be roughly to the major events in the annual cycle of the distinguished and populations with strong demo- oyster culture (growth, reproduction, post-breeding graphic outbursts or those that are dominant in bio- and pre-wintering periods). This 5 d replicating me- mass to be specified (Rougier & Lam-Hoai in press). In thod may reduce the variation in the zooplankton the following work, we aim to provide an understand- catch. Each daily zooplankton sample was made up of ing of the biomass fluctuations of tintinnid and rotifer 3 vertical tows at the station, from 2 m depth up to the populations in space and time and to outline the struc- surface, with a 40 pm mesh size net and a 0.3 m dia- tural diversity of these taxocoenoses. Determination of meter opening. Obviously, individuals less than 40 pm such features associated with the analysis of relation- and the fragile organisms (flagellates and aloricate ships between populations and environment helps to oligotrichs) were not retained in the samples. The evaluate the function of microzooplankton in the tintinnids (loricate oligotrichs) did not suffer any ecosystem, complementing previous studies on the damage when captured by a plankton net. The plank- other zooplankton groups at this site. ton material was then fixed in a buffered 4 "/o form01 so- lution and slightly coloured with Rose Bengal to obtain the besi cvnirasted image in image analysis. An aque- MATERIAL AND METHODS ous solution of 50% magnesium chloride was added to sub-samples (1 cm3 to about 100 cm3) before fixation in Zooplankton were collected at the Etang de Thau Stns order to reduce the stress contraction of the organisms, T and Z and M at the seaside (Fig. 1). Stn T is situated in such as aloricate rotifers, during identification. the central area (7 m depth),while Stn Z is in the middle Environmental conditions were recorded concur- of a shellfish culture area, near the NW bank of the la- rently with the plankton sampling. Meteorological goon (5 m depth), and not far from the Canaux de Sete data were limited to the wind direction and force, (about 7 m depth) by which the essential water ex- which were recorded in situ by B. Bibent (pers. comm. changes between the lagoon and the sea occur. 1995) with a digital data logger meteorological station. Water temperature ("C) and salinity (psu) were measured with a WTW 196 salinometer low 0 IOE coupled with a Tetracon 96T sensor cell. From

45~ water samples, chlorophyll a concentration (pg 1-l) was determined by A. Vaquer (pers. comm. 1995), cellular concentrations (ind. I-') of bacterioplankton, picophytoplankton and phytoplankton >2 pm were estimated by C. Courties (pers. comm. 1995) through a flow- cytometer. The multiple-species origin of chlorophyll data and the wide size range of phytoplankton prevented their use in further analyses. Because of the extremely high density of some samples, they were separated into suc- cessive fractions (Folsom splitter) in order to facilitate sorting a.nd to avoid cluttering in the MAR numeration of organisms Zooplankter count, measure of their size and estimation of their MEDITERRANEAN SEA biomass in wet weight were made by an image analysis technique proposed by Lam-Hoai (1991) and Lam-Hoai & Gril(1991). 5 km With this technique, a zooplankton individual viewed under the microscope appears as a Fig. 1. Etang de Thau; broken line delimits the shellfish culture sectors. Silhouettel the form Of which depends On the The 3 sampling stations, T, Z and M,were positioned inside and outside image contrast. This silhouette can be charac- the lagoon tensed by its perimeter and its surface, which Lam-Hoai et al.: Structural diversity and function of tintinnids and rotifers 15

define a specific form factor. To assess Table 1 Identified taxa, their identity codes, and their biomass percentages the third dimension of the object, a averaged over daily data during the 1994 survey at Stns M, T and Z morphometric model which preserves the form factor of the organism, and Taxon Code M (%) T(%) Z (%) therefore of its volume, was used. According to Mullin (1969) and Omori Tintinnids Amphorides amphora (Cl. & L ) AAM 1.60 0.01 & Ikeda (1984),if the specific weight of Codonella acerca Jorq C AC 0.04 0.01 an animal is close to 1, it is reasonable I Clodonella cratera [~eidvl CCR 0.23 0.05 1 to establish the equivalence of its vol- Codonella galea Hck. CGA ume to its wet weight (1 cm" 1 g). Codonellops~smorchella (C1 ] CM0 Codonellopsis orthoceros (Hck) Density and wet biomass units were COR Eutjntinnus fraknoil Dad E FR evaluated per cubic meter. Favella spp. FAV As the dimensions of the zooplank- Heljcostomella subulata (Ehr.) HSU ters depend on the different phases of Metacytis rnediterranea (Mereschk.) MME their development, it is difficult to Parundella aculeata Jorg. PAC Petalotricha ampulla (Fol) Kent PAM classify the individuals rationally into Rhabdonella spiralis (Fol) RSP the size scale proposed by Dussart Salpingella acuminata (Cl. & L.) SAC (1965). In the net sampled micro- Stenosemella ventricosa (Cl. & L.) SVE zooplankton, the tintinnids' and roti- Tintinnidium sp. TIN Tjntjnnopsis beroidea (Stein) fers' largest dimension in a few cases TBE Tintinnopsis ca~npanula(Ehr.] TCA exceeded 300 pm. For convenience, Tintinnopsis corniger Hada TCO crustacean nauplii, anthozoan and Tintinnopsis cylindi-ica Dada y TCY mollusk larvae were also classified Tjntjnnopsis sp.2 TS2 into this category (Table 1). The other Rotifers Brachion~isplicatills (Muller) BRA holoplankton and meroplankton or- Colurella colurus (Ehr.) ganisms collected by the net were CC0 Synchaeta baltica Ehr. SBA allocated to the mesozooplankton. Synchaeta cecilia Rousselet SCE Identification of tintinnids (ciliates) Synchaeta grimpei Remane SGR is made by their lorica morphology, Synchaeta neapolitana Rousselet SNE Synchaeta tnophtalma Lauterborn. STR according to classifications of Jor- Synchaeta vorax Rousselet svo gensen (1924), Kofoid & Campbell Testudjnella sp. TES (1939), Margalef & Duran (1953) and Tnchocerca marina (Daday) TMA Balech (1959). Nevertheless, Laval- Other microzooplankton groups Peuto & Brownlee (1986) underlined Anthozoan larvae ANT Cirripeda nauplii CIR the great variability of this shell. For Copepoda Calanoida nauplii CAL this reason, Tintinnopsis butschlii is Copepoda Cyclopolda nauplii CYC considered as a phenotype. . of T cam- I Copepoda Harpacticoida nauphl HAR 21.09 2.89 13 90 1 panula (TCA in Table 1). Some tintin- E"phausiacea nauplll EUP 3.35 0 02 Gasteropoda larvae GAS 0.11 8.09 8 79 nids have not been identified to the Lamellibranchla larvae LAM 3.45 14.40 23.90 specific level: Tintinnopsis sp. 2 (TS2) and Tintinnidium sp. (TIN). Favella spp, taxa (FAV) mainly includes F. serrata (Mob.) Jorgensen and sporadic individuals of days. Differences in biomass between sites or stations F ehrenbergii (Clap. & Lachm.) Jorgensen. Rotifers, and their evolution during the survey were recognised assimilated to ciliates in the beginning of the 18th cen- using frequency diagrams. Population organisation tury, are in fact very small metazoans (less than 1 mm), trends were assessed with a factorial correspondence and constitute a separate zoological embranchment, analysis (FCA) of these biomasses. Pearson's correla- Classification criteria of Voigt (in Koste 1978), as well tion coefficient r was computed from dally biomasses as these of Rousselet (1902), Remane (1929), Hollow- over the whole survey on the one hand between each day (1949), Berzins (1960), and Arndt et al. (1990), taxonomic group (Y) and each environmental variable were used for rotifer identification. The majority of the (X), and on the other hand between taxa (Yand X). species encountered during 1994 belonged to an alori- This coefficient measured the probable connection or cate group, the family of Synchaetidae. dependence between Y and X, thus allowing interpre- Most of the population analyses were performed on tation of relationships between populations and envi- tintinnid and rotifer biomass averaged over 5 sampling ronment and of assemblage structures. It is signifi- 16 ~VarEcol Prog Ser 152. 13-25, 1997

cantly different from zero when its absolute value is enced by these displaced water masses. During the larger than the one given by the Fisher & Yates tables 1994 survey, prevailing E-SEwinds in September and (2-tailed test) for n - 2 degrees of freedom, and for a in November-December were associated with cloud given error probability (Klugh 1970), n being the num- cover (barometric depression). Their direction and ber of data couples used to define r. For practical pur- their duration forced a fraction of the waters from the pose, only correlations calculated from at least 10 cou- Rhone Delta (100 km to the east) to move westward ples of data and having an error probability equal or along the coast. These events induced a drop in the less than 0.05 in a bilateral test were retained as signif- local salinity, particularly conspicuous at Stn M by icant. In some cases, microscopic preparations were September (from values of 36-37.5 to values as low as necessary in order to specify the type of relationship 30-34). In such meteorological conditions, the suitable existing between the populations. orientation of the lagoon inlets reinforced the coastal water input, which was detected at Stn Z. During the survey, the water temperature varied RESULTS between 12.7 and 23.2"C in the lagoon with a maxi- mum-minimum difference of 10.5"C. At the seaside, During the 1994 survey in the central part of the this difference in the range (11.8 to 20.2"C) was more Etang de Thau (Stn T), the overall biomasses of tintin- attenuated. The salinity in the sea remained close to nids and rotifers were estimated as high as 20.41 % of 37, except during the period of dilution by the waters the ilci zoopial~kivri totai biomass and 44.8'310 of the coming from the RhBne Dclta. In the lagoon, salinities, net microzooplankton biomass. Comparable counts of from low values in March (31.5-32.2) and in Novem- tintinnids larger than 40 pm, taken from bottle samples ber-December (30.5-31.5), were raised by evaporation as well as from net samples, showed an estimated to 35.9-36.5 in June and to 36.9-37.9 in September. abundance of up to 1 YO of the total ciliate density at Relationships between these environmental parame- Stn M and between 6 and 17 % at Stn T. The fraction ters and zooplankton populations will be analysed in a that escaped from the net collections was mostly alori- later section of this study. cate oligotrichs in the 10 to 60 pm size range (modal size: 20 to 30 pm). The remaining fraction was com- posed of tintinnids, loricate oligotrichs that could be of Variations of tintinnids' and rotifers' overall the magnitude of the copepod biomass (e.g. Stn T, June biomasses in space and time 1994). Among the 40 taxa identified in the whole microzoo- Highest recorded taxa biomasses were about plankton net collection, 21 tintinnid and 10 rotifer taxa 19000 pg m-3 (average 5200 1-19 m-3) for the tintinnids are listed in Table 1. The tintinnid specific richness and 12000 pg m-3 (average 2240 pg m-3) for the (taxa number) in the central lagoon Stn T was slightly rotifers, while rare taxa did not exceed 50 pg m-3 for inferior to the one from the seaside Stn M (13 vs 15). A the former group and 10 pg m-3 for the latter. The contrario, the marine station counted 7 rotifer species overall biomass of the taxocoenoses fluctuated from vs 8 found in the lagoon. Populations originating in one station to another and also according to the sam- coastal waters were sometimes found at shellfish cul- pling periods: 2 to 48% of the net microzooplankton ture Stn Z. These taxocoenoses lived in an environ- biomass at the seaside (Stn M), 27 to 68% in the lagoon ment under physical constraints and influenced by central area (Stn T) and 20 to 39% in the shellfish cul- forcing factors. ture zone (Stn Z).Cha.racteristic differences are shown in a sector diagram (Fig. 2). At the coastal Stn M, tintinnid and rotifer biomasses. Environment and forcing factors which were very low in March and in June (maximum 1810 pg increased 10-fold in September (19997 pg Hydrodynamics in the Etang de Thau are known to m-3).This increase was mainly due to the development be linked with meteorological conditions, especially of the rotifer Synchaeta triophtalma (with more than with the wind regime (Lam-Hoai & Amanieu 1989) 40 ind. I-'), which had the highest mean biomass of all Within the usual tidal range (maximum amplitude 0.05 the rotifers collected in 1994. The conditions encoun- to 0.07 m), most of the water exchanges between the tered at Stn M in September were rather unusual, lagoon and the sea occur through the Canaux de Sete being marked by a consistent drop of the salinlty (aver- because of their large size (7 m depth and 44 m width). aged values: 33.1 at Stn M compared to 37.7 in the Hydrodynamic modelling from Millet (1989) showed lagoon). Coastal water dilution in this period could be that in periods of S-SE winds, the area surrounding due to the RhBne River flows driven towards the Etang Stn Z facing these channels could have been influ- de Thau as previously mentioned. This situation would Lam-Hoai et al.. Structural diversity and function of tintinnids and rotifers 17

1994 March June September November-December El El Station TcA M

Fig 2. Biomasses of tintin- 4239 41246 37490 nids (grey area), rotifers 10907 (dark area) and other net microzooplankton (blank area) in proportion to the HSU overall net microzooplank- station ton mean biomass (number T in the bottom-left corner of SBA each box, in pg m-3) which is shown by the size of 17840 46626 11234 the sector diaarams..2 Some diagrams have had to be magnified (magnification 1x21 (X21 El m shown). Codes of tintinnid HSU FAV Station and rotifer dominant popu- z lation~are plotted adjacent (9 SBA S'"" to the corresponding sec- tors (see Table 1 for ex- 5576 10441 5715 1751 planation of identrty codes)

equally explain the presence of S. triophtalrna at Stn Z Structural diversity of tintinnid and rotifer and its practical absence at the other station in the assemblages lagoon (Stn T). Tintinnid and rotifer biomasses remained high (10736 1-19 m-3) in November-Decem- The factorial correspondence analysis of taxonomic ber. biomasses sums up to an inertia of 2.638. Indepen- The change in biomass throughout the year was dif- dently from the image quality in the ordination space, ferent inside the lagoon. On the one hand, whatever the horseshoe disposition (Guttman effect) of projected the season, biomass values at Stn Z in the shellfish- points on several factorial biplot displays suggested a culture zone were approximately 10 times less than correlation between the ordination factors. Therefore those at Stn T. This large difference may be caused by the gradient structure in the space formed by 2 factors the trophic pressure from the cultured shellfish and (or axes) F1 and F2 could be explained by 58 O/oof the their epifauna. Such a pressure is exerted both on the total inertia. phytoplankton bionlass, thus reducing available food Samples from the seaside Stn M (M1 to M4, Fig. 3a) resources in appropriate size fractions (even when liv- clearly show less dispersion than the samples collected ing food items are rejected by the filtering mechanism in the lagoon (T1 to T4 and Z1 to 24). The tintinnid and of larger predators, the probability of survival of the rotifer biomass distributions in the lagoon fluctuated to former remains reduced), and directly on the tintinnids a greater extent than they did at the seaside. The M3 and rotifers themselves. On the other hand, biomasses and T1 samples and the T1 and T2 samples contributed at Stn T rose to 12015 pg m-3 in March in conjunction to define respectively the factors F1 and F2, their with a high biomass of the rotifer Synchaeta baltica in absolute contribution values being more than 35% of June when the Tintinnopsis corniger outburst pro- the total inertia. The axis F1 represented a geographi- duced the highest biomass value measured in 1994 cal gradient (sea-lagoon) and the axis F2 a gradient (25215 pg m-3), and finally in September (11495 pg corresponding to the thermal periods (cold-warm peri- m-3) with the high growth of the tintinnids Favella spp. ods). In the ordination space, the lagoon samples T3, Thus, important demographic movements were very T4, 24 and especially 23 were closed to those collected localised in space and time. Tintinnids and rotifers con- at the seaside, their position could be related to the stitute an abundance structure which may characterise coastal water input via the Canaux de Sete by the a given site at a given time. Such organisation, sup- action of both the tidal movements and the prevailing ported synthetically by an ordination of biomass data winds. set crossing taxa and samples, can be related to their With their absolute contribution values greater than environment. 25 %, Synchaeta baltica (SBA) and S, triophtalma (STR) 18 Mar Ecol Prog Ser 152: 13-25, 1997

COLD PERIOD ~2 (27%) salinity at the seaside (30-34 vs usual 36-37.5). This coastal feature was valid for the 1994 survey, but I probably could not be generalised for SBA, a charac- teristically cold season species in the lagoon. Low bio- mass populations tended to occur either in the coastal waters (CMO, CGA, COR, PAM, SAC, SGR, TES) or in the lagoon (CAC, CCR, MME, PAC, TBE, BRA, CCO, SCE) except for Helicostomella subulata (HSU) which showed much higher biomass in the lagoon. SEA 1 LAGOON The position of the taxa on the biplot display depended on the sampling periods in which they were available. By their occurrence at all the stations and their intermediate disposition in the ordination space, Favella spp. (FAV), Tintinnopsis carnpanula (TCA), S. vorax (SVO) and Trichocerca marina (TMA) appear to have been opportunist populations in the assemblages. However, FAV and TMA populatlons developed better inside the lagoon, while TCA and SVO 11.ad p.l.eva1en.t biomasses at the seaslde. The analysis positioned the taxa in their preferential envi- SBA ronment and illustrated the fluctuation trends of pop- ulation~according to the sampling periods and to the stations. Similar features were found with the other --. , TIN. . I microzooplankton components (italicised codes, Fig. TCA . HSU CGA* EFR . 3b) considered as additional observations in the STR SVE *# *ANT -)BE dZS TS2 SNE analysis. Mollusk larvae (LAM, GAS) and most cir- RSP CyC *BRA** < riped nauplii (CIR) occurred inside the lagoon and in CL l &*, A /l I warm periods, while anthozoan larvae (ANT) and CM0 coR :W HAR~~~ FI euphausiacean nauplii (EUP) appeared only at the PAM . GAS CCR seaside in colder periods. Copepod nauplii (CAL, MME~?~ CYC, HAR), which occupied an intermediate position in the biplot display, increased their biomass towards TCY the fall, especially at Stns M and T. The biomass ordi- TCO nation of the net collected microzooplankton shows its CAC structural diversity in the pelagic biocoenosis. Such an organisation may result from relationships between the environment and the populations and between Fig. 3. Biplot display (axes F1 and F2, shown with their the populations themselves. The following analysis respective percentage of explained inertia) ~ssuedfrom facto- rial correspondence analysis of taxa biomasses (a) Samples tries to look for consistent links between these. (T, Z, M: stations; 1 to 4: sampling penods) disp1a)~cdalong geographic and thermal gradients; (b)taxa dlsplaycd In their preferential environment.See Table 1 for explanation of iden- Relationships between populations and environment tity codes. Codes in italics correspond to nduplu and mero- plankton. Codes shownwithout assoc~atedsymbols are for hidden plots Relationships between environmental variables and microzooplankton on the one hand and those between the different populations on the other can be simply defined the axis F1, and Tintinnopsis corniger (TCO) measured by the Pearson correlation coefficient, applied and S. baltica the axis F2 (Fig. 3b). The double defini- to the daily samples collected at each station (Table 2) tion of an axis by the same modality (e.g. taxon) Significant correlations were found more often at Stn M reflected the Guttmann effect previously mentioned. than at Stns T and Z. This seems to indicate more selec- SBA and TCO were plotted in the part of the ordina- tive conditions in the lagoon. Relationships of tintinnids tion space which represented the lagoon, while in- and rotifers with environmental variables such as the versely STR was found towards the sea pole. The water temperature (Tem) and the salinity (Sal) differed position of STR was due to a population bloom in spe- according to the populations and the stations. Within the cial environmental conditions at Stn M (M3), e.g. low value ranges observed in the Etang de Thau (see 'Envi- Lam-Hoal et al.: Structural diversity and funct~onof t~ntinnidsand rotifers 19

Table 2. Significant correlations (r)between the environmental parameters (Tern: temperature; Sal: salinity) and tintinnid and rotifer populations (alphabetical codes, see Table 1 for explanations), between pairs of these populatlons, and between the tintin- nid and rotifer populations and picophytoplankton (Pic; Ost: Ostreococcus tauri), bacterioplankton (Bac; Cya: cyanobacteria) and mesozooplankton (31: Sagitta minima, 56: Paracalanusparvus, 73: Acartia rnargalefi, 89: Oithona nana, 97: Euterpina acutifrons, 99: Microsetella norvegica, 108: Oikopleura dioica, 117: Phoronis. 122: spionid larvae, 123: capitellid larvae, 162: Ciona larvae). df: degrees of freedom

Relation- Stn M Stn T Stn Z Relation- Stn M Stn T Stn Z ships r df r df r df sh~ps r df r df r df - -0.45 13 CAL-FAV CAL-STR CAL-SBA CAL-SVO CAL-TMA CYC-FAV CYC-EFR CYC-TCY CYC-TCO CYC-TS2 CYC-STR CYC-TMA HAR-RSP EUP-FAV EUP-TCA

FAV-3 1 FA\'-73 FAV- 123 TCA-89 TCA-97 TCO-73 TCO-97 TCO-l08 TS2-97 HSU-l17 HSU-l62 FAV-STR RSP-56 FAV-SVO RSP-108 TCY-STR RSP-122 TS2-STR STR-99 CIR-FAV STR-123 CIR-TCY SBA-l08 CIR-TIN SBA-l17 CIR-STR SVO-73 CIR-SVO TMA-73 GAS-TCO TMA-97 LAM-TMA TMA-108 TMA-122 ronment and forcing factors'), these variables were talma (STR) at Stns M and T were found in periods of linked to populations in different ways, e.g relatively low salinity, while S, vorax (SVO) seemed to - Favella spp. populations (FAV) may develop well in prefer a high salinity environment. low temperature (negative correlation, Stn M) and in Biological factors included cellular concentrations of h~ghsalinity (positive correlation, Stn T); picophytoplankton (Pic; and Ost: Ostreococcus taurj), - Tintinnopsis cylindrjca (TCY,Stn Z)as well as Syn- of bacterioplankton (Bac; and Cya: cyanobacterla) and chaeta baltica (SRA, Stn T) occurred in low tempera- of other net collected zooplankton populations. Posi- ture and low salinity cond~tionsinside the lagoon; tive correlations between different populations did not - Tintinnopsis corniger (TCO) permitted warmer only mean their simultaneous occurrence at the site, waters with high salinity (Stn T); such correlations may also reflect either the same - Tintinnopsis campanula (TCA) and Tintinnopsis requirements for physical and chemical conditions and sp.2 (TS2) populations at Stn M and Synchaeta trioph- food availability, or the backward effect from popula- 20 Mar Ecol Prog S - - tion mutual controls. Negative correlations might sug- (e.g. spring and autumn periods) and on the food avail- gest predation pressure or the direct control of one ability (microflagellates, dinophyceans, diatoms, cili- population over another. ates). Biomass estimations of these larval stages figured Many positive correlations between tintinnid and in a range of 450 to 13500 pg m-3 (average 8872 pg m-3) rotifer populations and picophytoplankton as well as for the nauplii, 500 to 25000 pg m-3 (average 3154 pg bacterioplankton related generally their simultaneous m-3) for the veligers and 500 to 17 600 pg m-3 (average occurrence in the water column (Pic-TS2, Pic-STR, Pic- 4667 pg m-3) for the meroplankton. SVO, Ost-SVE, Ost-TS2, Ost-STR, Ost-SVO, Bac-TS2, Correlation analysis was conducted to establish the Bac-STR, Cya-EFR, Cya-STR). In some cases these trophic function of the tintinnid and rotifer popula- positive correlations may indicate trophic relationships tion~,which could be examined through microscope without a demographic impact on the prey popula- observations and literature data. It is obvious that the tion~,e.g. as for the couple cyanobacteria-Eutintinnus food diet of an organism cannot be fully defined by Eraknoii (Cya-EFR) at Stn M; Bernard & Rassoulzade- simple microscope observations. For instance, diatom gan (1993) stated that some tintinnids (Eutintinnus sp. frustules or some dinophyceans are more easily identi- and Tintinnopsis beroidea) fed exclusively on cyano- fied than other phytoplankton cells which constitute a bacteria. The positive correlation between the couple larger fraction of food for tintinnids and rotifers. Micro- bacterioplankton-Synchaeta triophtalma (Bac-STR, scope preparations show the occurrence of dino- Stn M) could have matched the trophic design from phyceans (Fig. 4a, b), of diatoms, and of other tintin- Do!ar? & Ga!!egos (1991): the predation of Sync19aei.d riids of smaller sizes, such as Tintinnopsis sp. in Favella spp. reduced the stocks of heterotrophic microflagel- cells during the 1994 survey. A tintinnid (Tintinnopsis lates and by this, reduced their grazing pressure on sp.) was observed in the body of a Synchaeta vorax bacteria. The only negative correlation, Ostreococcus predator (Fig. 4c), and a mastax of the small S. cecilia tauri-7: corniger (Ost-TCO) at Stn T, suggested that was found in another individual. The stomach of a S. this tintinnid might graze on the picophytoplankton. vorax individual from the November-December period Moreover, negative correlations between tintinnids was occupied by a dinophycean (Prorocentrum sp.) as and rotifers and other zooplankton populations may well as a diatom (Oestrupia sp.) (Fig. 4d) The above signify prey-predator relationships with demographic feeding behaviour can switch to cannibalism, if the control, e.g. prey is smaller than the predator; such an event was - Within the microzooplankton assemblages: at the observed twice with living plankton. seaside, between euphausiacean larvae and Tintin- nopsis campanula (EUP-TCA); in the lagoon, between cyclopoid nauplii and T corniger (CYC-TCO) or T. DISCUSSION AND CONCLUSION cylindrica (CYC-TCY), between calanoid nauplii and Synchaeta triophtalrna (CAL-STR). Estimations of the tintinnid and rotifer abundances - Within the mesozooplankton components: at the in the Etang de Thau and averaged over the 2 stations seaside, between the cyclopoid Oithona nana and and all the sampling periods were, respectively, 75 700 Tintinnopsls campanula (TCA-89) and between the ind. m-3 (5200 pg m-" and 3530 ind. m-3 (2240 pg m-3). harpacticoid Euterpina acutifrons and T campanula These values were less than those from other sites: (TCA-97) or Tintinnopsis sp.2 (TS2-97); in the lagoon, Gulf of Marseille (Travers & Travers 1971, net and between appendicularian Oikopleura dioica and Syn- Utermohl's methods), Villefranche Bay (Rassoulzade- chaeta baltica (SBA- 108). gan 1979, 50 pm mesh net). However, in contrast, they The simultaneous occurrence (positive correlations) were higher than in the eastern areas, as in Lebanese of tintinnid and rotifer populations with meso- coastal waters (Abboud-Abi Saab 1989, 50 pm mesh zooplankton populations (numerical codes in Table 2) net). North Irish Sea tintinnid densities reported by suggests that the former constitute potential food re- Graziano (1989) fluctuated from 1 to 729000 ind. 1-' sources for the latter, as has been proposed by many (Nansen-Peterson sampler). Moreover, density estima- authors (Koehl & Strikler 1981, Robertson 1983, tions of aloricate oligotrichs in the Etang de Thau may Stoecker & Sanders 1985, Williamson & Butler 1986, reach 6 to 18 times that of the tintinnids. Obviously this Ayukai 1987, Alvarez 1988, Egloff 1988, Urban et al. group needed more appropriate investigations. 1992, White & Roman 1992, Pinel-Alloul 1995). The Rotiferian densities were generally less than those col- positive correlations with naupliar stages (CAL, CYC, lected in 70 to 90 pm nets by Heinbokel et al. (1988), HAR, EUP, CIR), or with veligers (GAS, LAM) and other Ferran et al. (1982),and Hernroth (1983), the Etang de meroplankton (larvae),such as Phoronis (117),spionids Thau being more open to sea waters. The biomass (122), capitellids (123) and Ciona (162), should likely analysis shows 2 factors which affected the assem- signify a dependence on the environmental conditions blage structure of the tintinnids and rotifers: the geo- Lam-Hoai et al.. Structural diversity and function of tintinnids and rotifers 2 1

Fig. 4. Tintinnids and rotifers showing ingest- ed organisms. For all plots, scale bar = 50 pm. (a) Living Favella indi- vldual with d~nophy- cean cells (arrow); (b) a fixed Favella individual with dinophycean cells (arrow); (c) a tintinnid ~ndividual(Tint~nnopsis sp.) (arrow) inside Syn- chaeta vorax; and (d) a diatom (Oestrupia sp.) cell (right arrow) and a dinophycean (Proro- centrum sp.) cell (left arrow) inside S. vorax 22 Mar Ecol Prog -Ser 152 13-25, 1997

graphical position and the thermal period The geo- question: does 0. tauri, the smallest eucaryote cell graphical position integrated on the one hand the tidal (Courties et al. 1994), have the same trophic function influence (maximum tide amplitude: 0.05 to 0 07 m) as towards some tintinnid populations inside the lagoon a lagoon-sea gradient, and on the other hand the force as cyanobacteria has with Eutintinnus fraknoii at the and duration of prevailing winds. The effect of the seaside? Among the ciliates, aloricate oligotrichs may thermal period constituted another gradient which have a food diet similar to the tintinnids since they con- resulted both from population development cycles and sume particles in the size range of 0.5 to 10 prn (Ras- from environmental constraints (e.g. temperature, soulzadegan et al. 1988). But within the same size, salinity). Large hydrological variability linked to mete- these naked ciliates would feed on smaller prey (M. orological conditions may impose important demo- Peuto-Moreau pers. comm 19971, The rotifer genus graphic outbursts and declines in the pelagic bio- Synchaeta, the main representative genus found in the coenosis in an almost unforeseen way. Spatial and Etang de Thau, were micropredators, preferring temporal fluctuations of tintinnid and rotifer popula- microflagellates of the 10 to 20 pm size range (Pournot tions inside the lagoon were shown to be governed by 1977, Dolan & Gallegos 1991, Pont 1995). the trophic pressure of shells and epifauna from the Tintinnids and rotifers may be in competition with shellfish-culture installations and by the sea input each other for the 10 to 20 pm phytoflagellates. influence on Stn Z. It would be obvious to include the Taniguchi & Kawakami (1985) have cultivated the inter-population relationships (e.g.predation, competi- tintinnid Favella taraikaensis with Prorocentrum as the tion) among the multiple mechanisms dffecting the only source ot food, and in fact this dinophycean was assemblage organisation. Such features could be repli- also consumed by the rotifer Synchaeta vorax in the cated in term of densities analyses, since they concern Etang de Thau (see Fig, 4d). The competition could taxocoenoses without large differences in their size explain the scarcity of S. triophtalma in September at distributions (Rougier & Lam-Hoai unpubl. report Stn T, while [his rotifer was largely dominant at the 1995). other 2 stations; their tintinnid competitors, Favella, The outlined relationships between populations and were 15 times more abundant at Stn T. Hernroth (1983) environment were coherent with the previously attributed the decline of rotifers at Fjord Gullmar in described structural diversity. They underlined that Norway to the competition for food with tintinnids. salinity was a structuring factor at the seaside, and that Moreover, compared to their competitors, such as cili- temperature was an additional one inside the lagoon, ates and copepods, which may grow at lower concen- although each of them could exert their influence trations of food (Heinbokel et al. 1988) rotifers would locally on other processes (reproduction, growth). be penalised. Tintinnids are also in competition with Trophic function of tintinnids and rotifers in the copepods, because the latter can consume small parti- pelagic biocoenosis appeared to be important. They cles through one of their modes of filtration (passive are either predators or competitors as well as preys, as type), according to Pourriot & Lescher-Moutoue (1983). indicated by correlation analysis and by the occur- Tintinnids, as purifying agents, are far more efficient rence of nanoplankton in Favella cells and of tintinnids consumers of very small food particles (Rassoulzade- inside Synchaeta individuals Our observed data agree gan 1982), especially since their biomass could have with trophic information given by many authors: tintin- similar magnitude to the copepods' (June Stn T). nids and rotifers are trophic links between net micro- Copepods are the main predators of tintinnids (Koehl zooplankton and mesozooplankton populations. In the & Strikler 1981, Robertson 1983, Stoecker & Sanders literature (Hollibaugh et al. 1980, Rassoulzadegan & 1985, Ayukai 1987, Alvarez 1988, Egloff 1988, Urban et Etienne 1981, Burkill 1982, Andersen & Sorensen 1986, al. 1992, White & Roman 1992) According to Gifford Verity 1986, Fenchel 1987, Bernard & Rassoulzadegan (1991), calanids may consume phytoplankton as well 1993, Laval-Peuto 1993), tintinnids use a large spec- as zooplankton, and this ability would mean an adap- trum of food resources such as organic matters, bacte- tation to changes in food resources. Stoecker & Egloff ria, pico- and nanoplankton, maximum food particle (1987) noted that Acartia tonsa produces 25% more size being 41 to 46% of the consumer oral diameter eggs when they are fed with ciliates and rotifers than (Spittler 1973). Some tintinnids preferably select when they are fed with the same concentration of dinoflagellates (Stoecker et al. 1981). Rassoulzadegan phytoplankton. Copepods, the main predators of (1982) observed that growth was greater when they tintinnids, may also consume rotifers (Egloff 1988, fed on microflagellates. Conover (1982) reported that Pinel-Alloul 1995). As far as the predation on rotifers tintinnids ingested nanoplankton with daily rations is concerned, Synchaetae aloricate species are quite from 0.5 to 3 times their own biomass. The negative available food items for marine calanids (Williamson & correlation between Ostreococcus tauri and Tintinnop- Butler 1986, Egloff 1988, Pinel-Alloul 1995). These sis corniger observed at Stn T leads to the following data permitted the explanation of prey-predator rela- Lam-Hoai et a1 . Structural diversity and function of tintinnids and rotifers 23

tionships implied by correlations with mesozooplank- From the data obtained during 1994, the tintinnid ton found in this study (Table 2). and rotifer populations, of which neither the ecology Potential filtration may illustrate the trophic activity nor the life cycle has yet been studied in the Etang de of tintinnids and rotifers in the ecosystem. Taniguchi Thau, seem to be governed by environmental factors & Kawakami (1985) indicated tintinnid filtration rates (climatic as well as hydrological events). These are the of 0.4 to 14.5 p1 ind.-' h-'; and C. Rougier (pers. prevalent 'forcing' factors of the ecosystem which con- comm. 1995) compiled rates according to the size cat- trol the spatio-temporal repartition of the biomass of egories from the previous authors' d.ata and also from such taxocoenoses. A structural diversity results from Rassoulzadegan & Etienne (1981) and found a range this which is revealed by our data analysis. Moreover, of 0.1 to 3.5 p1 ind.-' h-' Rotifer filtration rates have the function of these 2 microzooplankton groups, in been estimated to be 0.1 to 4 p1 ind.-' h-' by Pont relation to the other zooplankton components, has (1995), 8.7 to 17.8 p1 ind.-' h-' by Dolan & Gallegos been pointed out in a lagoon system. (1991) and 2 to 18 p1 ind.-' h-' by Egloff (1988).These rates appear to be quite low compared to other micro- Acknowledgements. This study was supported by the zooplankton ones: 0.47 to 1.99 m1 ind.-' d-' for cope- PNOC/OXYTHAU program and conducted with the collabo- ration of IFREMER-University of Montpellier I1 URM5. The & pod nauplii grazing on phytoplankton (White authors thank CNRS-Un~versityof Montpell~erI1 UMR 5556 Roman 1992), 0.11 to 0.56 m1 ind.-' d-' for nauplii colleagues and technical staff for their valuable contributions. preying on ciliates (Dolan 1991), or 0.1 to 4.1 m1 ind.-' Meteorological data were provided by B. Bibent, and cytoflu- d-' for mollusk larvae feeding on diatoms and dinofla- orimeter data by C. Courties. The authors are also indebted to Dr M. Peuto-Moreau (Universite de Nice) and Dr R. Pourriot gellates (White & Roman 1992). As the average abun- (CNRS-Universlte de Paris VI) for identifying, respectively, dances in the Etang de Thau (throughout the sam- tint~nnidsand rotifers, and for their advice Many thanks to Dr pling periods and for all stations) were estimated to be A Vaquer for phytoplankton identificat~onand the aloricate 75700 ind. m-3 for the tintinnids and 3530 ind. m-3 for ollgotrlch density estimations. The manuscript was greatly the rotifers, these rates calculated at a potential filtra- improved by comments and suggestions of the reviewers. tion rate on the order of 10 1 d-' for the populations present in 1 m3 of water. 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This article was submitted to the editor Manuscript first received: June 27, 1996 Revised version accepted: April 7, 1997