original scientific paper UD C 593.17(450 Beneška laguna)"!995" FIRST CONTRIBUTION T O THE KNOWLEDGE OF MiCROBENTHIC PROTISTS FROM THE VENICE LAGOO N Olimpia COPPELLOm Department of Biology, University of Padova, IT-35131 Padova, Via G. Colombo 3 E mail: Otimpiak@civ.bio.ursipd.it Roberta USINO Department of Biology, University of Padova, IT-35131 Padova, Via C. Colombo 3 Ester PiCCINNI Department of Biology, University of Padova, IT-35131 Padova, Via G. Colombo 3 E mail: Piccinni@civ.bio.ynipd.it ABSTRACT The importance of protists, especially dilates, in marine communities has been stressed by many authors; since these organisms feed at various trophic levels, e.g., bacteria, algae of various sizes, and other ciiiates. The protists living in the Lagoon of Venice have been poorly studied, it seemed particularly interesting to investi­gate their populations in this environment, the hydrological dynamics of which have been seriously modified and which is continuously subjected to large-scale anthropic modifications and polluted by waste from several different sources. This paper presents preliminary data on microbenthic protists in sediment samples collected in May and Septem­ber 1995 from six stations of the Venice Lagoon. Twenty-one genera of ciiiates were found. The highest concentra­tion recorded in station 1, also characterized by the highest concentration of fine sand, was about 100 cells, mh •. whereas that of flagellates was about 1000 cells, ml'1, with a lower number oftaxa in all stations sampled. Key words: microbenthos, Protists, Ciiiates, Flagellates, Venice Lagoon INTRODUCTIO N Since the earlier part of this century it has been rec­ognized that protists form a diversified quota of the biota living within marine benthic habitats. Most work has been concentrated on ciliated protozoa, which ap­peared to be dominant consumers in some benthic habitats (Kahf, 1930-35; Czapik & Fyda, 1992; Dra­gesco, 1963a, b; Epstein et ah, 1992; Faure-Fremiet, 1950; Fenchel 1967, 1968, 1969, 1987; Hartwig, 1980a, b) and in recent years also on other protists, such as heterotrophic flagellates, ali involved in microbial food webs (Fenchel, 1986; Patterson et al„ 1989). Sedi­ment particle size influences the organic content of sediments, water and oxygen penetration, oxygen con­tent, and accessibility by protists or metazoan competi­tors, and granulometric characteristics have a marked effect on the composition of protist biota. Microbenthic organisms include sessile and vagile unicellular eu­karyotic species living on the surface of, or within, sediments; in the former case, the organisms are defined as components of the microbiotecton or epipsammon, in the second as mesopsammon. Many protists cannot be included exclusively in either class (Patterson et al, 1989). Admittedly, many difficulties are encountered when examining microbenthic commmunities, e.g. species de­termination, collection of qualitative and quantitative data, and the almost complete uselessness of analysing fixed samples (Finlay & Guhl, 1992). As already mentioned, the protists living in the La­goon of Venice have been poorly studied: very old data 231 Otimpia COPPELLOTT 1 etal. \ FIRST CONTRIBUTIO N T O KNOWLEDG E O F ..., 231-240 are available in the literature (Klesselbach, 1936} to­gether with some recent data on a new Euplotes mor­phospecies, L margherensis (Coppellotti & Cisotto, 1996), which has greater resistance to copper than other species of Euplotes (Coppetlotti & De Gabrieli, 1995). The Lagoon of Venice is a unique ecosystem which originated nearly 6000 years ago and now consists of a semi-enclosed body of water connected with the Adriatic Sea through three channels (Bendortcchio et a!., 1993). The hydrologica! dynamics of this environment have been modified by various anthropic activities. The Lagoon receives wastes from various sources, all of which are very numerous and complex, such as dis­charges of treated and untreated domestic sewage, treated industrial effluent, and cooling water from the industrial zone, and also pollutants, such as heavy met­als, transported down the waterways flowing into the Lagoon. Particular attention was paid to sediments, be­cause it is well known that heavy metals and organic micropoliutants are closely associated with this fraction, from which they may be resuspended (Donazzolo eta!., 1984; Martin et a!,, 1994). For all these reasons, this area may be highly selective. Some other types of organ­isms, such as macroalgae, have been used as biological indicators for the Lagoon of Venice (Favero et. al., 1996). It seems particularly interesting to investigate protist populations in this peculiar environment, which is con­tinuously subjected to large-scale anthropic modifica­tions. The studied organisms belonged to the taxonomic group of Ciliophora and to the flagellate group, a het­erogeneous assemblage of protists equipped with fia­gella. MATERIALS AND METHODS Samples were taken from the sediments of six sta­tions in the Venice Lagoon, chosen for their different environmental characteristics (Fig. 1). Station 1 was lo­cated near the hydrobiological station of Chioggia, sub­ject to pollution by urban waste; stations 2 and 3 were located at mussel-farming sites; station 4 was in an area polluted by industrial waste; station 5 lay between the industrial zone of Marghera and the city of Venice, and is polluted by both industrial and city waste; and station 6 was located in a "clean" site in the northern part of the Lagoon. Samples were collected in May 1995 from all sta­tions and in September 1995 from station 1 only. Sampling was carried out by pressing a plexiglass tube 3.2 cm in diameter some 10 cm into the sediment and that part of sediment from 0 cm to 2 cm below the surface was collected. Samples thus consisted of 16 mi each, and were placed in plastic 500-ml bottles. A minimum of three samplings was made for each station. 100 ml of seawater, filtered through 0,22 pm Sterivex-GS mesh (Millipore) and having the same salinity as that of the collection site, were added to the sediment sam­ples. Samples were taken to the laboratory in a refriger­ated container and were observed within 6 hours. Three procedures were adopted for examination of samples: 1) Uhlig's "seawater ice" method (Uhiig, 1964) for extracting interstitial microfauna: sediments were filtered through nylon nets (200, 100, 60 and 45 !.!m meshes). Fig. 1: Lagoon of Venice and location of sampling stations. Si. 1: Beneška laguna in lokacija vzorčnih postaj. Ofimpia COPPELIOTT I e! ai: FIRST CONTRIBUTIO N T O KNOWLEDG E O f .... 235-240 This method was only used for sediments composed of relatively iarge sand particles with iow percentages of silt and clay, which are washed through with the proto­zoa. 2) Three sub-sampies were prepared by withdrawing 10 ml of diluted sediment and adding 90 ml of filtered seawater. Ciliates and flagellates were counted in five 100-pl drops for each sub-sample under a Leitz Diaplan microscope at magnifications of 310x or 500x, following the indications of Finlay & Guhl (1992). 3) Six sub-samples were prepared from each bottle by withdrawing 5 ml, to which 45 ml of seawater were added. Quantitative observations and initial identifica­tion of ciliates were carried out on every sub-sample under a Wild M8 stereomicroscope. Living ciliates were removed by a Pasteur pipette and directly counted. The data on protozoan densities reported in this work were obtained using method 2 for flagellates and method 3 for ciliates, after washing of all sediments by Uhlig's "seawater ice" method where possible. In most cases, quantitative data refer to genera more than to species, due to the difficulty in collecting simul­taneously both qualitative and quantitative data on cili­ates. Impregnation by protargoi or silver nitrate was used for correct identification of most ciliates, following re­spectively Wilbert or Chatton-Lwoff procedures as modified by Foissner (1991). Some particularly fragile ciliates, such as those belonging to Kinetofragminopho­rea, were fixed before impregnation with Raikov's (1978) fluid, normally used in electron microscopy. Drawings of protargoi-impregnated specimens were made with the aid of a camera lucida under a Diaplan Leitz microscope. The taxonomic scheme by Levine et a!. (1980) was used. Species descriptions by Kahl (1930­1935), Curds (1975), Curds & Wu (1983), Dragesco (1963a, b), and Carey (1992) were also used. Flagellates were identified with the aid of Prescott's (1962) and Schiller's (1933-1937) descriptions. Grain-size fractions (pni) i 2 1000-500 0.38 3.07 500-250 34.82 12.11 9739 * 58.73* 250-125 54.61 26.58 125-63 7.58 16,96 63-15.6 0.65 14.71 1.24* 25.28* 15.6-3.9 0.59 10.57 Salinity values were determined with a refractome­ter. Samples were analysed for organic matter content and for grain-size composition according to Buchanan (1984). RESULTS AND DISCUSSION Abiotic data In May 1995 salinity was at a minimum value of 28%n at station 1 and peaked at 35 %o at station 5. A value of 30 %o was measured at all other stations. In September 1995, salinity was 35%« at station 1. Water temperatures were respectively 16°C and 21 °C at alt stations. Table 1 lists data referring to the May samplings. The sediments were characterized by compositions of differ­ing percentages: the highest sand content was recovered at station 1 (97.39%) and the lowest at station 6 (14.92%). The highest contents of fine sand (250-125 pm) were measured at station 1 (54.61 %) and of median sand (500-250 !.tm) at station 4 (49.49%). Very high contents of silt were found at stations 6 (68.39%) and 5 (49.55%). Very little organic matter was present at sta­tions 1 (0.26%) and 4 (0.22%). <3.9 1.37 15.99 Organic matter 0.26 3.13 Stations 3 4 5 6 1.90 10.73 13.57 0.49 13.40 49.49 7.24 0.57 S 63.72* 94.74* 45,00* 14.92* A 32.31 28.93 4,95 1.55 N 16.11 5.58 19.24 12.30 D S 18.81 2.19 27.50 42.54 1 26.58* 3.40* 49.55" 68,39* L 7.77 1.21 22.05 25,85 T C L 9.70 1.86 5.45 16.70 A Y 0.72 0.22 2.13 1.64 Tab. 1: Grain-size percentage distribution and organic matter content of sediments examined in may 1995. * Totai percentage values refer to sand and silt, respectively. Data kindly supplied by Prof. R. Brunetti. Tab. 1: Porazdelitev zrnavosti (v odstotkih) in vsebnost organske snovi v sedimentu, raziskanem v maju 1995 (v %). * Skupne odstotkovne vrednosti se nanašajo na pesek in mulj. Podatki s prijaznim dovoljenjem prof. R. Brunettija. Microfauna Taxa found in the May samplings in a(l 6 stations are listed in Table 2. With our counting procedures, flagel­lates were the most numerous protists (approximately 1000 celts, ml-1), although higher numbers of ciliate taxa were recorded at almost all stations. The highest number was recorded at station 1, where ciliates Sampling síations Taxa 1 2 3 4 5 6 Flagellates Amphidinium sp. +++ + Gymnodínium sp. + + Techadinium sp. ++ + Oxyrrhis sp. ++ + Anisonema sp. 4.4.4. + + ++ + + Chlorogonium sp. + + + + + ++ + + + •i-+ Bodo spp. + + + + 4-++++ +++ Otber species + + ++ + + + + Ciliates Kirietofrasminophorea Lacrymaria sp. + + + Mesodinium pulex + -t-+ Litonotus sp. + + Trachelocerca schuitzei + Trachelocerca sp. + Tracheloraphis sp. + Remane!la spp. + + + Geleia sp. + Conc/icwfoma longissimum + Colpoda cucullas + OI !gohy menophorea Frontonia sp. + + + + Uronema sp. + + Pleuronema coronatum + + + + + Cyclidium sp. + + + + Polyhymenophorea Conrlylostoma remanei + Slrombidium spp. + + + + + + + Tintinnopsis sp. + Holosticha spp. + Aspidisca lepiaspis + + Aspidisca sedigila + + Aspidisca spp. +++ + + + Üiophrys appendiculata + + Euplotes bisulcatus + Euplotes rariseta + + Euplotes vannus + ++ Uronychia transfuga + belonging to Kinetofragminophorea were represented by 9 genera, Polybymenophorea by 6, and Oligohy­menophorea by 4. The most frequent genera were Re­manella, Strombidium and Aspidisca. Remanella is common in fine marine sand, its diet comprising dia­toms and flagellates. Strombidium is generally found in the oxidized zone, where it feeds on diatoms and small phytoflagellates. Taxa Flagellates Amphidinium sp. Gymnodinium sp. Techadinium sp. Oxyrrhis sp. Anisonema sp. Chlorogonium sp. Bodo spp. Other species Ciliates Kinetofragminophorea Lacrymaria sp. Dileptus sp. Mcsodtnium pulex Litonotus sp. Trachelocerca binudeata Trachelocerca schuitzei Trachelocerca sp. Trachelonema minima Tracheloraphis sp. Remanella spp. Get eta sp. Conchostoma longissimum Cotpoda cucullus OI i go h y m enop ho rea Frontonia sp. Uronema sp. Pleuronema coronatum Cyclidium sp. Po i y hy m e nophorea Condylostoma remanei Strombidium spp. Holosticha spp. Aspidisca leptaspis Aspidisca sedigita Aspidisca spp. Diophrys appendicuhta Euplotes bisulcatus Eupiotes rariseta Euplotes vannus May + + ++ + ++ + + + +++ + + + + + + + + + + + + + + + ++ + + + + + + ++ + + •i­ + + + September + + + + •f -f + + ++ + + + + + + + + + + + ++ + -Í­ + + + + + + + + +,(<5 CELLS mi-'); ++, (5-15 CELLS mM); +++, 15-500 CELLSml-1); ++++, (>100 CELLS mH). +,(<5 CELLS i«H); ++, (5-15 CEI.iS mH); +++, 15-100 CELLS ml"1): ++++. (>100 CELLS ML"1). Tab. 2: List of taxa in samplings of May 1995. Tab. 2: Seznam taksonov v vzorcib iz maja 1995. Tab. 3: List of taxa in samplings of station 1 in May and September 1995. Tab. 3: Seznam taksonov v vzorcib s postaje 1 iz maja in septembra 1995. Olim p rs COPPEU.OTT I et al.: FIRST CONTRIBUTIO N T O KNOWLEDG E O F ...,231-240 30 •Flagellate s 0Cilia!e s 20 L ZI 10 3 4 Sampling stations Fig. 2: Number of taxa of Ciliates and Flagellates in six sampling stations of Venice Lagoon in May 1995. SI. 2: Število taksonov migetalkarjcv in bičkarjev na šestih vzorčnih postajah v Beneški laguni maja 1995. Ciliate density was very low at the other stations, Oligohymenophorea and Polyhymenophorea being the main groups.The lowest number of genera was found at station 4, i. e. 3 genera, whereas 9 were recorded at sta­ tion 3. Strombidium and Pleuronema were the most fre­ quently observed genera at all stations. As regards flagellates, Anisonema, ChSorogonium and Bodocould be observed at almost all stations, while Dinoflagellates such as Ampbidinium, Cymnodinium, Techadinium and Oxyrrbis were identified only at sta­tion 1, where the most numerous genera were the bac­terivorous Bodo and the phagotrophic Ampbidinium. It -must be noted that diatoms were very abundant in samples from all stations. The richness of taxa In the May samplings at all sta­ tions is reported in Fig. 2. The highest numbers of both flagellate and ciliate taxa are clearly present at station 1. In particular, ciliate taxa numbered 24, and at all sta­ tions 26. On the basis of the data obtained, it was decided to take samples only from station 1 in September 1995. The taxa of this station in May and September are listed in Table 3. Flagellate density was seen to have de­ creased, mainly because of the disappearance of Din­ oflagellates from the September samplings. A remark­ able increase in the density of some Karyorelictida, such as the predators Tracbelocerca and Tracbeiorapbis, was also noted. Indeed, Tracbelocerca was found to be rep­ resented by at least three species. Tracbeionema also appeared at station 1 in the September sampling. Direct counts of ciliates in the September samplings yielded the following data: about 70 cells. m H of Ki­ netofragminophorea, especially Karyorelictida; 20 cells. m h ' of Oligohymenophorea, especially Pleuronema coronatum; and about 1 5 cells, ml-1 of Polyhymeno­phorea, without any dominant genus. The morphologi­cal traits of some ciliate species after protargol impreg­nation are shown in Figs. 3, 4 and 5. These preliminary data indicate that the studied sta­tions of the Lagoon of Venice are characterized by rela­tively low densities of ciliates. It is well known that ciliates are most frequent in fine sand (250-125 pm). In finer sand (125-63 jjm) their numbers decrease drastically, and in coarser sands {500­250 !jrn) they also occur in smaller numbers (Fenchei,1969). Larger amounts of organic matter lead to a strongly reducing environment. The richness of sta­tion 1 with respect to the other stations may be ex­plained by the composition of its sediments (see Table 1) and by the amount of organic matter. In fact, the highest percentage (54.61%) of fine sand was found at this station. As regards organic matter, a value of 0.26% was recorded at station 1 and a similarly low value (0.22%) at station 4. However, station 4 was located in the industrial zone of the Lagoon, which is known to be highly polluted by heavy metals (Donazzolo et al., 1984; Basu & Molinaroli, 1994) which may thus strongly limit the biological characteristics of the envi­ronment and lead to the creation of a highly selective area for microfauna. ACKNOWLEDGEMENTS Financial support was provided by MURST, Project "Sistema Lagunare Veneziano". The authors are grateful to Prof. Riccardo Brunetti for abiotic analysis of sediments. Olimpia COp'f RLOTTI cl al.: FIRST CONTRIBUTION TO KNOWLEDGE OF .... 231-240 Fig. 3: Camera lucida drawings of protargol-impregnated ciliates, A: Lacrymaria sp,, 700x; B: Trachelocerca schultzei, 450x; C: Trachelocerca binucleata, 450x; D: Condylostoma remanei, 290x; E: Euplotes bisuicatus, ventral view, 1 lOOx; F: Euplotes bisuicatus, dorsal view, 1100x. Si. 3: Risbe migetaikarjev (napravljene ob pomoči tako imenovane camera lucida), prepojenih s protargolom. A: Lacrymaria sp., 700x; B: Trachelocerca schultzei, 450x; C: Trachelocerca binucleata, 450x; D: Condylostoma remanei, 290x; E: Euplotes bisuicatus, pogled s trebušne strani, 1100x; F: Euplotes bisuicatus, pogled s hrbtne strani, 1100x. Olimpia COPPELLOTTl el al.: EiftST CONTRIBUTION TO KNOWLEDGE OF 231-240 Fig 4: Micrographs of protargol-impregnated specimens. A: Trachelocerca binudeata, anterior part of cellular body, 960x; B: Trachelocerca binudeata, nuclear apparatus, 1280x; O Trachelocerca schultzei, nuclear apparatus, 1280x. SI. 4: Mikrografiprimerkov, prepojenih s protargolom. A: Trachelocerca binudeata, prednja stran celičnega telesa, 960x; B: Trachelocerca binudeata, jedrni aparat, 1280x; C Trachelocerca schultzei, jedrni aparat, 1280x. 237 Olimpis COPPELIOITI et si.: BRST CONTRIBUTION TO KNOWLEDGE OF 231 -2-10 Fig. 5; Micrographs of protargol-impregnated specimens. A: Pleuronema coronatum, ventral view, 1120x; B: Uronychia transfuga, dorsal view, 1280x; C: Aspidisca sedigita, ventral view, 1280x; D: Diophrys appendicuiata, ventral view, 1280x; L: Eupiotes vannus, ventral view, 960x. Si 5: Mikrografiprimerkov, prepojenih s protargolom. A: Pleuronema coronatum, pogled s trebušne strani, 1120x; B: Uronychia transfuga, pogled s hrbtne strani, 1280x; C: Aspidisca sedigita, pogled s trebušne strani, 1280x; D: Diophrys appendiculata, pogled s trebušne strani, 1280x; E: Euplotes vannus, pogled s trebušne strani, 960x. Oiimpi a COPPEU.OTT i etal. : FIRST CONTRIBUTIO N T O KNOWLEDG E O F ..., 23T-240 PRV I PRISPEVE K K POZNAVANJ U MiKROBENTOŠKI H ENOCELIČARJE V V BENEŠKi LAGUNI Oiimpia COPPELLOTTI Department of Biology, University of Padova, if-35131 Padova, Via G. Colombo i E mail: Olimpiak@civ.bio.unipd.it Roberta USINO Department of Biology, University of Padova, ST-35131 Padova, Via G. Colombo 3 Ester PiCCINNi Department of Biology, University of Padova, 1T-35131 Padova, Via G. Colombo 3 E mail: Piccinni@civ.bio.unipd.it POVZETEK Na pomen enoceličarjev, posebno migetalkarjev, v morskih združbah so opozorili že mnogi avtorji, saj se ti organizmi branijo na več trofičnih ravneh, npr. z bakterijami, algami različnih velikosti in drugimi migetalkarji. Enoceličarji, ki živijo v Beneški laguni, so slabo preučeni, zato se nam je zdelo še posebno zanimivo raziskati njihove populacije v tem okolju, katerega hidrološka dinamika se je do danes že temeljito spremenila. Nenehno je namreč izpostavljena velikim antropogenim vplivom in onesnaževanju z odpadki iz več različnih virov. Pričujoči Članek predstavlja preliminarne podatke o mikrobentoških enoceličarjih v vzorcih sedimenta, zbranih v maju in septembru 1995 na šestih postajah v Beneški laguni. Ugotovljenih je bilo 21 rodov migetalkarjev. Njihova največja koncentracija, ki je bila zabeležena na postaji 1 in katere značilnost je tudi največji delež mivke, je bila približno 100 celic, ml"1, največja koncentracija bičkarjevpa okrog 1000 celic, ml"l z manjšim številom taksonov na vseh vzorčnih postajah. Ključne besede: mtkrobentos, enoceličarji, migetalkarji, bičkarji, Beneška laguna REFERENCES Curds, C.R. 1975. A guide to the species of the genus Euplotes (Hypotrichida, Ciliatea). Bull. Br. Mus. nat. Basu, A.f & Moiinarolf, E. 1994, Toxic metals in Venice Hist. (Zool.), 28: 1-61. Lagoon sediments: model, observation and possible re-Curds, C.R. & Wu, I. C.H. 1983. A review of the Euplo­moval. Environ Geol., 24: 203-216. tidae (Hypotrichida, Ciliophora). Bull. Br. Mus. nat. Hist. Bendoricchio, G., Di Luzio, M., Baschieri, P., & Capo-(Zool.), 44: 191-247. dagtio, A.G, 1993. Diffuse pollution in the Lagoon of Czapik, A. & Fyda, J. 1992. Contribution a la con-Venice. Wat. Sei. 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