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Peridinium sp. corresponded to the nanoplankton fraction, considering that they are smaller than 20 pm GALD. In relation with G. helveticum, it is important to.
Algological Studies 107

117-129

Stuttgart, November 2002

Summer population development and diurnal vertical distribution of dinoflagellates in an ultraoligotrophic Andean lake (Patagonia, Argentina) CLAUDIA QUEIMAL~OS, GONZALO PEREZ and BEATRIZ MODENUTTI Laboratorio de Limnologia, Centro Regional Universitario Bariloche, Universidad Nacional del Comahue, Bariloche, Argentina With 8 figures and 1 table in the text

Abstract: Diurnal vertical distribution of dinoflagellates in relation to environmental parameters was analysed in Lake Moreno Oeste (North Patagonia, Argentina) during a spring-summer period, when the lake was thermally stratified. Seven unarmored and armored dinoflagellates species were registered, including four species of Gymnodinium, which are reported for Argentina and South America for the first time. Four species belong to the net phytoplankton fraction, two others are nanoplanktic, while the last one is considered as a planktic protist since it is colourless. The two dominant species of the larger fraction, G. puradoxum and G. uberrimum, were recorded all along the water column, but they clearly preferred deep levels between 28 and 40 m depth which receive 1 % of surface PAR irradiance. In this way, these species are included in the deep chlorophyll maxima observed in this lake. On the contrary, the smallest species showed different vertical distribution patterns. Peridinium sp. developed its maximum abundances in the epilimnetic levels, while G. vuriuns was randomly distributed along the water column. Key words:

Dinoflagellates, diurnal vertical distribution, light climate, ultraoligotrophic lakes, Andean lakes.

Introduction Although dinoflagellates are important members of both marine and freshwater ecosystems, data about life history in relation to environmental parameters in this group are scarce (STOECKER 1999). Therefore, their role is poorly understood in lake ecosystem dynamics. In previous studies on plankton assemblages of South Andean lakes of Argentina (QUEIMALIROS et al. 1999, MODENUTTI et al. 2000) we pointed out that dinoflagellates are important components of the phytoplankton community in these lakes. The genera Gymnodinium, Peridinium and Ceratium have been previously and frequently reported in Andean lakes of Argentina 0342-1 123/02/0145-117$3.25 02002 E. Schweizerbart’scheVerlagsbuchhandlung, D-70 176 Stuttgart Algological Studies 107 = Arch. Hydrobiol. Suppl. 145

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(SECKT 1950, THOMASSON 1959, 1963, IZAGUIRRE et al. 1990, QUEIMAL~OS 1997, D f u et al. 1998) indicating that these lakes present favourable conditions for dinoflagellate development. Dinoflagellates have been found to be common constituents of the deep chlorophyll maximum at 75-150 m below the surface in nutrient-poor oceans (VAN DEN HOECK et al. 1998) and also in lakes (LINDHOLM 1992). These organisms are able to profit from the dim regions of the euphotic zone (POLLINGHER 1988). Considering that in Andean lakes deep chlorophyll maxima have been noticed (QUEI M A L ~ O Set al. 1999, MODENUTTI et al. 2000), dinoflagellates can also be expected as components of these deep maxima. On the other hand, dinoflagellates play different trophic roles in aquatic communities being primary producers, predators, herbivores or parasites (LOEBLICH 1984). In particular, mixotrophy, as a combination of both phototrophy and 1984, BOCKSTAHLER & phagotrophy, is widespread within the group (SPECTOR COATS 1993a, 1993b, JACOBSON & ANDERSON 1996, STOECKER 1999), and heterotrophy itself is well studied in marine dinoflagellates (HANSEN & CALADO 1999, JEONG 1999). Information on responses to light, dissolved inorganic and organic nutrients and prey quality and quantity for most dinoflagellate species is still unknown (STOECKER 1999). In the present study we attempt to analyse the diurnal vertical distribution of dinoflagellates in an ultraoligotrophic Andean lake in relation to environmental parameters. Study site Lake Moreno Oeste (41'5's; 71"33'W; 758 m a.s.1.) belongs to the Nahuel Huapi system (Patagonia, Argentina) (Fig. 1). The lake is of glacial origin, and has a surface area of 6 kmz and the maximum depth is 90 m. The regional climate is classified as temperate under the influence of westerly winds, with 1500 mm of annual precipitation and 8.7 "C of mean annual temperature. The thermal regime is warm monomictic with seasonal stratification from early spring to early fall (QUEIMAL~OS et al. 1999). Dissolved oxygen concentration remained at saturation levels all along the water column. During thermal stratification, oxygen vertical distribution describes an orthograde curve, typical of an unproductive lake. Lake chemistry and net phytoplankton have been partially described by IZAGUIRRE et al. (1990) indicating its ultraoligotrophic condition.

Material and methods A sampling point was established at the central part of the basin (z = 70 m). Sampling was carried out in 9 occasions, during Southern summer, between November 1998 and April 1999, always at mid-day, 1 h before astronomic noon. Temperature and light (Photosynthetically Active Radiation, PAR, 40&700 nm; W - B , 305 and 320 nm; UV-A, 340 and 380 nm) profiles from 0 to 52 m were measured with a P W 500B submersible radiometer (Biospherical Instruments). Extincton coefficients for each date were calculated by re-

Dinoflagellates in an ultraoligotrophic Andean lake (Patagonia, Argentina)

1 19

Fig. 1. Geographical location of Lake Moreno Oeste. The symbol (X) indicates the Sampling station site.

gressing log-transformed light with depth. In situ Chlorophyll a profiles (G52 m) were determined on the basis of the natural fluorescence measured with the PUV 500B ( P W 683). Concurrently, water samples of 12 litres were obtained by duplicates with a sampling bottle from 0 to 52 meters each 4 m intervals. The obtained water was transferred to 5 1 polypropylene containers, which were rinsed with the water sampled at the beginning of the collection. Containers were kept in darkness and carried immediately to the laboratory (half an hour after the collection). Water was tested for total phosphorus (TP) and total dissolved phosphorus (TDP) concentrations following APHA (1985). Dissolved organic carbon (DOC) was estimated by spectrophotometry through a regression model based on MORRIS et al. (1995). A volume of 250 ml of water of each depth was fixed with acid Lugol solution for phytoplankton quantification. In addition, live samples were taken and they were immediately carried to the laboratory. These samples were examined under a direct microscope OLYMPUS BX50 and images were digitalized with Image Pro Plus Program (Media Cybernetics). Individuals were measured using the same computer program. Measurements are indicated as an average with their calculated standard errors. Phytoplankton and dinoflagellatespecies abundances were quantified with an inverted technique (UTERM~HL 1958) and using 50 ml UTERmicroscope following the UTERM~HL MdHL chambers. The limit between nano and net phytoplankton was considered as 20 pm GALD (Greatest Axial Linear Dimension). At least 30 cells of each phytoplankton species were measured and cell biovolume was calculated by approximation to appropriate geometric figures. The identification of dinoflagellate species was accomplished following HUBER-PESTALOZZI (1968), BOURRELLY (1971) and POPOVSKT & PFIESTER (1990).

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Results Recorded dinoflagellates species (Fig. 2a and b) Gymnodinium helveticum PENARJJ The cells are 37.6 f 1.4 pm long and 23.7 f 1.2 pn wide, with 6462 pm3 in average. This dinoflagellatehas a typical drop-shaped cell. The cell is not flattened, and its surface presents a fine longitudinal striation. The episome is oval and smaller than the hyposome, which is conical in front of view and has the antapex sharp-pointed. At the apex there are frequently one or two small teeth-like projections, which can be absent in some specimens. The cingulum is wide and deeply incised; it is localized at the premedian part of the cell and describes a descending spiral. The sulcus is narrow and rather deep and is extended about 3/4 of the way into both the epi- and hyposome. The large nucleus is located below the cingulum, and was easily visible in almost all the alive specimens. Also, in the cytoplasm, food vacuoles have been observed on several occasions. Chloroplasts and stigma are absent. Number of cells observed 45. Remarks : This species is euplankter and has been found in oligohophic lakes of Europe and North America (HUBER-PESTALOZZI 1968, MUNAWAR et al. 1987, POPOVSK~ & PFIESTER 1990). This is the first record for Argentina and South America.

Gymnodiniumparadoxum SCHILLING (Fig. 3a and b) The cells are 35.6 f 0.7 pm long and 3 1.8 f 0.8 pm wide, and mean biovolume of 18227 pm3. The shape is oval in longitudinal section. The episome is slightly larger than the hyposome and both are convex. The cingulum is not very deep, and the sulcus is hardly recognised, extending to the hyposome reaching the antapex, but does not intrude into the episome. In the cytoplasm there are numerous and brownish chloroplasts radially arranged. A red eyespot situated below the longitudinal flagellum, was visible in almost all the specimens. The nucleus was not noticeable in the examined specimens, although it was clearly observed in cells stained with DAF’I (fluorochrome4’,6-diamidino-2-phenylindole)under an epifluorescent microscope. Number of cells observed: 54. Remarks : The species is euplankterand has been found in ponds and lakes of Europe (HUBER-PESTALOZZI 1968, POPOVSK? & PFIESTER 1990) and North America (AGBETI et al. 1997). This is the first record for Argentina and South America.

Gymnodinium uberrimum (ALLMAN) KOFOID et SWZY (Fig. 4a and b) The cells are 48.0 f 0.8 pn long and 46.6 f 0.7 pm wide, with 42 439 p n 3 ; oval shaped and slightly flattened dorso-ventrally.The episome has a bell-like shape, and is longer than the hyposome, which is wider than the first one. The antapex presents a typical form with a ventral sinus. The cingulum is wide and the sulcus is shallow and rather wide, extending nearly to the antapex and intruding quite into the episome. In the cytoplasm, numerous and yellow-brown chromatophores radially arranged can be easily observed. The eyespot situated just above the flagella insertion point is easily recognisable, however the nucleus was not observed in the studied specimens. However, the dinokaryon were noticed under

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3b n

Figs 2-5. Gymnodinium species recorded in Lake Moreno Oeste. 2 - Gymnodinium helveticum, 2a - dorsal view, 2b - ventral view, scale 20 p;Fig. 3 - G. paradoxum, 3a ventral view, 3b - antapical view, scale 20 pm; Fig. 4 - G. uberrimum, 4a - ventral view, 4b - lateral view, scale 20 pm; Fig. 5 - G. varians, in ventral view, scale 5 p.

epifluorescence like those of G. paradoxum. In some samples we were able to observe quiescence states, which presents a spherical-gelatinous cover. Number of cells observed: 32. Remarks: The species is euplankter and has been found in oligotrophic lakes of Europe and North America (HUBER-PESTALOZZI 1968, MUNAWAR et al. 1987, POPOVSK? & PFIESTER 1990). This is the first record for Argentina and South America.

Gymnodinium varians MASKELL (Fig. 5 ) The cells are small, 11.4 f 0.3 pm long and 9.7 f.0.4 pm wide, with 370 p m 3 of mean biovolume, and have an oval shape. The episome and the hyposome are rounded, and the former is slightly larger than the latter. The cingulum is wide and nearly equatorial. The sulcus is hardly recognised, and nearly reaches the antapex. Inside the cytoplasm there are four or five oval and parietal chromatophores, which have clearly been distinguished by autoflorescence using an epifluorescent microscope. A stigma is lacking. Number of cells observed: 27. Remarks: The species was previously reported in New Zealand, Java, Europe and 1968, MUNAWAR et al. 1987, POPOVSK? & PFIESTER North America (HUBER-PESTALOZZI 1990). This is the first record for Argentina and South America.

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Three other species were present in our samples: Peridinium willei HUITFELD-HAAS This species was extensively cited in Andean lakes (THOMASSON 1959, 1963). Our specimens were 44.5 f 2.5 pm long and 44.9 f 4.9 pn wide, with a mean biovolume of 50 025 p m 3 . Cerutium hirundinella (0.F. M.) DUJARDIN This species was also previously recorded in Andean lakes (THOMASSON 1963). Our specimens corresponded to the type silesiacum (following HUBER-PESTALOZZI 1968) and were 185.0 f 0.8 pm in length and 49.0 h 0.8 pn in width, with 34 62 1 pm3 in average. Peridinium sp. This is a small species (17.5 f 0.5 pn long and 15.1 f 0.5 pm wide, 2155 pm3 in average), which could not be identified with certainty. Our specimens are thinwalled with plates that are hardly recognisable.

Species vertical distribution During the study period the lake developed a direct stratification with a marked thermocline around 30 m depth, giving a broad mixing layer (Fig. 6a). Daily surface PAR irradiance varied slightly during the sampling season (Fig. 6a). Temperature ranged from 15 "C to 17 "C in the epilimnion and was of 7 "C in the hypolimnion (Fig. 6a). The obtained values of the diffuse extinction coefficient (Kd) were considerably low and fairly constant, varying between 0.121 and 0.154 m-1. Euphotic zone (1 % of surface PAR irradiance) was extended up to 38 m, including the whole mixing layer within it (Fig. 6a). UV-B radiation (305 and 320 nm) reached up to the 15 m depth whereas UV-A (340 and 380 nm) the 30 m depth except in November when reached 38 m depth (Fig. 6b). Phosphorus concentrations, both TP and TDP, were always very low with no remarkable differences along the water column (Table 1). Dissolved Organic Carbon (DOC) concentration was also low (0.61-0.63 mg 1-1) and no significant shifts were noted along the water column (Table 1). Vertical profiles of Chlorophyll a concentrations showed maximum values near the limit of the euphotic zone, just below the upper limit of the metalimnion (Table 1). Epilimnetic Chlorophyll a concentration was always less than 1 pg 1-1, while metalimnetic (36 m) maximum reached 2.61 pg 1-l (Table 1). The seven dinoflagellate species were recorded all along the sampling period. Four species (G. paradoxum, G. uberrimum, P. willei and C. hirundinella) belonged to the netphytoplankton fraction; meanwhile the species G. varians and Peridinium sp. corresponded to the nanoplankton fraction, considering that they are smaller than 20 pm GALD. In relation with G. helveticum, it is important to clarify that as it is a colourless species, we have considered it as a planktic protist,

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a

PAR lrradiance [pE m"sec-'] 1oE 1 [ r 1 8 1 o ? l 0 1 8 lo? 10418 lo? 1 0 1 8 lo? 1 0 1 8 102 1 0 1 8 1oz I@ 0

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-305nm

..........320nm

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Fig. 6. Light and temperature vertical distribution in Lake Moreno Oeste during the studied period. a - Photosynthetically Active Radiation (PAR)(400-700 nm) and temperature profiles; b - U V - B (305-320 nm) and UV-A (340-380 nm) radiation profiles.

Table 1. Total Dissolved Phosphorus (TDP), Total Phosphorus (TP), Dissolved Organic Carbon (DOC) and Chlorophyll a (Chl) concentrations in Lake Moreno Oeste during the studied period. Values are expressed as mean standard error, and Chl a, as minimum and maximum values.

*

Depth [m] 0

TDP [pg I-]]

TP [pg I-']

DOC [mg I-]]

Chl a [pg 1-l]

1.86 f 0.24

3.82 f 0.38

0.61 f 0.06

0.22-0.55

4

1.86 f 0.24

3.82 f 0.38

0.61 f 0.06

0.38-0.60

16

2.05 f0.24

3.76 f 0.25

0.62 f 0.05

0.38-0.81

28

1.90f 0.3 1

3.50 f 0.25

0.63 f 0.06

0.45-1.45

36

1.75 0.23

*

3.42 f 0.44

0.62 f 0.05

0.56-2.61

44

1.70 f 0.29

3.07 f 0.39

0.63 f 0.07

0.54-1.34

52

1.55 f0.30

2.86 f 0.27

0.63 0.06

*

0.66-1.29

Dinoflagellates in an ultraoligotrophic Andean lake (Patagonia, Argentina)

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G helveficum

Fig. 8. Specific abundances and vertical distribution of five dinoflagellatespecies in Lake Moreno Oeste during the studied period. a - Nanoplanktic dinoflagellates;b - Net phytoplanktic dinoflagellates.

On the other hand, the small Peridinium sp. preferred the epilimnetic levels during the summer months (Fig. 8a). Both G. paradoxum and G. uberrimum showed the same pattern during the studied period, since they were recorded all along the water column (0 to 52 m), with maximum densities between 28 m and 40 m depth (Fig. 8b). On the contrary, G. helveticum was present only in intermediate levels (12 to 40 m depth) (Fig. 8b). The largest thecate species, P. willei and C. hirundinella were very scarce with densities lower than 0.5 cells per ml, therefore it was not worthy to present them in a graph. In relation with the trophic roles that these species would exert, at present we are able to affirm that G. varians is bacterivorous, since it has been recently (2002), and that evidently the colourless G. helvetiestablished by QUEIMAL~OS cum is a heterotrophic species. Regarding the other species, the literature provides scarce information about the presence of phagotrophy in the genus Peridinium (SPECTOR 1984, HANSEN & CALADO 1999), and establishes the predatory behaviour in Ceratium hirundinella (HOFENEDER 1930), but this report has

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& CALADO 1999, STOECKER 1999). been either in doubt or withdrawn (HANSEN Moreover, it emerges that there are no available data yet about the possible mixotrophic condition of the species G. paradoxum and G. uberrimum (JEONG 1999, STOECKER 1999).

Discussion Considering that Lake Moreno Oeste is well oxygenated and a high light-low nutrient environment (Table 1, Fig. 6), it can be considered as an ultraoligotrophic system. In this scenario, dinoflagellates may be favoured since most species prefer well-oxygenated waters and tend to avoid more eutrophic systems that experience periodic oxygen depletion (POLLMGHER 1988). The recorded species corresponded to assemblages reported in other oligotrophic environments (MUNAWAR et al. 1987, POPOVSK? & PFIESTER 1990, NYGAARD 1996). Light is not a limiting factor in Lake Moreno Oeste (Fig. 6a), but W - B radiation is potentially hazardous (KARENTZ et al. 1994) since it reached up to 15 m depth (Fig. 6b). The upper levels of the water column were always avoided during our daytime study by the larger Gymnodinium species, which clearly preferred the level with 1 % of PAR surface irradiance (Fig. 8b). In other lakes it has been noticed that species of Gymnodinium developed near the bottom of the euphotic zone in a layer about 1 % of full daylight (MITCHELL & GALLAND 1981, LINDHOLM 1992). This situation closely resembles that of Lake Moreno Oeste where maximum densities received at noon an irradiance of 3.65 to 10 pE.m-2.s-1 of PAR (Fig. 6a). Phototrophic bacteria, other phytoplankton species and mixotrophic et al. 1999, MODENUTTI et al. ciliates preferred also this position (QUEIMAL~~OS 2000), indicating that in this lake, during daytime, the deep levels are favourable for phototrophy. On the other hand, the nanoplanktic species Peridinium sp. was observed in the epilimnetic levels and G. varians showed a no clear depth preference (Fig. 8a). Therefore, these species may have a stronger resistance to U V radiation considering that they were able to develop at 0 to 15 m depth influenced by UV-B (Fig. 6b). et al. (1999) indicated that Chlorophyll In Lake Moreno Oeste, QUEIMAL~OS a concentration was related to the biovolume ofthe different photosynthetic fractions (net and nano phytoplankton and endosymbiotic Chlorella of the ciliate Ophydium naumanni PEJLER).Symbiotic Chlorella biovolume was found to account for the highest explained variance and to be directly related to Chl a conet al. 1999). Nevertheless, net phytoplankton biovolume centration (QUEIMAL~OS et al. 1999). In this fracincreased in 4 % the explained variance (QLIEIMAL~OS tion, G. paraduxum plays an important role, particularly in terms of biovolume. Therefore, this species is also an important constituent of the plankton that causes the deep chlorophyll maxima in Lake Moreno Oeste.

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In addition, dinoflagellates are also favoured in oligotrophic environments due to their feeding mode and their movement capacity, since they can screen the whole water column for nutrients through vertical migration (POLLINGHER 1988). Many planktic dinoflagellates in natural environments depend on the ingestion of particulate material (LOEBLICH 1984, HANSEN& CALADO 1999), therefore mixotrophy, which combines phototrophy and heterotrophy, is a widespread feeding mode among them. Dinoflagellates have been reported to be capable to 199 1) and relatively larger sized particles including ingest cyanobacteria (STROM 1984, BOCKalgae, ciliates, copepod eggs and other dinoflagellates (SPECTOR STAHLER & COATS 1993a, 1993b, JACOBSON & ANDERSON 1996, HAVSKUM & HANSEN 1997, JEONG 1999, STOECKER 1999). Consequently, the distribution of the recorded species in Lake Moreno Oeste can also be related with cyanobacteria, phytoplankton and ciliate abundances. In our study, it is clear that all planktic organisms showed the same depth preference during daytime, however further experimental studies are necessary to understand the physiological and ecological roles that dinoflagellates play in ultraoligotrophic lakes.

Summary In this study we analysed the diurnal vertical distribution of dinoflagellates in an ultraoligotrophic Andean lake in relation to environmental parameters. The study was carried out in Lake Moreno Oeste, an ultraoligotrophic deep lake located in the Andean region of North Patagonia (Argentina) (Fig. 1). The sampling was performed in 9 occasions during a spring-summer season (November 1998 to April 1999), when the lake was thermally stratified. In each sampling date temperature, light and in situ chlorophyll a profiles for 0 to 52 m were measured with a PUV 500B submersible radiometer (Biospherical Instruments). At the same time, duplicate water samples of 12 litres were obtained with a Sampling bottle from 0 to 52 meters each 4 m intervals, for phytoplankton quantification and nutrient determination. Seven unarmored and armored dinoflagellatesspecies were registered, including four species of Gymnodinium, which are reported for Argentina and South America for the first time (Figs 2-5). Four species belong to the net phytoplankton fraction (Gymnodinium paradoxum, G. ubem'mum, Peridinium willei and Ceratium hirundinella), and the other two are nanoplanktic species (G. varians and Peridinium sp.). G. helveticum is considered as a planktic protist since it is colourless. The two dominant species of the larger fraction, G. paradoxum and G. ubem'mum, were recorded all along the water column, but they clearly preferred deep levels between 28 and 40 m depth which receive 1 YOof surface PAR irradiance (Fig. 6a). Consequently, these species are included in the deep chlorophyll maxima previously observed in this lake (QUEIMALIROS et al. 1999). On the contrary, the nanoplanktic speciesPeridinium sp. was observed in the epilimnetic levels and G. varians showed a no clear depth preference (Fig. 8a). Therefore, these species may have a stronger resistance to UV radiation considering that they were able to develop at 0 to 15 m depth influenced by UV-B (Fig. 6b). Dinoflagellates might be also favoured in this ultraoligotrophic environment due to their combining feeding mode that includes phototrophy and heterotrophy, and their movement capacity that allow them to screen the whole water column for nutrients.

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Acknowledgements This work was supported by Grants provided by the CONICET PIP 0739/98 and FONCyT PICT 01-6035. GONZALO PBREZis funded by a CONICET fellowship, and CLAUDIA QUEIMAL~JOSand BEATRLZ MODENUTTI are CONICET researchers.

References AGBETI, M. D.; KINGSTON, J. C.; SMOL, J. P. & WATTERS, C. (1997): Comparison of phytoplankton succession in two lakes of different mixing regimes. -Arch. Hydrobiol. 140: 37-69. APHA (1985): Standard methods for the examination of water, sewage, and wastewater, 16th Ed. - 1 134 pp. American Public Health Association, Washington, D. C. BOCKSTAHLER, K. R. & COATS, D. W. (1993a): Grazing of the mixotrophic Gymnodinium sanguineum on ciliate populations of Chesapeake Bay. -Mar. Biol. 116: 477-487. - 1993b): Spatial and temporal aspects of mixotrophy in Cheasapeake Bay dinoflagellates.- J. Eur. Microbiol. 40: 49-60. BOURRELLY, P. (1970): Les algues d’eau douce. Tome 111: Les-alguesbleues et rouges, les EuglCniens, Pkridiniens et Cryptomonadines. - 512 pp., Editions N. BoubCe & Cie., Paris. D t u , M. M.; PEDROZO, F. L. & TEMPORETTI,P. F. (1998): Phytoplankton of two Araucanian lakes of different trophic status. - Hydrobiologia 369/370: 45-57. HANSEN, P. J. & CALADO, A. J. (1999): Phagotrophic mechanisms and prey selection in free-living dinoflagellates. - J. Eukariot. Microbiol. 46: 382-389. HAVSKUM, H. & HANSEN, A. S. (1997): Importance of pigmented and colourless nanosized protists as grazers on nanoplankton in a phosphate-depleted Norwegian fjord and in enclosures. - Aquat,.Microb. Ecol. 12: 139-151. HOFENEDER, H. (1930): Uber die animalische Ernahrung von Ceratium hirundinella 0. F. MOLLERund iiber die Rolle des Kernes bei der Zellfunktion. - Arch. Protistenkd. 71: 1-32. HUBER-PESTALOZZI, G. (1968): Cryptophyceae, Chloromonadophyceae, Dinophyceae. Das Phytoplankton des Siil3wassers, 3. Teil, 2. Auflage - 322 pp., E. Schweizerbart’sche Verlagsbuchhandlung, Stuttgart. IZAGUIRRE, I.; DEL GIORGIO, P.; O’FARRELL, I. & TELL, G. (1990): Classificacion de 20 cuerpos de agua andino-pataghicos (Argentina) en base a la estructura del fitoplancton estival. - Cryptogamie, Algologie 11: 31-46. JACOBSON, D. M. & ANDERSON, D. M. (1996): Widespread phagocytosis of ciliates and other protists by marine mixotrophic and heterotrophic thecate dinoflagellates. - J. PhyCOI. 32: 279-285. JEONG, H. J. (1999): The ecological roles of heterotrophic dinoflagellates in marine planktonic communitiy. - Eukaryot. Microbiol. 46: 390-396. KARENTZ, D; BOTHWELL, M. L.; COFFIN, R. B.; HANSON, A.; HERNDL, G. J.; KILHAM, S. S.; LESSER, M. P.; LINDELL, M.; MOELLER, R. E.; MORRIS, D. P.; NEALE, P. J.; SANDERS, R. W.; WEILER, C. S. & WETZEL, R. G. (1994): Impact of UV-B radiation on pelagic freshwater ecosystems: Report of working group on bacteria and phytoplankton. - Arch. Hydrobiol. BeihJErgebn. Limnol. 43: 3 1-69. LINDHOLM, T. (1992): Ecological role of depth maxima of phytoplankton. - Arch. Hydrobiol. 35: 35-45. LOEBLICH, A. R. 111. (1984): Dinoflagellate physiology and biochemistry. - In: SPECTOR, D. L. (ed.): Dinoflagellates, p. 299-342, Academic Press Inc., New York. A. N. (1981): Phytoplankton photosynthesis, eutrophication MITCHELL, S. F. & GALLAND, and vertical migration of dinoflagellatesin a New Zealand reservoir. - Verh. Internat. Verein. Limnol. 21: 1017-1020.

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