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Offprint Botanica Marina Vol. 39, 1996, pp. 103-115 © 1996 by Walter de Gruyter • Berlin ■ New York

The Diatom GenusThalassiosira (Bacillariophyta) in the Estuaries of the Schelde (Belgium/The Netherlands) and the Elbe (Germany)

K. Muylaert* and K. Sabbe

Department of Morphology, Systematics and Ecology, Botanical Laboratory, University of Gent, K. L. Ledeganckstraat 35, B-9000 Gent, Belgium * Corresponding author

A taxonomic and ecological study of the phytoplankton of the estuaries of the Schelde (Belgium/The Nether­ lands) and the Elbe (Germany) revealed the presence of numerous species belonging to the diatom genus Thalassiosira. Its representatives were a dominant component of the phytoplankton spring bloom in these estuaries. A total of 13 species were identified. All of these were present in the Schelde, while only 10 were found in the Elbe. Seven and five species respectively had previously not been reported from the Schelde and Elbe. A detailed light and electron microscopical description of these species is given. Most species had their distributional optimum in the polyhaline reaches of the estuaries. Community struc­ ture in these reaches was different from the one in the euhaline zone, indicating that the lower and middle reaches of these estuaries harbour specific assemblages which do not occur in the neighbouring coastal envi­ ronment. Only one species,Thalassiosira proschkinae, had its maximal abundance in the mesohaline zone and can thus be regarded as a truly brackish water species. Thalassiosira pseudonana was restricted to the tidal freshwater zone of the estuaries. Some taxa often appeared to be associated with sediment and detritus particles. The significance of this phenomenon is discussed.

Introduction was carried out. This study revealed the presence of numerous representatives of the diatom genus Thal­ The tidal parts of the Western European rivers assiosira Cleve, most of which had a specific distri­ Schelde and Elbe constitute well mixed coastal plain bution within the estuaries. Some species were locally estuaries. Extensive mud- and sandflats are present dominant, concerning both abundance and biomass, in the meso- and polyhaline zones. A turbidity maxi­ in the phytoplankton communities. The genusThal­ mum occurs in the upper reaches of both estuaries. assiosira comprises more than one hundred species As nutrient concentrations are high in both estuaries (Round et al. 1990). It is often a major component (and especially in the Schelde), phytoplankton of the phytoplankton assemblages of marine (e.g. growth is probably mainly light-limited (Brockmann Lange et al. 1992, Hallegraeff and Jeffrey 1993), estu- 1992, Soetaert et al. 1994). The Schelde mainly differs arine (e.g. Belcher and Swale 1986, Sancetta 1990) from the Elbe in water residence time, which is higher and limnetic water bodies (e. g. Belcher and Swale in the Schelde because of the tenfold lower river dis­ 1977). Despite this widespread occurrence, the identi­ charge (Brockmann 1992, Soetaert and Herman 1995) and in pollution levels, both organic (e. g. sew­ fication of Thalassiosira species is often difficult. This age) and inorganic (e.g. heavy metals), which are is mainly due to the need for electron microscopy to very high in the Schelde estuary (Heip 1988). The observe certain distinguishing characteristics and the high organic loading causes near-anoxic conditions in scatter of taxonomic information over many papers the oligohaline and limnetic reaches of this estuary (cf. Gaul et al. 1993). throughout the year. At the time of sampling a sig­ The aim of this paper is to give a detailed account nificant difference in water temperature between the of the observed Thalassiosira species, with remarks two estuaries was observed, the Schelde (13-17 °C) on their taxonomy, morphology and ecology. Their being on average about 6 °C warmer than the Elbe occurrence within the studied estuaries is compared (7-10.5 °C); this was probably caused by both lati­ to data from other estuaries worldwide. tudinal and seasonal (the Elbe was sampled in April, the Schelde in May) factors. In the framework of the MATURE-project (Bio­ Materials and Methods geochemistry of the MAximum TURbidity zone in Estuaries), an ecological survey of the phytoplankton Subsurface water column samples were taken along spring bloom in the estuaries of the Schelde and Elbe a longitudinal transect in the estuaries of the Schelde 407

104 K. Muylaert and K. Sabbe

samples were fixed with neutralised formalin (30%) to a final concentration of 1-2%. Quantitative cell O counts were made on the unconcentrated material us­ ing the Utermöhl-method (Utermöhl 1958). The sul­ phuric acid-nitric acid oxidation method (Round et al. 1990) was applied to the nct-conccntratcd material to remove the organic content from the diatom frus- tules. Permanent mounts were made with Naphrax. For light microscopy (LM) a Leitz diaplan micro­ scope with PlanAPO and Differential Interference Contrast (DIC) optics and for scanning electron mi­ croscopy (SEM) a Jeol JSM-840 at 15 kV were used. Terminology is based on Ross et al. (1979) and Hasle (1978 a). ELBE Additional information on the ecology of some Thalassiosira species was obtained from an existing dataset comprising 360 intertidal sediment samples (30 stations sampled monthly during one year) from the Schelde estuary. However, no similar information was available for the Elbe estuary. For each Thalassiosira species, reference is made to those studies which were used for its identification. Frustule dimensions (diameter, areolar density and NORTH SEA spacing of the marginal fultoportulae) were deter­ mined on all material examined. For every dimension the range, average value and the standard deviation are given. Unless stated otherwise, ten specimens of every species were measured. If a species was too rare or if the above-mentioned dimensions could only be distinguished in the SEM, less than ten specimens were measured. SCHELDE

Fig. 1. Map of the Elbe (E) and Schelde (S) estuaries and Observations their location in NW Europe. Sampling stations are shown Thalassiosira angulata (Gregory) Hasle 1978 a as dots; the borders between the different salinity zones are indicated (1 = limnetic or freshwater tidal, o = oligohaline, Basionym: Orthosira angulata Gregory 1857 m = mesohaline, p = polyhaline and e = euhaline, accord­ ing to Anonymous 1958). Scale bar corresponds to 50 km. Description: Hasle (1978 a) Morphology: Valve diameter is 13-26 (16 ± 4.1) pm. Cells are connected by mucus threads forming chains (4 May 1993, 11 samples within a salinity range of 1 of up to 6 cells (Fig. 2). There are 8-11 (9.7 ± 1.1) to 23%o) and the Elbe (21 April 1993, 8 samples areolae in 10 pm. The areolae are usually arranged in within a salinity range of 0.5 to 34%o) (Fig. 1). At an eccentric pattern and become smaller towards the each sampling station, both unconcentrated (1 L) and margin of the valve. Near the margin and on the net samples (mesh size 10 pm) were collected. All mantle, the areolae are arranged in radial rows (Figs

Figs 2 —6. Thalassiosira angulata. Figs 2-5. LM. Scale bars = 10 pm. Fig. 2. Cells in chain formation. Fig. 3. Valve view. Figs 4a—b. Valve views, same specimen at different focal levels. Fig. 5. Valve view. Arrowheads indicate position of marginal rimoportulae in Figures 4a and 5. Fig. 6. SEM. Scale bar = 10 pm. External valve view, showing marginal rimoportula (arrowhead) and cap-like structure around outer opening of marginal fultoportula (arrowhead). Figs 7 - 8 . Thalassiosira anguste-lineata. SEM. Scale bars = 10 pm. Fig. 7. External valve view. Fig. 8. Internal valve view. Arrowhead indicates position of marginal rimoportula. Note the presence of a ring of small groups of fultoportulae near the centre of the valve (arrowheads in Figs 7-8). Figs 9 —10. Thalassiosira decipiens. Scale bars = 10 pm. Fig. 9. SEM. External valve view. Note the position of the marginal rimoportula between two fultoportulae (arrowhead). Figs 10a—b. LM. Valve view, same specimen at different focal levels. Figs 2—6: Schelde estuary (plankton). Figs 7—8: Elbe estuary (plankton). Figs 9-10: Schelde estuary (benthic). 408

The diatom genus Thalassiosira 105

3-6). A marginal ling of fultoportulae [3—3.5 (3.2 ture is very reminiscent of the ‘flared skirt’ structure ± 0.2) in 10 pm], one marginal rim oportula (which is on the fultoportulae inT. n o rd e n sk io e ld iiC leve, usually placed closer to one fultoportula) and one central fultoportula are present (Figs 4-6). The ex- Ecology: Common in the polyhalinicum of the ternal tubes of the marginal fultoportulae possess Schelde estuary (up to 250 cclls/mL); rare in the poly- ‘nnp-liVr’ structures at their ends (Fig. 5) Ttiis slruc hulinicum of the Elbe estuaiy. 409

106 KL. Muylaert and K. Sabbe

Thalassiosira anguste-lineata (A. Schmidt) Fryxell et (Fig. 11). The central areola is surrounded by 7 areo­ Hasle 1977 lae and the areolae diminish in size towards the valve mantle. Two marginal rings of fultoportulae and one Basionym:Coscinodiscus anguste-lineatus A. Schmidt marginal rimoportula are present (Fig. 12); the exter­ 1878 nal opening of the latter is large and can be dis­ Description; lúyAell and Hasle (197 /) tinguished in the LM through careful focussing. In Morphology:Valve diameter is 17-33 (25.6 ± 6.7) addition to one sub-central fultoportula, numerous pm; 11 areolae in 10 pm (n = 3). The areolation pat­ fultoportulae occur scattered over the valve face (Fig. tern is linear to fasciculate (Fig. 7). A marginal ring 12). An irregular ring of spines is present on the valve of fultoportulae (3.5 in 10 pm) and a marginal rimo­ mantle (Fig. 11). portula are present (Figs 7, 8). Small arcs of 2 to 3 This description corrresponds to the description of fultoportulae are arranged in a circle around the cen­ T. eccentrica as given by Fryxell and Hasle (1972), tre of the valve (Figs 7, 8). Hallegraeff (1984), Mahood et al. (1986) and San- cetta (1990). Unfortunately, the typical valvocopula Ecology:This taxon was rare in the polyhaline sta­ structure (Fryxell et al. 1981, Hallegraeff 1984) could tions of the Elbe and the Schelde. not be observed as after the acid treatment no intact frustules were found. Thalassiosira decipiens (Grunow) Jorgensen 1905 In our samples, we also found some valves which Basionym:Coscinodiscus eccentricus var.? decipiens were very similar to those of T. eccentrica but mainly Grunow 1878 differed from the latter in having only one (subcen­ tral) valve face fultoportula. All other valve morpho­ Description: Hasle (1978a, 1979) logical features that could be discerned in the LM Morphology:Valve diameter is 8.7—16.2 (13.2 ± 2.3) were identical (size, areolation density and pattern, pm. There are 10—13 (11.5 ± 1) areolae in 10 pm. irregular ring of spines). Whether these valves con­ The areolation pattern is eccentric (Figs 9, 10). The cern a morphological form of T. eccentrica or a yet areolae become smaller towards the valve margin. A unknown taxon is hard to assess as no SEM obser­ marginal ring of fultoportulae [4-6 (5 ± 0.6) in vations were made of this material. We will refer to 10 pm, n = 4], one marginal rimoportula (whose pos­ this form as T. cf. eccentrica. ition is exactly between two fultoportulae in the mar­ ginal ring) and one central fultoportula are present Ecology:During the counts, T. eccentrica and T. cf. eccentrica were lumped together and occurred in (Fig. 9). densities of up to 100 cells/mL in the polyhaline sta­ Ecology:This species was common (up to 1.2 X 10s tions of both studied estuaries. Both were rare in the cells/g sediment dry weight) in silty sediment samples eu- and mesohaline stations. of the Schelde estuary. It was, however, never found We frequently observed cells with sediment or de­ in the plankton of the Elbe or the Schelde. tritus particles attached to their girdle. In the raw material, however, it was impossible to ascertain Thalassiosira eccentrica (Ehrenberg) Cleve 1904 whether these cells belonged to T. eccentrica or T. cf. Basionym:Coscinodiscus eccentricus Ehrenberg 1841 eccentrica, or to both. Interestingly, the same phenomenon was observed in other Thalassiosira Description: Fryxell and Hasle (1972) species with an eccentric areolation pattern. Gaarder Morphology:Valve diameter is 28—52 (37 ± 8.4) pm; and Hasle (1962) and Cloern et al. (1983) identified there are 8—10 (9 ± 0.8) areolae in 10 pm. The valve their specimens as T. eccentrica. However it is not face is flat and the areolation pattern is eccentric sure whether their observations truly concern T. ec-

Figs 11 — 12. Thalassiosira eccentrica. Scale bars = 10 pm. Fig. 11. LM. Valve view. Arrowheads indicate the marginal spines. Fig. 12. SEM. Internal valve view. Note the position of the marginal rimoportula (arrowhead). Figs 13 — 14. Thalassiosira hendeyi. Fig. 13a—b. Scale bars = 10 pm. LM. Valve view, same specimen at different foci. The two opposite rimoportulae are indicated (arrowheads) in Fig. 13b. Fig. 14. SEM. Scale bar = 1 pm. Detail of external marginal area, showing the external opening of a rimoportula and the radial ridges on the valve mantle (arrowheads). Fig. 15. Thalassiosira minima. Scale bar = 10 pm. SEM. Internal valve view. The arrowhead indicates the marginal rimo­ portula. Fig. 16. Thalassiosira nodulolineata. Scale bar = 10 pm. LM. Valve view. The arrowhead indicates the 5 -6 fultoportulae which are present inside the central areola. Figs 17—19. Thalassiosira nordenskioeldii. Scale bars = 10 pm . Fig. 17. LM . Cells in chain form ation. Fig. 18. LM . Valve view. Note the ‘flared skirt’ structures around the outer openings of the marginal fultoportulae (arrowheads), the depressed valve centre and the wide valve mantle. Fig. 19. SEM. External valve view. The ‘flared skirt’ structures are largely eroded. Fig. 20. Thalassiosira pacifica. Scale bar = 10 pm. LM. Cells in chain formation. Figs 11-12, 17-20: Elbe estuary (plankton). Figs 13-16: Schelde estuary (plankton). 410

The diatom genus Thalassiosira 107 411

108 K. Muyîaert and K. Sabbe

céntrica as neither study gives enough morphological Description: Hasle and Fryxell (1977) details for correct identification. Lange et al. (1992) Morphology:Valve diameter 37 pm, 6 areolae in also described an unidentified taxon with an eccentric 10 pm (n = 1). Areolation pattern linear (Fig. 16). areolation pattern (referred to as T. decipiens'!) which One marginal ring of fultoportulae and one marginal had particles attached Lo the girdle. Further study is rimoportula are present. This species is characterized necessary to assess whether all these taxa concern one by a cluster of 5 to 6 fultoportulae, which are located and the same (possibly unidentified) taxon. inside the central areola (Fig. 16). A ring of irregu­ larly placed processes is present on the valve mantle. Thalassiosira hendeyi Hasle et Fryxell 1977 Thalassiosira nodulolineata mainly differs from T. Synonym: Coscinodiscus hustedtii Müller-Melchers densannula Hasle et Fryxell in the density of the mar­ 1953 ginal fultoportulae and the presence of occluded pro­ cesses (Hasle and Fryxell 1977). Although these Description: Hasle and Fryxell (1977),Mahood et al. characters could not be distinguished in the single (1986) specimen observed, we could still identify it as T. nod­ Morphology:Valve diameter is 61—75 (68 ± pm, 7) 6 ulolineata, as its marginal processes were not regu­ areolae in 10 pm (n = 2). The areolation pattern is larly arranged (cf. Hasle and Fryxell 1977). linear (Fig. 13a). Two marginal rings of fultoportulae and one central fultoportula can be distinguished; Ecology:This taxon was rare in the polyhaline sta­ two marginal rimoportulae are present on opposite tions of the Schelde estuary. sides of the valve (Fig. 13b). The valve mantle is characterized by radially arranged ridges which are Thalassiosira nordenskioeldii Cleve 1873 separated by two to three areolae (Fig. 14). Description: Hasle (1978 a) Ecology:This species was rare in the polyhaline rea­ Morphology:Valve diameter is 9—23 (14 ± 3.8) pm. ches of the Schelde estuary. Cells are connected by mucus threads to form chains of up to 24 cells (Fig. 17). There are 20 -2 4 (22 ± 1.2) Thalassiosira minima Gaarder 1951 areolae in 10 pm (n = 11). Areolation pattern is fas­ Synonyms: Coscinosira floridana Cooper 1958, Thal­ ciculate (Fig. 18). One marginal ring of fultoportulae assiosira floridana (Cooper) Hasle 1972 [4—6 (5 ± 0.6) in 10 pm, n = 12], one central fulto­ portula and a marginal rimoportula are present (Figs Description: Belcher and Swale (1986); Hasle 18, 19). The centre of the valve face is depressed. The (1976a); Hasle (1980) valve mantle is wide which gives the frustules their Morphology:Valve diameter is 10 pm (n = 1). The typical, octangular shape in girdle view (Fig. 17). The areolar density and the areolation pattern could not outer openings of the marginal fultoportulae are sur­ be determined. A marginal ring of fultoportulae, one rounded by a ‘flared skirt’ (cf. Hasle 1978 a). This marginal rimoportula and 2 central fultoportulae are structure can also easily be distinguished in LM (Fig. present (Fig. 15). 18). Ecology:Only one valve of this taxon was found in a Ecology:This species was common (up to 250 cells/ SEM mount from a polyhaline station of the Schelde mL) in the eu- and polyhaline zones of the Elbe estu­ estuary. ary. It Was only rarely found in the polyhaline sta­ tions of the Schelde estuary. Thalassiosira nodulolineata (Hendey) Hasle et Fryxell 1977 Thalassiosira pacifica Gran et Angst 1931 Basionym:Coscinodiscus nodulolineatus Hendey 1957 Description: Hasle (1976 a, 1978 a)

Figs21—23. Thalassiosira pacifica. Scale bar = 10 pm. Fig. 21. LM. Valve view. Fig. 22. SEM. External valve view. The arrowhead indicates the marginal rimoportula, which replaces a fultoportula. Fig. 23. SEM. Detail of external marginal area. Figs 24—26. Thalassiosira proschkinae. Fig. 24. Scale bar = 10 pm. LM. Living cell. Note the four chloroplasts. Fig. 25. Scale bar = 1 pm. SEM. Internal valve view. Arrowhead indicates the subcentral rimoportula. Fig. 26: Scale bar = 10 pm. SEM. External valve view. Note the presence of detritus and sediment on the girdle of the cell. Figs 27-28. Thalassiosira pseudonana. Fig. 27. Scale bar = 10 pm. LM. Valve view. Fig. 28. Scale bar = 1 pm. SEM. External valve view. Figs 29—30. Thalassiosira punctigera. Scale bar = 10 pm. SEM. Fig. 29. External valve view, showing the presence of 5 occluded processes. Fig. 30. Internal valve view. Arrowheads indicate the marginal rimoportula. Fig. 31. Thalassiosira rotula. Scale bar = 10 pm. LM. Valve view. Figs 21 — 22, 29-31: Elbe estuary (plankton); Figs 23-28: Schelde estuary (plankton). 412

Tile diatom genus Thalassiosira 109 413

110 K. Muylaert and K. Sabbe

Morphology:Valve diameter is 14-24 (17 ± 3.1) pm. Thalassiosira punctigera (Castracane) Hasle 1983 Cells are connected by mucus threads to form chains of up to 6 cells (Fig. 20). There are 11-18 (15 ± 1.9) Basionym:Ethmodiscus punctiger Castracane 1886 areolae in 10 pm and the areolation pattern is radial Synonym: Thalassiosira angstii (Gran) Makarova to tasciculate (Fig. 21). liacli valve po33C33C3 a mar­ ginal ring of fultoportulae [3.5-5 (4.1 ± 0.5) in 10 1970 pm], one central fultoportula and a marginal rimo­ Descriptions: Fryxell (1975); Hasle (1983) portula which takes the same position as a fultoport­ ula (Fig. 22). The valve mantle is three rows of areo­ Morphology:Valves are 45 —100 (88 ± 7) pm in dia­ lae wide (Fig. 23); the mantle areolae are smaller than meter and there are 10-16 (12 ± 2.3) areolae in those on the valve face. 10 pm. The areolation pattern is fasciculate. One Ecology:This taxon was very common (up to 800 marginal ring of fultoportulae [4.5—6 (5.1 ± 0.5) in cells/mL) in the polyhaline stations of both estuaries. 10 pm], one marginal rimoportula and one central fultoportula are present (Figs 29, 30). This species is Thalassiosira proschkinae Makarova 1979 characterized by the presence of large, occluded pro­ cesses near the valve margin; their number and ar­ Descriptions: Belcher and Swale (1986); Feibicke et rangements is variable. al. (1990); Krammer and Lange-Bertalot (1991); Makarova et al. (1979) Ecology:This species was rare in the eu- and polyha­ line reaches of the Elbe estuary (up to 3 cells/mL) Morphology:The valve diameter is 7—8 (7.5 ± 0.5, and in the poly- to mesohaline reaches of the Schelde n = 8) pm; there are 16-22 (19 ± 2.1, n = 8) areolae estuary (1 cell/mL). However, because of its large size in 10 pm. In living cells, four chloroplasts can be dis­ compared to most other observed Thalassiosira re­ tinguished (Fig. 24). The areolation pattern is radial presentatives, its contribution to total phytoplankton to eccentric. This species is characterized by a mar­ biomass was often considerable (up to 14%). ginal ring of fultoportulae, one subcentral rimoport­ ula and a central fultoportula (Fig. 25). Thalassiosira rotula Meunier 1910 Ecology: This species was extremely abundant (up to 3370 cells/mL) in the polyhaline and mesohaline sta­ Descriptions: Hasle (1976a); Syvertsen (1977) tions of the Schelde estuary. In the Elbe estuary it was present from the polyhaline to limnetic stations Morphology:Valve diameter is 22—34 (27 ± 3.3) pm. but reached its maximum abundance in the polyha­ The frustules are connected by mucus threads for­ line stations (up to 675 cells/mL). Most cells belong­ ming chains of up to 6 cells. Numerous fultoportulae ing to this species were density covered with sediment are present; they are arranged in different marginal and detrital material on their girdle face (Figs 24, 26). rings but also occur scattered over the valve face and clustered in the centre of the valve (Fig. 31). The Thalassiosira pseudonana Hasle et Heimdal 1970 valve face is covered with radially arranged ridges [20-25 (22.5 ± 1.5) in 10 pm]. However, some valves Synonym:Cyclotella nana Hustedt 1957 from the Elbe estuary did not display these ridges Description: Belcher and Swale (1977); Hasle but were characterized by rows of radially arranged (1976 b); Hasle and Heimdal (1970) areolae. This pattern is typical of Thalassiosira grav­ ida Cleve, a form which is considered as an ecologi­ Morphology:Valve diameter is 4.5 pm (n = 2). The cally induced form of T. rotula (Hasle 1976 b, Sy­ areolation density and pattern could not be deter­ vertsen 1977). In our material, numerous valves were mined because of the minute size of the valves. There present which displayed a valve pattern that is tran­ are 7-12 marginal fultoportulae and one marginal sitional between these two morphological types. rimoportula (the latter is not visible in Figs 27 and These transitional forms have also been reported 28). The external valve face is covered with granules and ridges; the latter are radially arranged near the from monoclonal cultures (Syvertsen 1977). There­ valve face margin. fore we did not treat T. gravida and T. rotula as two Thalassiosira pseudonana is very similar to T. guil­ separate species. lardii Hasle. The difference between these two species Ecology:This species was common in the eu- and po­ was treated in detail by Hasle (1978 b). Our speci­ lyhaline zones of the Elbe (up to 80 cells/mL) and in mens clearly concern T. pseudonana, as the external the polyhaline zone of the Schelde (up to 36 cells/ valve face is not smooth (as in T. guillardii, cf. Hasle mL). The form corresponding to T. gravida was only 1978 b, figs 32 and 33) but is covered with silicious found in the Elbe estuary. This is most probably due ridges and warts (Fig. 28). to the lower water temperature in this estuary, which Ecology:This taxon was rare in the oligohaline and induces T. rotula to form valves of the gravida-type limnetic stations of both estuaries studied. (cf. Hasle 1976 a). 414

The diatom genus Thalassiosira 111

Discussion whereas this pattern is usually eccentric in T. decipi­ ens and T. angulata. Moreover, in LM, colonies of T. Identification problems pacifica can be discerned from those of T. angulata Thalassiosira angulata, T. decipiens, (?) T. levanderi in having shorter connecting threads between the Van Goor, T. nordenskioeldii and T. pacifica hc.long to cells and in having a less sharp distinction between the complex of Thalassiosira species with one central the girdle and valve (Hasle 1978 a and Jbig. 20). fultoportula, one marginal ring of fultoportulae and Although Thalassiosira levanderi is often reported one marginal rimoportula. Notwithstanding the fact in high numbers from brackish and marine plankton that most representatives of this species group have (Drebes 1974, Bakker et al. 1990, Pankow 1990, been described in detail by Hasle (1978 a, 1979), some Tikkanen and Willén 1992, Rijstenbilet al. 1993, of them are still often misidentified because of their Snoeijs 1993), the identity of this species is as yet un­ clear as, to our knowledge, the type material has difficult identification in the LM. Thalassiosira nordenskioeldii can easily be dis­ never been examined. The type description of this tinguished from the other species of this complex by species (Van Goor 1924) does not contain enough de­ its typical, octangular shape in girdle view and the tailed information (e. g. on the presence and/or pos­ ition of fulto- and rimoportulae) to make a positive presence of the ‘flared skirt’ structure around the dis­ tal ends of the marginal fultoportulae (Hasle 1978 a). identification of this species possible. Many small Thalassiosira angulata is very reminiscent of T. de­ Thalassiosira species, such as T. allenii Takano, T. pa­ cipiens (cf. Hasle 1978 a, 1979) but differs from the cifica and the very common species T. proschkinae have been described since; their relationship to T. lev­ latter in the following respects: (1) The distance between the marginal fultoportu­ anderi is as yet unknown. Until the type material of lae is larger in T. angulata (about 3 in 10 pm) than in this taxon has been studied in detail, the use of this name should be avoided. T. decipiens (4 -6 in 10 pm); (2) the position of the marginal rimoportula is dif­ ferent (close to one fultoportula in T. angulata, be­ Diversity and distribution tween two fultoportulae in T. decipiens)', (3) T. decipiens does not possess the typical ‘cap­ The genus Thalassiosira is a dominant component of like’ structures at the distal ends of the marginal ful­ the spring phytoplankton assemblages in the eu-, toportulae; poly- and mesohaline reaches of both the Elbe and (4) all specimens of T. angulata in the material the Schelde. This observation is in accordance with studied were characterized by the radial arrangement the findings of other studies on estuarine phytoplank­ of the areolae near and on the valve mantle. This ton worldwide (e.g. Belcher and Swale 1986, Ma- feature was never observed in any specimens of T. hood et al. 1986, Gayoso 1989, Sancetta 1990, Haigh decipiens. Although this characteristic is also visible et al. 1992, Marshall and Alden 1993, Ragueneauet in the type specimens of T. angulata (and all other al. 1994). In the present study, a total of 13 Thalas­ specimens illustrated in Hasle 1979, figs 73, 74), it siosira species has been identified. All of these were has previously not been mentioned as a major dis­ present in the Schelde material; 10 species occurred in tinguishing characteristic. the Elbe. However, a more comprehensive sampling In addition to these morphological features, an campaign in different seasons might yet reveal more ecological difference between the two species is sus­ Thalassiosira species, as the presence of single valves pected: T. angulata appears to be a typical marine, of e. g. T. leptopus (Grunow) Hasle et Fryxell and T. planktonic species (Hasle 1978 a), whereasT. decipi­ bramaputrae (Ehrenberg) Hákanssonet Locker in the ens is most often recorded from shallow, coastal and intertidal sediments of the Schelde (Sabbe, unpub­ estuarine environments and seems to be a tycho- lished) already suggests. planktonic (or even benthic) species (Drebes 1974, Comparison of our results with previously pub­ Belcher and Swale 1986, Bérard-Therriault et al. lished checklists and single observations of Thalas­ 1987). In the Schelde estuary, T. angulata was com­ siosira species from both the Schelde (Bakker and De mon in the plankton, whileT. decipiens was never Pauw 1974, De Pauw 1975, Somers 1978 and Rijsten­ observed in the water column. However, the latter bil et al. 1993) and the Elbe (Schulz 1961, Nötlich species was frequently found in intertidal benthic 1972) revealed that 7 and 5 species respectively are samples from that estuary (Sabbe 1993). It is there­ new records for these estuaries. It mainly concerns fore suspected that many reports of T. decipiens from recently described species (such as T. proschkinae) or estuarine plankton actually concernT. angulata (cf. ‘difficult’ taxa (such as Thalassiosira angulata). Wtikowski 1994). Most taxa were also observed in similar studies Thalassiosira pacifica resembles both T. angulata from estuarine systems in the Northern Hemisphere. and T. decipiens but can be distinguished from these Mahood et al. (1986) described 20 Thalassiosira spec­ in the position of the marginal rimoportula, which ies from the San Francisco Bay system, 9 of which replaces a fultoportula. In addition, Thalassiosira pa­ were also found in the Schelde estuary. Sancetta cifica often has a fasciculate valve areolar pattern, (1990) reported 15 Thalassiosira species from a fjord 415

112 K. Muylaert and K. Sabbe

Table I. Summary of the data on the distribution of the Thalassiosira species in the different salinity zones (according to Anonymous 1958) of the Schelde (S) and Elbe (E) estuaries. Note that Thalassiosira decipiens has not been included in this list as it was never observed in the plankton.

Sampling station: Euhalinicum Polyhalinicum Mesohalinicum Oligohalinicum Limneticum

E ESES ESE

T. nordenskioeldii + + + + + + + - - - - - T. rotula + + + + + + - - - - T. punctigera + + + - - - T. eccentrica + + + + + - + - — - T. anguste-lineata - + + - - - - - T. hendeyi - - + - - - - - T. minima — — + — — — — — T. nodulolineata - - + - - - - - T. angulata - + + + + - + - - - T. pacifica - + + + + + + + + + + - - - T. proschkinae - + + + + + + + + + + + + + + + + + + T. pseudonana ------+ +

[— = absent, + = rare (less than 10 cells/mL), + + = common (10-100 cells/mL), + + + = very common (more than 100 cells/mL)] system in British Columbia; 7 of these were also pre­ and 71 rotula, occurred. Similar blooms, dominated sent in our material. Of the 13 Thalassiosira species by S. costatum and Thalassiosira species, have al­ Belcher and Swale (1986) found in British estuaries, ready been reported for both the Schelde (Rijstenbil 6 occurred in the Schelde. The most striking feature et al. 1993) and Elbe (Schulz 1961, Nötlich 1972)and of their study is the predominance of minute taxa appears to be the typical spring situation in the meso- such as T. proschkinae, T. minima and T. profunda and polyhaline reaches of numerous estuarine sys­ (Hendey) Hasle. This could be due to the fact that tems worldwide (cf. Sancetta 1990, Haigh et al. 1992, most of their samples were taken during the summer. Ragueneau et al. 1994, Marshall and Alden 1993). In temperate, marine environments, the plankton Only two species, 71 proschkinae and 71 pseudonana, community characteristically undergoes a seasonal actually reached their maximum abundance in the change from a spring bloom situation, dominated by more upstream, mesohaline reaches of the estuaries. net-plankton, to a post-bloom situation in summer, Thalassiosira pseudonana was rare in the freshwater when the plankton is dominated by nano- and pico- tidal reaches of the Schelde and Elbe, which is in ac­ planktonic taxa (Kiorboe 1993). Possibly, similar ev­ cordance with its distribution in other rivers, such as ents in the estuarine environment could explain the the Weser (Hustedt 1957) and many English rivers absence of the larger Thalassiosira taxa from their (Belcher and Swale 1977).Belcher and Swale (1986) species list. Coastal (as opposed to estuarine) en­ only rarely found this species in brackish waters. vironments seem to harbour rather different Thalas­ However, Hasle (1978b) lists several other localities siosira populations: Rivera (1981), Hallegraeff (1984) from both freshwater and marine environments. and Gayoso (1989)reported between 20 and 25 Thal­ Thalassiosira proschkinae was the most abundant assiosira species in coastal samples from South Amer­ phytoplankton species in the meso- and polyhaline ica and Australia, most of which were not observed stations. In the Schlei estuary (Germany), Feibicke et in the Schelde and Elbe. This discrepancy in species al. 1990 observed this species within a salinity range composition probably reflects the different environ­ of 2.7-16.6%o, with a maximum at about 4%o, and mental conditions in estuarine and coastal environ­characterized it as mesohalobous and euryhaline. ments rather than biogeographical differences, as the While the lower limit of this salinity range is in close majority of these species have also been observed in agreement with our observations from the Schelde coastal waters of the Northern Hemisphere (cf. Hal­ and the Elbe, T. proschkinae also seems to tolerate legraeff 1984). higher salinities and occurred in high numbers in the The distribution of the observed Thalassiosira polyhaline reaches of both estuaries. However, its ab­ species within both estuaries seems to be species- sence from the euhaline Elbe station could indicate specific and limited to certain salinity zones (Table I). that it does concern a truly brackish water species. Diversity was highest in the polyhaline reaches of Interestingly, since its description by Makarova et al. both estuaries, where a mixed bloom of Skeletonema (1979)it has subsequently been reported as a com­ costatum (Greville) Cleve and several Thalassiosira mon, sometimes dominant, species from estuaries in species, such as T. pacifica, T. eccentricalT. cf. eccen­ Europe and North America (e. g. Belcher and Swale trica, T. proschkinae, T. angulata, T. nordenskioeldii1986, Bérard-Therriault et al. 1987, Feibicke et al. 416

The diatom genus Thalassiosira 113

1990, Wendker 1990). Because of its minute size, it ment particles just causes them to sink more rapidly. has probably been overlooked or misidentified (cf. Cloern et al. (1983) postulated that in estuaries the above) in many estuaries. presence of sediment aggregates on the girdle could The dominant Thalassiosira species in the euhaline promote the retention of the cells in nutrient-rich zone of the Elbe estuary were T. nordenskioeldii, T. estuarine waters by rapidly sinking into the upstream rotula and, to a lesser degree, T punctigera. These flowing salt wedge, a mechanism they called ‘hydro- three species displayed a similar distribution pattern dynamical trapping’. in the San Francisco Bay system (Mahood et al. Oddly enough, both living and empty frustules of 1986), where they were also restricted to the marine T. proschkinae appear to be very abundant in the in­ reaches. They are often abundant in coastal waters tertidal sediments of the Schelde estuary (cf. Sabbe such as the North Sea (Meunier 1915, Kat 1982) and and Vyverman 1991, as Spec. 1), while other species, can therefore be characterized as marine, coastal which were also abundant in the water column, were species, which do not penetrate deeply into the estu­ much less frequently found in benthic samples. As, aries. given its minute size, one would normally expect T. proschkinae cells to sink slower, the sediment aggre­ gates could possibly cause the cells to sink quicker to Association ofThalassiosira cells with detritus and the sediment and thus prolong their time within the sediment particles estuary and more specifically on the intertidal areas. We frequently observed cells of Thalassiosira Such a mechanism would actually be very remi­ proschkinae (Figs 24, 26) and T. eccentrica/T. cf. ec­ niscent of the behaviour of certain surf-zone diatoms centrica whose girdle was covered with sediment and (e. g. Anaulus australis Drebes et Schulz), which pos­ detritus particles. In the case of T. eccentricalT. cf. sess an analogous mechanism that prevents them eccentrica this sometimes caused the cells to form from being washed out to the sea (Talbot et al. 1990). larger aggregates of several cells and sediment par­ Clearly, the association between diatom cells and ticles. Similar phenomena have been reported before sediment or detritus particles and its ecological sig­ by several authors. It usually involved diatoms (often nificance need further investigation. This phenom­ tentatively) identified as T. eccentrica (Gaarder and enon might be much more widespread than pre­ Hasle 1962, Cloern et al. 1983), T. decipiens (Ernissee viously thought and may, apart from in surf zones, and Abbott 1975, Langeet al. 1992), T. aculeata also be of importance in estuaries. Proschkina-Lavrenko (Gleser et al. 1988) or T. proschkinae (Feibicke et al. 1990). These literature re­ ports indicate that this phenomenon might be more Acknowledgements widespread than previously thought. Moreover, it ap­ pears to be distinctly species-specific. Gaarder and Both authors are research assitants of the National Hasle (1962) explained this phenomenon as a mere Fund for Scientific Research (Belgium). This study agglutination of particles with the threads protruding was supported by the European Union (MATURE- from the girdle. However, from an ecological view­ project, nr. EV 5V-CT92-0064). Financial support point, the association of planktonic diatoms with was provided by FKFO project nr. 2 0094 92. Finally, sediment particles seems to be paradoxical. Usually many thanks are due to two anonymous referees who the cells are characterized by the presence of features provided useful comments on the manuscript. which promote their retention in the water column (Reynolds 1984), while their association with sedi- Accepted 22 December 1995

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