ICES mar. Sei. Symp., 195: 249-259. 1992

Variability in phytoplankton biomass in the German Bight near Helgoland, 1980-1990

W. Hickel, J. Berg, and K. Treutner

Hickel, W., Berg, J.. and Treutner, K. 1992. Variability in phytoplankton biomass in the German Bight near Helgoland, 1980-1990.-IC E S mar. Sei. Symp., 195:249-259.

The variability of total phytoplankton biomass and species composition was measured from surface-water samples taken every working day near the island of Helgoland, German Bight, North Sea. These data were analysed, together with data on inorganic nutrients, salinity, and Elbe river discharge. Main diatom growth periods were found in April and June through August, whereas non-diatom phytoplankton (“flagellates’') bloomed in July and August. The biomass in the winter months consisted mainly of unidentified, small “^-flagellates" of uncertain trophic state. Single peaks, or plankton blooms, varied considerably in size and time of occurrence within the vegetation period. Variations of single phytoplankton values ranged from almost nil to 1000/(g organic carbon/1 during the year; variations of two orders of magnitude within a few days were not uncommon, reflecting sequences of different watermasses with their plankton populations. Monthly median values ranged from <10 to 350//g C/1. While the total phytoplankton biomass near Helgoland increased during the last three decades, the potential eutrophication effect on phytoplankton is not very clear. For the decade 1980-1990, there is no apparent trend in phytoplankton increase or decrease, in contrast to other findings in the open North Sea. Analysing two periods of large Elbe river floods (1981/1982 and 1987/1988), an influence of additional nutrient supply on phytoplankton stocks of the inner German Bight was different: whereas late summer floods in 1981 resulted in very large phytoplankton stocks also near Helgo­ land, early (April) floods in 1987 and 1988 had no such consequences. From the hydrographical structure of the German Bight it is more likely that large river water quantities influence phytoplankton stocks first by increased density stratification and then by adding nutrients; this might be true particularly for the inner German Bight, whereas towards the outer German Bight, where nutrient concentrations rapidly decrease, the eutrophication effect might become more significant.

W. Hickel, J. Berg, and K. Treutner: Biologische Anstalt Helgoland, Notkestrasse 31, 2000-Hamburg 52, Germany.

Introduction 1990 are given here in more detail, together with inor­ ganic nutrient and salinity data as well as Elbe river The variability of total phytoplankton biomass and discharge volumes, which influence the German Bight in species composition was measured from surface-water many ways. samples, taken every workday at Helgoland Roads, The Helgoland Roads data have been analysed by German Bight, North Sea (Fig. 8). These time-series Gillbricht (1983) for 1981 and Gillbricht (1988) for the measurements were started in 1962 (by Gillbricht) and period 1962-1986. Radach and Berg (1986), Radach et comprise other biological parameters as well as hydro- al. (1990), and Radach and Bohle-Carbonell (1990) graphic and inorganic nutrient measurements. analysed the Helgoland data from 1962 through 1984 in The sampling station, in a narrow channel between respect of the structure of the variance as well as to the two islands of Helgoland, represents a mixed water identify possible trends. from the surrounding sea area and is considered to be representative for a larger area of this transition zone between estuarine and coastal water, and open North Methods Sea water. The last decade being the topic of the ICES Vari­ Sampling was done on Helgoland Roads (54°11.3'N ability Symposium, the phytoplankton data from 1980- 7°54.0'E) from a boat at a fixed time every workday,

249 thus not taking into account the tidal phase. The water phic Noctiluca) dominated by far in terms of biomass column at the sampling station is about 5 m deep and during their growth period (Fig. 1), though/i-flagellates always well mixed due to strong tidal currents. There­ were present in large numbers. In winter, however, the fore, the surface sample was considered to be represen­ "flagellate” biomass consisted mainly of tiny, unident­ tative for the water column. ified “^-flagellates”. The microplankton was counted with the inverted Salinity was measured with an inductive salinometer, microscope after fixation with Lugol's iodine solution. and inorganic nutrients using the methods described in The determination to the species level was only partly detail by Grasshoff et al. (1983). W ater samples were possible with the fixed material. More often, only the analysed for nutrients immediately after sampling, ex­ genera could be determined, or higher taxonomic levels. cept in the case of silicate which was analysed from In the case of minute, naked ^-flagellates, only size deep-frozen samples. The Elbe river discharge data classification was possible with the fast counting pro­ were taken from the yearly reports of the “Arbeits­ cedure applied here. Counted plankton was converted gemeinschaft für die Reinhaltung der Elbe” (ARGE to organic carbon using factors calculated from size and Elbe 1990a, b, c). The salinity and temperature data shape of the plankters based on Hagmeier (1961). These from the RV “Gauss” cruise in August, 1981. were biomass values, as organic carbon, were then summed measured with a bathysonde by members of the Ger­ up for diatom and non-diatom ( = “flagellate”) biomass man Hydrographic Institute, Hamburg, and the nutri­ at least. The “flagellates” thus included various taxono­ ent analyses were made by Dr K. Eberlein, University mic groups; the dinoflagellates (without the heterotro- of Hamburg.

Carbon D i a t o m s Helgoland Roads Pg/1 Years 1980-1990 600!

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Figure 1. Annual cycles of diatoms and flagellates, Helgoland Roads (1980-1990). All year cycles projected into one year. Results unidentified, small, naked "^-flagellates” which might have been heterotrophic. Apart from them, very low Growth period of the phytoplankton phytoplankton biomasses were found in winter. Hetero­ The growth period of diatoms and non-diatoms trophic flagellates, frequent among the size-classes (= “flagellates”) was first determined by projecting all counted as ^-flagellates, would have no problems surviv­ year-cycles 1980-1990 of the calculated biomasses into ing in winter during poor light conditions, when auto- one year. Figure 1 shows the year-cycles of the single trophic phytoplankters could thrive only in the surface years. Figure 2 gives a scatter plot with the median, water layer, and only during calm wind periods. Seston upper, and lower quartiles. Main diatom growth periods concentrations being high, and wind turbulence nor­ are obvious from the end of March, with peaks in April mally considerable, conditions for a net production of and May, but further diatom growth also occurred phytoplankton in the water column outside the vege­ during the whole summer, until mid-September. Non­ tation period (March to September) would be rare and diatom phytoplankton (“flagellates”), however, are of short duration. This makes it unlikely that a consider­ abundant in a much more restricted period, from June to able and constant autotrophic ^-flagellate population mid-September only, with a clear peak in July. Obvi­ could possibly persist throughout the winter. Hence, the ously, the flagellates bloom under typical summer con­ winter flagellate population, representing a biomass of ditions with high temperatures and high regeneration about 10-15 ug C/1 in the decade considered here, is rates of phosphate and ammonia, whereas diatom likely to be heterotrophic at least during the winter blooms are found both under “new” and “regenerated” period. The separate analysis of the phytoplankton nutrient conditions. during the vegetation period seems to be more appropri­ The biomass in the winter months consisted mainly of ate.

Carbon Diatoms m onthly Medians 1980-1990 ]ig/l Helgoland Roads and 25%, 75% Quartiles 150

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Figure 2. Variations in diatom and flagellate biomass at Helgoland Roads. All data for 1980-1990 pooled, with median, upper (75%), and lower (25%) quartiles.

251 Variation of phytoplankton stocks in time body towards the open North Sea; the sites of potential growth-limiting nutrient concentrations in summer are Considering single values, phytoplankton concen­ not far away from Helgoland. trations varied considerably in size and time of occur­ rence within the vegetation period. Variations in bio­ The influence of Elbe river freshwater runoff on mass values ranged from almost nil to 1000 fig organic phytoplankton stocks carbon/1. Variations of two orders of magnitude within a few days were not uncommon, reflecting sequences of The potential eutrophication effect on phytoplankton watermasses with different plankton populations. abundance is not very clear from the Helgoland data, Monthly median values ranged from <10 to 350 fig C/1 certainly not in the decade considered here. A diatom (Fig. 6). increase might have taken place during the period of Considering yearly median biomass values of the phosphate increase, whereas a flagellate increase seems vegetation periods, when a net production of the auto- to have occurred a decade later, along with a nitrogen trophic plankton in the water column is possible, an increase. However, the year-to-year variability was an increase of phytoplankton biomass for the last three order of magnitude larger than a possible trend, and decades seems evident (Fig. 3). Separating the potential single events like the dinoflagellate blooms in 1981 tend bloom periods of diatoms and flagellates (according to to mask a trend. Figs. 1 and 2), diatom stocks seem to increase up to the If there was a direct influence of eutrophication by the early 1980s only, whereas average flagellate stocks seem river Elbe - as the main freshwater and nutrient source - to increase during the 1980s (Fig. 3). However, the year- on phytoplankton growth, then a correlation between to-year variation in diatom and flagellate biomass during the Elbe discharge volumes with phytoplankton stocks the growing season is about one order of magnitude could be expected. Such relations could lead to more higher than a possible upward trend. Also, the monthly insight than calculating trends despite the large inter­ medians of phytoplankton, diatom, and flagellate bio­ annual variation. From Figure 7, two periods of particu­ masses of the decade considered here show no clear larly large Elbe river floods are obvious, in 1980/1982 trend (Fig. 6). The years with exceptional flagellate and 1987/1988. The daily discharge values give the short­ blooms are the prominent features. The large diatom term peaks, whereas the lower graph of Figure 7 stocks in 1985 were the result of peculiar hydrographic accumulates the discharge volumes for the months Janu­ conditions: in 1984 and 1985, the coastal water zone was ary through August of the respective years. less extended due to low Elbe river water outflow (Fig. In 1987, the discharge volumes were particularly 7). In 1985, diatom blooms developed in the North large. In the first half of the year, 21.7 x 109 m3 of fresh Frisian coastal water (Bauerfeind et al., 1990) in April water from the Elbe river had flowed into the German and extended farther southward than usual, reaching Bight, about the average discharge volume of a whole Helgoland waters. year. In 1987 and 1988, the major flood events took The long-term variations of the inorganic nutrients place in April, in contrast to 1981 when a late flood event phosphate and nitrate are given in Figure 4 as yearly was recorded in July/August (A R G E Elbe, 1990a, c). medians. This figure shows the rise and fall of phosphate These periods were evaluated here, as they could be concentrations as well as the late rise of nitrate concen­ expected to show an influence of additional nutrient trations. The rise of phosphate in the inner German supply on phytoplankton stocks of the inner German Bight comes to an end around 1980, levelling off and Bight. They were, on the other hand, examples of soon declining. Nitrate concentrations, however, characteristic hydrographic situations caused by high started to rise in the 1980s. The large Elbe river floods in freshwater inflow into the German Bight. In 1981, large 1987/1988 with their additional nitrogen loads (Gerlach, Elbe river water inflow followed by a late (July/August) 1990; A R G E Elbe, 1990b) led to a marked increase in flood event resulted in a large area of the German Bight nitrate concentrations at Helgoland (Fig. 9); in the with a strong vertical stratification due to salinity gradi­ following years, too, these high levels remained in the ents during a calm weather period. In spring 1987 and coastal water. 1988, early (April) floods caused rather normally ex­ This eutrophication process, first with phosphate, tended Elbe water plumes without such large stratified then with nitrate, leads to the question of possible areas, due to windy weather. biological effects. Though the absolute nutrient levels in The consequences of the river floods appearing at the Helgoland waters are not growth-limiting for phyto­ different seasons seemed to be strikingly different: plankton in summer (Gillbricht, 1988), the shift of N/P- whereas a late summer flood in 1981 resulted in the ratios (Fig. 5) as the result of the above mentioned largest phytoplankton blooms found so far in the area, difference in P- and N-eutrophication might have had an early (April) floods in 1987 and 1988 (Fig. 9) did not effect on the composition of phytoplankton populations. result in much larger phytoplankton stocks near Helgo­ Furthermore, there is always a steep gradient of nutrient land. This cannot be explained from additional inor­ concentrations from the German Bight coastal water ganic nutrient supply alone; rather one would have

252 Carbon Phytoplankton jig/l Medians March 15 - Sept. 15 1001

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Figure 3. Phytoplankton biomass at Helgoland Roads (1962-1990). Yearly medians of the growing season (middle of March through mid-September, upper graph). Yearly medians of the potential blooming periods of diatoms (April through mid- September) and flagellates (mid-June through mid-September).

253 no; - n Helgoland Roads po;- -p Carbon Diatom s prnol/l yearly Medians jjm ol/l jig/1 monthly Medians 30 n 0.9 300

-0.7 250 20 - - 0.6 200 - 15- -0.5 150- -0.4 10- -0.3 1 0 0 -i - 0.2 50- - 0.1 - 0.0 80

Years 1962 - 1990 Carbon Flagellates Figure 4. Nitrate and phosphate concentrations at Helgoland Roads (1962-1990), yearly medians. p.g/1 m on thly Medians 350 q 300 J expected the contrary. In 1987/1988, nitrate concen­ 250- trations were twice as high, silicate concentrations 200 - almost ten times higher, as the average of the decade 150- before. Only phosphate concentrations had decreased, 100H indicating their origin from (constant) point sources and 50- a dilution effect (Fig. 9). The particularly high nitrate concentrations resulted in a large nitrogen surplus in the coastal water even during summer (Fig. 5), when nor­ mally a phosphate surplus is found due to faster P- carbon Phytoplankton remineralization. H g/l m on thly Medians Additional data from the whole German Bight give more insight into the effects of Elbe river floods, namely 300 their influence on vertical density stratification and the 250 resulting growth conditions for phytoplankton. Figure 8 200 shows results from a RV “Gauss” cruise on 17-26 150 August 1981, just after the summer flood events of the 100^ Elbe river. On this cruise, a grid of stations as close as 50t five nautical miles to each other was visited (10 miles for biological and chemical parameters). The Elbe water outflow and a long period of calm weather had caused an Years 1980 - 1990 intensely stratified water mass (Fig. 8, as the density Figure 6. Phytoplankton, diatom, and flagellate biomass at difference Aat between the surface and bottom water Helgoland Roads (1980-1990), monthly medians. samples).

At the edges of this stratified water body, extending in N/P-Quotient, N03-N / P04-P a northwest direction throughout the whole German N/P Ratios of m onthly Medians Bight, large blooms of the dinoflagellate Ceratium furca 300 n were found. The southern bloom obviously had spread out as far as Helgoland (where it has been described by Gillbricht (1983); however, without taking into con­ 200 sideration its origin). In the stratified water, very low phosphate concentrations (<0.1^mol/l) were found. As also silicate was depleted, a previous diatom bloom must 100 have consumed the nutrients. Though the light con­ ditions were favourable for plankton blooms within the stratified water, the nutrient exhaustion might have restricted the extension of the Ceratium blooms to the Years 1980 - 1990 frontal zones. Figure 5. Nitrate-nitrogen to phosphate-phosphorus ratios at In the southern Ceratium bloom area in August 1981 Helgoland Roads (1980-1990). Monthly median values. (Fig. 8), a highly significant negative correlation be-

254 Elbe River Discharge bodies off the river estuaries are too turbid to sustain m 9/se c large phytoplankton blooms, though nutrients are in 3500 q good supply. Farther north and northwest, light con­ 3000- ditions in the water column improve, mainly under the 2500 influence of salinity stratification and sedimentation of riverborne seston. Nutrient concentrations decline as 2000 phytoplankton production of the water column in­ 1500- creases. Such patterns are known from other coastal 1000- waters directly influenced by turbid river water (Cadée, 500 1978) and can be detected by remote sensing from satellites (e.g. Szekielda, 1982; Aarup eta l., 1990). To trace the point where phytoplankton growth starts in the German Bight, after the low salinity and bad light Elbe River Discharge climate prevented marine phytoplankton growing in the Elbe estuary itself, the deviation of nutrient versus salinity plots from a linear relationship was analysed (Hickel, unpublished data from several cruises in the Helgoland Bight). During the phytoplankton growth season, this point where fast growing marine phyto­ plankton changes the nutrient/salinity regression by nutrient uptake was found mostly at a salinity between S = 28 and 29. This is the salinity at which Cadée (1978) found maximum production rates in the Zaire river plume and also from the Ems estuary. The S = 28 Years 1980 - 1990 isohaline is normally found close to Helgoland. Until the bloom is fully developed, the northgoing residual cur­ Figure 7. Elbe river discharge volumes (1980-1990). Single daily values (upper), cumulative volumes, January-August, rent will have carried it to positions north of Helgoland. lower graph. The interpretation of plankton stocks in relation to nutrients from the Helgoland data is thus limited by the fact that the phytoplankton could originate from distant growing centres well away from Helgoland. The residual tween Ceratium numbers and phosphate concentrations current, going normally from south to north (Hickel, was found in the upper layer. This indicated that the 1980), can reverse in certain wind conditions, bringing Ceratium population was actively taking up phosphate. watermasses from the northern German Bight with their Therefore, the rising phosphate levels (and possibly larger plankton populations to Helgoland. These popu­ other growth-enhancing substances) in the western fron­ lations might have profited earlier from the eutrophica­ tal zone might have been the reason for the occurrence tion of the German Bight, but this might not be evident there. from Helgoland data. Large freshwater quantities might support phyto­ Discussion plankton blooms first by increased density stratification, with the resulting improvement of light climate, and In the German Bight, phytoplankton blooms have often then by additional nutrient supply in the outer German been found associated with hydrographic frontal sys­ Bight. To prove these effects, more horizontal surveys tems (Krause eta l., 1986). The convergence zone of the of the sort given in Figure 8 are needed, in addition to German Bight (Goedecke, 1968) is a typical site of such the continuing of the Helgoland time-series measure­ blooms, and Figure 8 is a good example of blooms in ments. The latter should be continued by all means, as frontal systems. Repeatedly, large phytoplankton no other sampling scheme in a better suited area of the blooms have also been found north of Helgoland within German Bight could possibly be conducted at such a the north Frisian coastal water, e.g. diatom blooms in high sampling frequency and low cost. It should now be the years 1987 and 1988 (Hickel et al., 1989; Bauerfeind self-evident that man-made changes versus the notori­ et al., 1990). Such blooms will not always be found by the ously high natural variability in the inner German Bight Helgoland Roads sampling scheme, but they can drift to can only be separated by time-series measurements of Helgoland during certain wind directions. From the this kind. hydrographical structure of the German Bight it can thus Comparing the Helgoland time-series data with other be understood why an additional eutrophication effect long-term plankton records, the continuous plankton on phytoplankton need not be detected at the Helgoland recorder (CPR) data might first be considered. Recent monitoring station: the shallow, turbulent coastal water changes in the summer plankton of the North Sea

255 30'

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Figure 8. Density stratification (right) and Ceratium furca concentrations (left) in the German Bight in August, 1981 (following an Elbe river flood event in July/August). The water density stratification is given as the density difference Atrt between the surface and the bottom water; Ceratium numbers are mean values (in 103 cells/1) of the upper 10 m layer (three sample depths). Elbe Discharge at Neu Darchau Carbon Phytoplankton 1976-86 m 3/s e c Pg/1 monthly Medians 1987-88 3500-q 350 T 3000- 300- 2500- 250

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Figure 9. Elbe river water discharge at Neu Darchau, nutrients and phytoplankton at Helgoland in 1987 and 1988, as compared with long-term average values. (Dickson et al., 1991) comprised largely increased Cera­ in the German Bight, where recurrent patterns are hard tium abundance in the north-central North Sea along to recognize. To improve this knowledge, and to relate with increased stratification of the water column. The the German Bight data with open North Sea data as preference of Ceratium spp. for stratified water is well documented by the CPR, the Helgoland plankton data known. A westward extension of the Jutland coastal will be reevaluated in more detail (e.g. for Ceratium water may have supported the observed smaller increase species), together with the numerous (partly unpub­ of Ceratium spp. during the late 1980s in the German lished) data on horizontal quasisynoptic surveys of the Bight, according to these authors. The Helgoland data whole German Bight. failed to show this increase, or an earlier occurrence of Among the much discussed potential effects of eutro­ dinoflagellate blooms in the year-cycle as found in the phication are the oxygen depletion events 1981-1983 in open North Sea, though the salinity decrease and nutri­ bottom water of the southeastern North Sea associated ent increase by the Elbe river floods in 1987 and 1988 with mass mortality of benthic animals (von Western­ were well documented. Only the 1981 blooms after the hagen and Dethlefsen, 1983; von Westernhagen et al., unusual extension of a stratified water zone in the 1986). The possible sources and the effects on the German Bight confirm the views of Dickson et al. bottom fauna were subsequently investigated (Hickel et The extensive literature on phytoplankton changes in al., 1989). Besides the obviously dominating role of the North Sea on the basis of CPR data (e.g. Radach, water column stratification during calm weather 1984 for a review) does not cover most of the coastal periods, a contribution of the large phytoplankton water of the North Sea adequately. This narrow and blooms of these years (Fig. 6) to the organic detritus load eutrophic water body off the Dutch and German coasts and thus oxygen consumption in the bottom water would is separated from the open North Sea by frontal systems be likely; however, the data from the respective years (see Otto et al., 1990, for a review), and a response of were not sufficient to prove this in a particular case. Only phytoplankton populations different to those in the in 1989 were low oxygen concentrations again found in open North Sea should not be surprising. Long-term the bottom water of the northern German Bight (north changes within this coastal water are monitored by the of Sylt) and the Danish coastal waters of Horns Rev Marsdiep time series (Cadée, 1988, 1991), besides the (Niermann, 1990); this might have been the result of Helgoland Roads time series. plankton blooms which escaped detection by the Helgo­ In the westernmost Dutch Wadden Sea, the Marsdiep land Roads sampling scheme. area, the Rhine water influence is a more stable and predictable factor than the Elbe river influence is for Helgoland. The Rhine water keeps close to the Dutch Acknowledgments coast, where its quantities are positively correlated with The plankton counts of the earlier years (up to 1975) phytoplankton biomass (Gieskes and Schaub, 1990). were contributed by Dr E. Hagmeier. The nutrient The increase in phytoplankton in the Marsdiep area has analyses were carried out by Mr P. Mangelsdorf. We been described in many papers by Cadée, both as would like to thank them for their long standing co­ increased primary production (Cadée, 1986) and phyto­ operation. We also thank two reviewers for their valu­ plankton abundance (Cadée, 1991), but this increase able critique. was due to non-diatom plankton, particularly Phaeocys- tis globosa. This species is rarely a major component of the Helgoland phytoplankton biomass, though it regu­ References larly occurs there. The main blooms of Phaeocystis are found more in the east Frisian and north Frisian coastal Aarup, T., Groom, S., and Holligan, P. M. 1990. The process­ ing and interpretation of North Sea CZCS imagery. Neth. J. waters close to the coast. Sea Res., 25(1/2): 3-9. The Elbe river water, discharging only about one- ARGE Elbe Arbeitsgemeinschaft für die Reinhaltung der third of the Rhine river volume, is at normal discharge Elbe. 1990a. Wassergütedaten der Elbe. Zahlentafeln rates transported to the North between Helgoland and (yearly reports), 1982-1990. ARGE Elbe, 1990b. Gewässergütebericht 1985-1990. the peninsula of Eiderstedt, but after high river dis­ ARGE Elbe, 1990c. Nährstoffstudie der Elbe. Wasser­ charge or strong easterly winds, the Elbe river water gütestelle Elbe, Hamburg, 52 pp. plume will reach Helgoland. On the other hand, it has Bauerfeind, E., Hickel, W., Niermann, U., and Western­ been mentioned before that occasionally reversed resi­ hagen, H. von. 1990. Phytoplankton biomass and potential dual surface current flow can carry plankton bloom nutrient limitation of phytoplankton development in the southeastern North Sea in spring 1985 and 1986. Neth. J. Sea patches from the northern German Bight to Helgoland, Res., 25(1/2): 131-142. adding to the variability of plankton time series at the Cadée, G. C. 1978. Primary production and chlorophyll in the Helgoland Roads station. Zaire river, estuary and plume. Neth. J. Sea Res., 12(3/4): The review of Reid et al. (1990) shows the complexity 368-381. Cadée, G. C. 1988. Increased phytoplankton primary pro­ of phytoplankton dynamics in the North Sea. The plank­ duction in the Marsdiep area (western Dutch Wadden Sea). ton distribution is even more complex in time and space Neth. J. Sea Res., 20(2/3): 285-290.

258 Cadée, G. C. 1991. Phytoplankton variability in the Marsdiep, Niermann, U. 1990. Wieder Sauerstoffdefizit in der südlichen 1980-1990. ICES CM 1991/Variability Symposium, No. 14, Nordsee. Biologische Anstalt Helgoland, Jahresbericht Mariehamn. 1989: 107-110. Dickson, R. R., Colebrook, J. M., and Svendsen, E. 1991. Otto, L., Zimmerman, J. T. F., Furnes, G. U., Mork, M., Recent changes in the summer plankton of the North Sea. Saetre, R., and Becker, G. 1990. Review of the physical ICES CM 1991/Variability Symposium, No. 16, Mariehamn. oceanography of the North Sea. Neth. J. Sea Res., 26(2-4): Gerlach, S. A. 1990. Stickstoff, Phosphor, Plankton und Sauer­ 161-238. stoffmangel in der Deutschen Bucht und der Kieler Bucht. Radach, G. 1984. Variations in the plankton in relation to Abschlussbericht über ds Vorhaben “Eutrophierung der climate. Rapp. P.-v. Réun. Cons. int. Explor. Mer, 185:234— Nord- und Ostsee”. Ber. Umwcltbundesamt, 4/90: 1-357. 254. Gieskes, W. W. C., and Schaub, B. 1990. Correlation of the Radach, G., and Berg. J. 1986. Trends in den Konzentrationen seasonal and annual variation of phytoplankton biomass in der Nährstoffe und des Phytoplankton in der Helgoländer Dutch coastal waters of the North Sea with Rhine river Bucht (Helgoland Reede Daten). Ber. Biol. Anst. Helgo­ discharge. Coastal Estuarine Studies, 36: 311-320. land, 2: 1-63. Gillbricht, M. 1983. Eine “red tide” in der südlichen Nordsee Radach, G., Berg, J., and Hagmeier, E. 1990. Long-term und ihre Beziehungen zur Umwelt. Helgoländer Meeres- changes of the annual cycles of the meteorological, hydro- unters., 36: 393-426. graphic, nutrient and phytoplankton time series at Helgoland Gillbricht, M. 1988. Phytoplankton and nutrients in the Helgo­ and FV Elbe 1 in the German Bight. Cont. Shelf Res., 10(4): land region. Helgoländer Meeresunters., 42: 435^167. 305-328. Goedecke, E. 1968. Über die hydrographische Struktur der Radach, G., and Bohle-Carbonell, M. 1990. Strukturunter­ Deutschen Bucht im Hinblick auf die Verschmutzung in der suchungen der meteorologischen, hydrographischen, Konvergenzzone. Helgoländerwiss. Meeresunters., 17: 108— Nährstoff- und Phytoplankton-Langzeitreihen in der Deut­ 125. schen Bucht bei Helgoland. Ber. Biol. Anst. Helgoland, 7: Grasshoff, K., Ehrhardt, M., and Kremling, K. (Eds) 1983. 1-425. Methods of seawater analysis. Verl. Chemie, Weinheim, Reid, P. C., Lancelot, C., Gieskes, W. W. C., Hagmeier, E., 419 pp. and Weichart, G. 1990. Phytoplankton of the North Sea Hagmeier, E. 1961. Plankton-Äquivalente. Kieler Meeres­ and its dynamics: a review. Neth. J. Sea Res., 26(2-4): 295- forsch., 17: 32-47. 331. Hickel, W. 1980. The influence of Elbe River water on the Szekielda, K. H. 1982. Investigations with satellites on eutro­ Wadden Sea of Sylt (German Bight, North Sea). Deutsche phication of coastal regions. In Transport of carbon and Hydrogr. Z., 33(2): 43-52. minerals in major world rivers, pp. 13-37. Ed. by E. T. Hickel, W., Bauerfeind, E., Niermann, U., and Western­ Degens. SCOPE/UNEP Sonderbd. Mitt. geol. paläontol. hagen, H. von 1989. Oxygen deficiency in the south-eastern Inst. Univ. Hamburg 52. North Sea: Sources and biological effects. Ber. Biol. Anst. Westernhagen, H. von, and Dethlefsen, V. 1983. North Sea Helgoland, 4: 1-148. oxygen deficiency 1982 and its effects on the bottom fauna. Krause, E. G., Budeus, G., Schaumann, K., and Hesse, K. Ambio, 12: 264-266. 1986. Frontal systems in the inner German Bight and their Westernhagen, H. von, Hickel, W., Bauerfeind, E., Nier­ physical and biological effects. In Marine interface ecohydro- mann, U., and Kröncke, 1. 1986. Sources and effects of dynamics, pp. 119-140. Ed. by J. C. J. Nihoul. Elsevier, oxygen deficiencies in the south-eastern North Sea. Ophelia, Amsterdam. 26: 457—473.

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