Fig. 3 Hovmöller diagrams (years 1948-2003 versus is the southeastern part of the Southern Bight of the North months) of the Phytoplankton Colour index (PCI) in the Sea, directly off The Netherlands North Sea. For region location see Fig. 1b. Rectangle 'Ow'

pattern is in contrast with a high frequency of occurrence of Phaeocystis and its long season of presence before 1955. After 1995 the Phaeocystis season was again longer, an observation confirmed by Breton et al. (2006) who described the Phaeocystis record since 1988 off the Belgian coast, and by the Phaeocystis record of Philippart, Cadee and van Iperen (not published) that covers the period 1975-2006.


The distribution map of Phaeocystis presented here can hardly be improved, not even by ocean colour remote sensing: the frequent cloud cover over the North Atlantic hinders satellite-borne observations, but not the CPR survey. Also, the pigment signature of Phaeocystis is not very specific (Antajan et al. 2004) so the absorption spectrum and therewith the light reflectance hardly differs from that of other fucoxanthin- and fucoxanthin-derivative-containing phytoplankton groups, frustrating remote distinction of this particular species group. Without the survey it would not have been possible to construct the detailed year-month diagrams spanning many decades; those of low but persistent Phaeocystis occurrence in spring far offshore in the mid-Atlantic regions (Fig. 2) and in the Atlantic water of the northern North Sea, in areas C1 and C2 (Fig. 2) are probably the most unexpected. Not only in neritic water but apparently also in the open Atlantic, far away from anthropogenic nutrient sources (eutrophication), environmental conditions are clearly quite suitable for lifecycle development from single cells to colonies (the only stage recorded during the CPR survey).

Even so, changes in eutrophication have often been invoked to explain variation in Phaeocystis abundance and length of the season of blooming and occurrence, but this interpretation has not been satisfactory in view of the restricted number of stations, often limited to just one (Hickel et al. 1996; Cadee and Hegeman 2002). Breton et al. (2006), who also used observations at a single

Fig. 4 Hovmoller diagrams of chlorophyll-a concentration on a section perpendicular to the Dutch coast starting from the city of Noordwijk (just north of the river Rhine outflow), at 2, 10, 20 and 70 km from the coast. Notice the gradual shift of the start of the vegetative season to an earlier date at all four stations

Fig. 4 Hovmoller diagrams of chlorophyll-a concentration on a section perpendicular to the Dutch coast starting from the city of Noordwijk (just north of the river Rhine outflow), at 2, 10, 20 and 70 km from the coast. Notice the gradual shift of the start of the vegetative season to an earlier date at all four stations station (off Belgium), drew attention to the influence of larger-scale phenomena, namely the North Atlantic Oscillation that governs climate. Much earlier, an analysis of CPR survey results obtained in the same area had revealed trends of Phaeocystis (Gieskes and Kraay 1977a) that did not simply follow the eutrophication trend (Philippart et al. 2000): a decrease of Phaeocystis frequency of occurrence in the 1960s and early 1970s, a period when anthropogenic nutrient input in the southeastern North Sea increased.

The higher frequency of occurrence and longer growing season of Phaeocystis before 1965, when eutrophication was still quite low (Philippart et al. 2000), is particularly striking (Figs. 2, 5). Actually, colony abundance was already reported to be extensive more than 80 years ago (Savage 1930). This also suggests that Phaeocystis abundance is not determined by anthropogenic nutrient input only. On the other hand, phytoplankton biomass in general has always suggested a direct relation with eutrophication (Cadee and Hegeman 2002). Also in our study a relationship can be established between chlorophyll concentrations measured off the Dutch coast (Fig. 4) and river run-off

(not shown), which confirms previous findings by Schaub and Gieskes (1991); recently Breton et al. (2006) have also pointed out this link. Increased nutrient availability of North Sea coastal waters after high freshwater fluxes following periods of heavy rainfall (a response to the North Atlantic Oscillation, cf. Breton et al. 2006) in the catchment area of the continent's rivers clearly sets the stage for phytoplankton abundance in the southeastern North Sea. Such a batch culture-like response to nutrient enrichment (light is apparently not limiting primary production here) can be observed to the present day (Fig. 4). It can readily be explained by nutrient flushed out from the agricultural lands along the continent's rivers, and probably also resuspension of nutrient-rich bottom sediment when river flow is rapid after heavy downpours upstream; Schaub and Gieskes (1991) stated that phytoplankton biomass near the Dutch coast can be predicted on the basis of meteorological data on precipitation, which has now also been suggested for Belgian coastal waters by Breton et al. (2006). There is a suggestion of a gradual shift of the start of the growing season to an earlier date in the southern North

Fig. 5 Hovmöller diagrams, years 1948-2003 versus months of the year of: (A) standard deviations of the phy-toplankton colour index (PCI), (B) standard deviations of Phaeocystis occurrence frequency, data averaged over North Sea regions C1, C2, D1 and D2 (cf. Fig. 1a). and (C)

cumulative sum (see "Materials and methods" section) plots of mean phytoplankton colour index (PCI, in gray) and Phaeocystis frequency of occurrence (black) for the same region

Sea (Fig. 4). Whether or not this is the consequence of a slight but gradual warming of southern North Sea waters remains to be shown.

The Phaeocystis component of the phytoplank-ton is not necessarily related to river-induced eutrophication: long-term changes of Phaeocystis are quite different from those of the phytoplank-ton (as Phytoplankton Colour index PCI, i.e. chlorophyl, in the "Materials and methods" section) in general (Fig. 5). As we have seen above, environmental conditions in open ocean water, not necessarily those of coastal waters, promote colony development from single cells. Atlantic water inflow into the North Sea may therefore well be an important factor for the development of Phaeocystis in the southern North Sea, a suggestion made earlier for phytoplankton in general by De Jonge et al. (1996) and De Jonge (1997). The inflow of Atlantic water into the North Sea through the Dover Straits has unfortunately never been monitored over longer periods; it has usually been no more than deduced, e.g. from the potential induced in submarine cables by the water flow (Prandle 1978), most often by constructing hydrodynamic models that simulate currents on the basis of tides, wind stress over the North Sea and freshwater input (Salomon et al. 1993; Laane et al. 1996; Skogen and S0iland 1998; Siegismund 2001). Rather sudden changes in climate-ocean interactions that influenced regime shifts in North Sea ecosystem components took place in the late 1970s, late 1980s and late 1990s (Weijerman et al. 2005). The long-term changes in Phaeocystis described here (Fig. 5) do not correspond well with these regime shift periods, probably because both variability in the mix of nutrient sources in the southern North Sea and in the sampling route of the plankton recorders do not allow corresponding biological and hydrog-raphical observations.

Phaeocystis has been reported to accumulate preferentially far offshore, not on the coast, in the southern North Sea in the 1920s (Savage 1930). Later, Gieskes and Kraay (1977b) also described preferential abundance offshore. According to Brunet et al. (1996) accumulation on French beaches of the British Channel is the effect of eastward transport of offshore Phaeocystis blooms, not of in situ growth. The line of increased abundance off the southern coasts of Greenland, in the region of the front between the extension of the North Atlantic current in the Irminger Sea and the East Greenland current (Fig. 1b), may be explained in these terms. In view of the current system the Phaeocystis distribution here suggests advection from the Denmark Straits or even from the west coast of Iceland (regions not covered by the CPR survey), where Phaeocystis has been reported to be abundant (Thordardottir and Astthorsson 1986; Ste-fansson and Olafsson 1991). The total absence of colonies since 1985 can be explained simply (albeit speculatively) by assuming a shift in the front to an area outside the plankton recorder routes.

Offshore accumulation of Phaeocystis along frontal zones as suggested here may well be a more general phenomenon; in the southern North Sea it would explain an apparent dependence on the inflow of Channel/Atlantic water through the Dover Straits, a source of nutrients in this region that can be more important than local river sources of nutrients (Radach and Lenhart 1995; Laane et al. 1996; De Jonge et al. 1996; De Jonge 1997). The high Phaeocystis abundance far off the Netherlands, all the way between Holland and England in 1925 and 1926 (Savage 1930), can be understood in this light. The Atlantic Ocean water mass entering the North Sea from the southeast forms a front with the coastal water off the coasts of Belgium and the Netherlands. Interestingly, part of the decrease of Phaeocystis abundance in the CPR record in the 1960s and 1970s may be explained by a change of the position of the front, in line with the suggested front shift south of Greenland that may have brought Phae-ocystis out of the reach of the CPR survey in that region. In the southeastern North Sea the sampling route of the CPR survey has remained the same geographically while the coastal water/ ocean water front has shifted up to 20 km eastward to shallow Dutch coastal waters since the gradual man-made closure of the estuaries in the south-estern Netherlands following the catastrophic storm surge of 1953 (J. de Kok and L. Villerius, Rijkswaterstaat-RIKZ, pers. comm.).

Wind forcing may of course broaden the Rhine plume considerably, especially when winds from the east persist (Gieskes 1974). Wind forcing, later often suggested to be a dominant factor in setting the stage for water mass distribution and flow in the North Sea (Salomon et al. 1993; Laane et al. 1996; Smith et al. 1996; Pingree 2005), is a parameter with a long-term measurement record at many meteorological stations along the coasts. Exploitation of such data to hindcast and predict large-scale current patterns would enhance and improve existing models to estimate inflow of Atlantic Water through the Dover Straits. These models currently produce contradictory results, and no trend has so far been revealed (Otto et al. 1990). Low phytoplankton abundance in the North Sea and a late spring bloom and changes in other ecosystem components between the mid 1970s and the late 1980s have been ascribed to a cold-water period considered to be the consequence of low Atlantic water inflow into the North Sea (Corten and van de Kamp 1992, 1996; Lindeboom et al. 1995; Taylor et al. 1998; Edwards et al. 2002; Weijerman et al. 2005). It is well known that biological responses may magnify changes in the physical or chemical environment, and the annual variation of Phaeocystis colony occurrence in the southeastern North Sea may well be an example of this concept.

Phaeocystis plays a key role in element fluxes relevant to climate (reviewed by Schoemann et al. 2005) and therefore the results presented here have implications for biogeochemical models of cycling of carbon and sulphur. Sea-to-air exchange of carbon dioxide (CO2) and dimethyl sulphide (DMS) has been calculated on the basis of measurements made during cruises in a single year. Manizzi et al. (2005) already issued a warning to prevent this practice. Thomas et al. (2004) presented CO2 fluxes in the southern North Sea based on measurements from August 2001 to May 2002 only. They concluded that coastal seas would take up 0.4 Pg C per year. In view of the large annual variation both in phytoplankton and in Phaeocys-tis abundance presented in this paper such extrapolations cannot be correct. Discrepancies noted by Thomas et al. (2004) with results obtained in the same area by Borges and Frankignoulle (2003) may well have been the consequence of diVer-ences in plankton activity between the years in which the cruises were carried out.

Acknowledgements Financial support from the Dutch Royal Academy of Sciences (KNAW) allowed W.W.C.G. to spend a sabbatical at the Sir Alister Hardy Foundation of Ocean Sciences in Plymouth (UK); the SAHFOS directory is gratefully acknowledged for generous hospitality. We thank the Dutch National Institute for Coastal and Marine Management (RIKZ) for access to their monitoring data through waterbase, and a group of students of Groningen University coached by Rob Middag for the analyses. Comments by two unknown referees and editing by Dr M.A. van Leeuwe have improved the manuscript considerably. We acknowledge the assistance of the reviewers, and of colleagues who inspected earlier versions of the manuscript.

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