The spring bloom of phaeocystis pouchetii (haptophyceae) in Dutch coastal waters

37 Netherlands Journal of Sea Research 20 (1): 37-48 (1986)

THE

SPRING

BLOOM

OF PHAEOCYSTIS POUCHETII DUTCH COASTAL WATERS*

(HAPTOPHYCEAE)

IN

M.J.W. VELDHUIS 1, 2, F. COLIJN 1 and L.A.H. VENEKAMP 1, 2 1 Department of Marine Biology, University of Groningen, P.O. Box 14, 9750 AA Haren, The Netherlands 2 Netherlands Institute for Sea Research, P.O. Box 59, 1790 AB Den Burg, Texel, The Netherlands

ABSTRACT A Phaeocystis pouchetii (Harlot) Langerh. bloom,

which contained up to 22x10s cells odm-3, occur. red in the spring of 1984 along the Dutch coast of the North Sea. The largest cell numbers of P. pouchetii were observed near the coast, with cell numbers decreasing towards the open sea. In contrast to a sharp peak in the cell numbers along the coast in May, P. pouchetii cell numbers in the open sea slowly increased towards June. During a preceding bloom of diatoms, P. pouchetii was already present from an early stage onwards while at the end of the P. pouchetii bloom a high percentage of the cells was observed as microflagellates. The distribution of dissolved nutrients (Si, N, P) showed a typical pattern with highest values near the coast, apparently due to the Rhine outflow, and a gradual decrease towards the open water. This distribution pattern coincided with particular stages of the P. pouchetii bloom. Whereas growth of the P. pouchetii population may be due to increasing temperature and irradiance, its decline is probably caused by phosphate limitation. Total primary production measured at one station and based on short term 14C incubation ex. periments was 121 gC.m -2 for the period 17 March to 20 May with a daily rate of production of up to 4.8 gC.m-2. The mean proportion of extracellular carbon release based on 4 h incubation periods was 7.5%.

1. INTRODUCTION Reports of mass development of the colony forming haptophycean phytoplankton alga Phaeocystis pouchetii (Harlot) Lagerh. in the

North Sea are given by SAVAGE (1930) while referring to the possible negative effects on herring fisheries. It has also been reported from polar, North Atlantic and North Pacific regions (KASKIN, 1963; BOUGARD, 1979). The species was also isolated from warmer areas (GUlLLARD & HELLEBUST, 1971; ATKINSON et al., 1978; HALLEGRAEFF, 1983). This distribution pattern fits into KASKIN'S (1963) characterization of P. pouchetii as a stenohaline eurythermal algal species. However, there is still uncertainty whether all these observations refer to the same species (PARKEet al., 1971; CADEE & HEGEMAN, 1986). Dense P. pouchetii blooms were recently observed along the North Sea coast of Belgium (LANCELOT, 1984), the Netherlands (CAD~E & HEGEMAN, 1974, 1979; GIESKES & KRAAY, 1975, 1977; COLIJN, 1983), Germany (MICHAELIS, personal communication; EBERLEIN et al., 1985; WEISSE et al., 1984) and the English Channel (BOALCH,1984). The massive P. pouchetii populations are generally observed shortly after a diatom peak and characterized by rapid growth, resulting in large colonies (up to 15 mm) followed by disintegration of these colonies, a phenomenon which may occasionally give rise to large quantities of foam on the beaches. This phenomenon is often interpreted as a result of ongoing eutrophication. In this paper we decribe the development of a P. pouchetii bloom along the Dutch coast in the spring of 1984. The study aims at elucidating the factors that accompany growth and decline of this alga and at quantifying the contribution of this species to the annual primary production. This paper is one in a longer series on the ecology of Phaeocystis (cf. VELDHUIS & ADMIRAAL, 1985; VELDHUIS et al., 1986).

*Publication no. 6 of the project Ecological Research of the North Sea and Wadden Sea (EON).

38

SPRING BLOOM OF PHAEOCYSTIS

Acknowledgements--The authors wish to thank the crew of R.V. "Aurelia" for assistance during the work at sea, the technicians of the Dutch Government Institute of Sewage and Industrial Waste Treatment (RIZA) for their analysis of the nutrients, A. Kop for counting the bacteria and G. Kamstra for his technical assistance. Winfried Gieskes, Wim Admiraal and Chris van den Hoek critically read and improved the manuscript. This investigation was supported by the Foundation for Fundamental Biological Research (BION), which is subsidized by the Netherlands Organization for the Advancement of Pure Research (ZWO). 2. MATERIAL AND METHODS 2.1.

WATER

SAMPLING AND MEASUREMENTS

CHEMICAL

The route of R.V. "Aurelia", with the sampling stations is shown in Fig. 1. Six cruises were carried out on 19 March, 9 and 24 April, 5 and 15 May and 12 June 1984. At each sampling station surface water temperature and salinity were measured. The underwater irradiance was measured with 4o'

5°

__6_~ (~

40'

D C

/

D /

/"

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S~

I~

~,.

a LICOR underwater quantum sensor (Ll-192s). Measurements at different depths were used for the calculation of the vertical irradiance attenuation coefficient (Kd) (COLIJN, 1982). All water samples were taken from the surface. Samples for analysis of chlorophyll a were collected by filtration (GF/C); they were immediately frozen until further analysis, according to the method of LORENZEN (1967), within one week after sampling. The samples for dissolved inorganic nutrients were collected after membrane filtration (Sartorius SM 11106, 0.45 #m) and also frozen. The samples for ammonia, nitrite, nitrate and phosphate were analyzed by RIZA (Dutch Government Institute of Sewage and Industrial Waste Treatment) by a Technicon autoanalyzer method. Reactive silicate was analyzed immediately on board by the method of STRICKLAND & PARSONS (1972); samples and standards were measured the next day. For the identification of the phytoplankton species, 500 ml-large samples were taken and preserved with Lugol (KJ(J2) buffered with Na-acetate). P. pouchetii cells were counted after concentrating, by the Uterm0hl sedimentation technique (UTERMOHL, 1958), with an error of <10%. Samples for bacteria were preserved with formalin (81.2 ml sample with 10 ml 37% formalin). Bacterial numbers were counted by epifluorescence microscopy (HOBBLE et al., 1977). 2.2. INCUBATION EXPERIMENTS One-litre samples of all stations from the first survey were incubated at 11°C and 100 #E.m-2.s -1 at a 12:12 light/dark cycle; these samples were inspected every 2 to 3 days to test whether P. pouchetii cells or colonies were present. 2.3. PRIMARY PRODUCTIVITY MEASUREMENTS

/

(T

/ ~B

/

Fig. 1. Map of the area studied, position of the sampling stations and division into 4 sub-areas.

For the primary production measurements a sample of 1000 liter was taken at station 8 at each survey. It was then shipped to the institute. Here 20-ml-large subsamples were incubated in a small volume incubator (LEWIS & SMITH, 1983). These volumes proved to be adequate for 140 incubations (VELDHUIS& ADMIRAAL, 1985). The irradiances used were: 0, 19, 53, 81, 168, 390, 473, 643, 946 and 1706 #E.m-2-s -1, provided by an Osram metallogen HMI lamp. The added amount of NaH14CO3 was 125 #Ci per litre. After 2, 4, 6 and 8 hours incubation at each irradiance sub-

SPRING BLOOM OF PHAEOCYSTIS

39

TABLE 1 List of dominant algal species observed during the spring of 1984 in the 4 areas A to D. Area

A

B

C

D

Survey 1 (19 March)

Plagiogramma brockmanni Skeletonema costatum Asterionella kariana

P. brockmanni S. costatum A. kariana

P. brockmanni S. costatum A. kariana

P. brockmanni S. costatum A. kariana

Survey 2 (9 April)

P. brockmanni S. costatum A. kariana Chaetoceros sp.

P. brockmanni P. brockmanni S. costatum S. costatum A. kariana A. kariana Chaetoceros sp.

P. brockmanni S. costatum

Survey 3 (24 April)

Chaetoceros socialis Phaeocystis pouchetii

C. socialis S. costatum P. pouchetii

Rhizosolenia stolterfothii Rhizosolenia delicatula P. pouchetii

R. stolterfothii R. deficatula P. pouchetii

Survey 4 (5 May)

P. pouchetii

P. pouchetii

P. pouchetii

P. pouchetii

Survey 5 (15 May)

P. pouchetii

P. pouchetii

P. pouchetii

P. pouchetii

Different diatom species

R. delicatula R. stolterfothii Nitzschia sp.

R. delicatula R. stolterfothii

P. pouchetii

Survey 6 (12 June)

P. pouchetii

samples were filtered (Sartorius SM 11106, 0.45 /~m) with a gentle filtration pressure (<100 mm Hg). Filters were counted in a liquid scintillation counter (Packard Tricarb 460 CD) after 0.8 ml propylacetate and 5 ml Instagel II had been added. The amount of organic compounds released by the phytoplankton in the medium was estimated after removal of the inorganic bicarbonate. For that purpose, in duplicate, 5 ml filtrate samples were acidified (pH = 2 with 6% H3PO4) and purged with air for 30 minutes. The radioactivity in the filtrates was counted after a twofold volume of Instagel II had been added. The measurements of the P versus I relationship, together with the irradiance measured continuously at the NIOZ (Texel) with a Kipp solarimeter, and the mean underwater irradiance attenuation (Table 2) were used for the calculation of the daily and seasonal primary production and extracellular release at station 8, according to COI_IJN (1983). 3. RESULTS 3.1. HYDROGRAPHY OF THE SAMPLING AREA Due to strong tidal currents the Southern Bight of the North Sea must be regarded as a vertically

N. species

completely mixed water mass (CREUTZBERG & POSTMA, 1979). Detailed information on the currents and water masses along the Dutch North Sea coast is given by LEE (1970) and VAN BENNEKOM et al. (1975). Two major types of water masses occur in the area investigated. The first water type is characterized by oceanic water with a high salinity ( - 3 5 ) entering through the Channel. The second water type, with a much lower salinity, is found near the coast. It is a mixture of oceanic water and fresh water supplied by rivers. The patterns of isohalines found during 6 surveys (Fig. 2) are similar to those presented in GIESKES & KRAAY (1975, 1977). Based on the salinity distribution, differences in nutrient concentrations and P. p o u c h e t i i cell numbers, the area was divided into 4 sub-areas (Fig. 1) which can be characterized as follows: area A, situated in the river Rhine plume, with a low salinity ( - 3 3 ) and a high input of nutrients. The second, coastal area B is comparable with the first except for the maximal P. p o u c h e t i i Cell numbers, which are lower. Area D contains a water mass characteristic of the open sea with high salinity and low nutrient concentrations, while area C can be regarded as an intermediate between area C and D. In Fig. 3 the surface water temperature of all stations is given. It shows a gradual-increase from 6 to 14°C with slightly

40

M.J.W. VELDHUIS, F. COLIJN & L.A.H. VENEKAMP

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3.2. SPATIAL AND TEMPORAL DISTRIBUTION OF T H E PHYTOPLAN KTON

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Fig. 3. All data on surface water temperatures (°C). Dots represent surface samples taken at the various stations and the dotted line represents the mean of these values.

In Table 1 a list of d o m i n a n t algal spemes is given for the 4 areas. At the start of the spring bloom o n l y d i a t o m s were observed, but after inc u b a t i o n of s a m p l e s from all s t a t i o n s in the laboratory P. p o u c h e t i i cells and c o l o n i e s were found w i t h i n one week, except for the w a t e r from s t a t i o n s 6 and 11. Up to the third survey an increasing n u m b e r of d i a t o m s was found, a l t h o u g h there are differences b e t w e e n area B and the areas C and D due to the o c c u r r e n c e of R h i z o s o l e n i a species in the latter areas. At that time P. p o u c h e t i i started to develop vigorously, increasing both in cell numbers, c o l o n y numbers and c o l o n y size. The h i g h e s t cell n u m b e r s of this algal species were observed during the fourth survey, e x c e p t in area A, w h i c h had its peak at

SPRING BLOOM OF PHAEOCYSTIS

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Fig. 5. Percentages of microflagellates among total P. pouchetii cell numbers.

JULIAN OAY

JULIAN DAY I

80

• , ./•

80

60 ~o 16o ~" 12o ~o 16o ~.o

I

JUN

the total P. pouchetii cells. Up to the fourth Fig. 4. Changes of total Phaeocystis pouchetii cell survey (5 May) these cells formed less than 10% numbers (xl06.dm -3) with time in the 4 sub-areas. of the total cell numbers except for area D, but in

the decline phase a considerable increase was observed in all areas. the fifth survey (Fig. 4). The time of the peak of the P. pouchetii bloom corresponds with a peak in the chlorophyll a concentration (Fig. 6). A second increase in the chlorophyll a concentration in area B is due to a new diatom bloom which appeared after the Phaeocystis maximum. Meanwhile, in area D P. pouchetii further increased its cell numbers. Microscopic observations of the field material showed another cell type besides the large single cells and colony cells, which varied in average diameter from 7 to 9 #m. This small cell type varied in diameter from 3 to 5 #m and closely resembled the socalled microflagellates described for the first time by SCHERFFEL (1900) and later by KORNMANN (1955). Fig. 5 shows the percentage of this cell type of

32 28

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TABLE 2 Values observed for irradiance attenuation coefficients (Kd) at 5 dates in 1984. Date

19 9 24 1 15

March April April May May

K d (m - i)

0.336 0.361 0.434 0.731 0.666

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JULIAN DAY I

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Fig. 6. Concentrations in chlorophyll a in mg.m -3 at the successive sampling dates in the 4 sub-areas.

42

M.J.W. VELDHUIS, F. COLIJN & L.A.H. VENEKAMP TABLE 3

s.oo 2.50

2.501

2.00

2.001

~- 1.50

1.5o ]

Computed values for primary production and extracellular release for the period 17 March to 20 May 1984, based on 4 different incubation times.

Incubation time (h)

Prim. prod. (g C.m-2)

Extra rel. (g C.m-2)

Proportion (%)

2

162.1

13.9

7.9

4

111.7

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16.2 23.3

14.3 19.8

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Fig. 7 shows the distribution pattern of silicate in the 4 subareas. In all areas a decrease in the concentration was observed with time owing to the diatom bloom, but the concentrations in the coastal zone remained slightly higher than in the open sea. Inorganic phosphate (Fig. 8) showed a distribution pattern as for silicate, with high initial concentrations near the coast, due to the large phosphate load of the Rhine. At the time of the diatom bloom, preceding the abundance of P. pouchetii, there was a slight increase in the in-

I AREA A

1.00

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3.3. DISTRIBUTION OF NUTRIENTS

56

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Fig. 8. Concentrations of ortho-phosphate (/~mol.dm- 3) at the successive sampling dates in the 4 subareas.

organic phosphate concentration. However, at the time of the vigorously developing P. pouchetii population a rapid decline in the concentration of phosphate was observed. At the time of the bloom peak the concentration fell to AREA B' 0.08 #mol.dm - 3 and remained low during the decline phase. The initial concentrations of the 3 measured • %, • :'% • inorganic nitrogen compounds ammonia, nitrite %, and nitrate also decreased from the coast towards the open water (Fig. 9A, 9B, 9C). Near i"% the coast a rapid decline in the ammonia concentration during the diatom bloom occurred, whereas in the offshore region there was a slight t.|... : 6o-~o 1~o i~o 14o l~o 18o change. The seasonal fluctuations in nitrite and nitrate concentrations of all 4 areas showed a 'AREA D pattern almost similar to phosphate. Up to the third survey, the time of the maximal diatom numbers, an increase in both these nitrogen compounds was observed followed by a rapid decline at the time of the P. pouchetii peak. In contrast to phosphate these nitrogen compounds were slightly increasing again at the sixth survey.

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3.4. PRIMARY PRODUCTION AND EXTRACELLULAR RELEASE

(

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Fig. 7. Concentrations of reactive silicate (#mol.dm -3 at the successive sampling dates in the 4 sub-areas.

Fig. 10 shows the results of the primary production and extracellular release measurements of a

SPRING BLOOM OF PHAEOCYSTIS

' AREA

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Fig. 9c

o

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Fig. 9a. Concentrations of nitrogenous nutrients (in #mol.dm -3) at the successive sampling dates in the 4 sub-areas: NH 4 - N.

O.O0

~o 18o l~o 14o 1~o ]8o Fig. 9b. Concentrations of nitrogenous nutrients (in

l.qO

'AREA D

#mol.dm -3) at the successive sampling dates in the 4 sub-areas:

1,20

1.20

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O,80

~z 0.60

0.50

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Fig. 9c. Concentrations of nitrogenous nutrients in #mol.dm -3) at the successive sampling ates in the 4 sub-areas:

t

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Fig. 9b phytoplankton population dominated by diatoms and small P. pouchetii colonies (A) and that of one entirely dominated by large P. pouchetii colonies (B). In general, a decrease in the primary production rate with incubation time occured at all irradiances. Whereas the extracellular release in A paralleled that of the primary production, the extracellular release in the P. pouchetii material in B increased very rapidly after 4 hours of in-

NO 3 - N.

cubation. Apparently, the extracellular release of the full-grown P. pouchetii is more affected by a prolonged incubation time than that of diatoms and small colonies. The results of the measurements of the P-I curves together with the mean Kd values (Table 2) and measurements of daily irradiance are used for calculation of the daily primary production and extracellular release of the whole water column at station 8 (Table 3, Fig. 11). Table 3 shows that based on the data of a 2-hour incubation period, a higher seasonal primary production was found than with production based on longer incubation periods. For the extracellular release the opposite can be observed. Both these differences will affect the percentage of extracellular release (PER), which, therefore, varied from 7.5"to 19.8% during the spring season.

44

M.J.W. VELDHUIS, F. COLIJN & L.A.H. VENEKAMP

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Although viable P. pouchetii cells were already present at the first survey in most of the area investigated, the actual bloom formation was later with a higher water column irradiance and at a higher water temperature. Presumably growth conditions were still unfavourable for mass development at the first survey. Culture experiments (VELDHUIS, own observations), however, show that P. pouchetii is capable of vigorous growth and colony formation at a temperature of 4°C. In the winter of 1984-1985 water samples taken at the beach near station 13 revealed low numbers of P. pouchetii, both cells and colonies, at a water temperature of - 1 ° C (cf. CADI~E & HEGEMAN, 1986). These cells were capable of forming dense populations within one week after incubation at a temperature of 11°C and an irradiance of 100 #m E.m-2.s -1. These observations together with the occurrence of P. pouchetii in polar regions (IVERSON et al., 1979; EL-SAYED et al., 1983; PALMISANO & SULLIVAN, 1985) suggest that the low temperatures observed in early spring in the North Sea are not the ma-

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Fig. 10. Time course of particulate fixation (left graph) and extracellular release (right graph) of phytoplankton samples taken at station 8 during the 2nd (A) and 4th (B) survey, incubated at 4 irradiance levels, viz. 19 (@), 160 (O), 473 (V) and 1706 (V) # E-m-2.s -1.

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The bacterial counts are summarized in Fig. 13. Numbers ranged from 5-105x 108.dm -3 with peak values 10 days after the maximum in the P. pouchetii numbers. 4. DISCUSSION AND CONCLUSIONS Although the occurrence of P. pouchetii in the spring of 1984 was not strictly limited to the coastal region, the highest cell numbers were found in the areas directly influenced by the runoff of the rivers. These high cell numbers strongly suggest a causal relationship between high amounts of inorganic nutrients and the growth and biomass (yield) of P. pouchetii. However, a possible interference from unknown terrigenous compounds that might enhance the growth of P. pouchetii (JONES & HAQ, 1963; FOSTER et al., 1982) cannot be excluded.

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Fig. 11. Primary production and extracellular release (mg C.m-2.d -1) of samples taken at station 8, based on 4-hour incubation data (arrows indicate sampling data).

SPRING BLOOM OF PHAEOCYSTIS

jor limiting factor for mass development of P.

pouchetii at that time. Therefore, the diatom bloom which preceeds the Phaeocystis bloom must be due to the ability of diatoms to grow more rapidly at lower irradiances and temperatures than P. pouchetii. Howevei5 we cannot exclude the possibility that P. pouchetii of poiar waters is a physiologically different variety or even a different species (ELBR~.CHTER, personal communication). Several authors (FEDEROV & KUSTENKO, 1972; EPPLEY, 1977) have shown that organic substances are involved, both in interactions between phytoplankton species and in the succession of these. BOALCH (1984) mentions a possible, positive interaction of P. pouchetii with Chaetoceros, while CHU (1946) demonstrated that an organic phosphate compound (phytin) had a growth-stimulating effect on P. pouchetii. Further investigations on the influence of organic and inorganic phosphate on the growth and colony formation of P. pouchetii are in progress. The observed course in the dissolved inorganic phosphate concentration and the low values during the bloom of the alga strongly sug200

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45

gest that phosphate is the limiting factor. This was found earlier by VAN BENNEKOM et al. (1975), who described very high NIP ratios of over 50, suggesting that phosphorus and not nitrogen was the limiting factor (Fig. 12). We also calculated NIP ratios of >30. In contrast to our findings, LANCELOT (1983) observed nitrogen limitation in Belgian coastal waters of the Southern Bight of the North Sea. Substantial evidence for the limiting role of phosphate is given by the longer growth period observed and the timing of the peak values of P. pouchetii found later in area A than in B and C. The first area has a residual current pattern that enables a continuous replenishment of phosphate, and therefore results in the observed higher biomass yield of P. pouchetii. Towards the end of the bloom the large colonies disrupted and another cell type, the socalled microflagellates appeared. However, the areas differ: in the coastal zone the decrease in Phaeocystis colonies and total cell numbers coincided with an increase in the percentage of microflagellates, whereas in the more open water region a further growth of P. pouchetii was observed together with a decrease in the proportion microflagellates. Are these cells stages in a more complex life cycle of the alga or must they be regarded as survival cells? (KORNMANN, 1955). These cells capable of surviving temperatures above 15°C for a long period (KORNMANN, 1955) could also be an inoculum for later summer and autumn blooms of Phaeocystis (COLIJN, 1983; CADCE & HEGEMAN, 1986). Apart from limitation by nutrients, temperatures above 15°C also act negatively on the formation of colonies (unpublished results). The seasonal primary production we observed for station 8 is comparable with that reported by GIESKES & KRAAY (1975, 1977), who for the same area estimated a value of 130 g C.m -2 in the spring season with daily values of 2-3 g C.m -2 during a period with Phaeocystis. Daily values based on oxygen measurements (TIJSSEN & EYGENRAAM, 1982) amounted to -1.8 g C.m -2 Our calculated daily values at the peak of the Phaeocystis bloom are higher, ranging from 4-5 g C.m-2. The percentage of exudate release (PER) was not constant during the season but varied from 10% at the start up to 30% (based on an 8 h incubation period) at the end of the Phaeocystis bloom. Much higher values were observed by LANCELOT (1983) and slightly higher ones by COLIJN (1983), but similar values are

46

M.J.W. VELDHUIS, F. COLIJN & L.A.H. VENEKAMP i i • AREA

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Fig. 13. Total bacteria numbers ( x 108.dm -3) at successive sampling dates in the areas B and D.

reported by GIESKES & VAN BENNEKOM (1973). Recently VELDHUIS & ADMIRAAL (1985) have shown that these differences may well be caused by filtration artifacts. The time course pattern in Fig. 10 shows great differences in the amount of label in the particulate fraction and the extracellular organic compounds released in the medium. These data suggest differences in the physiology of the algae in the course of the bloom (LANCELOT, 1984; LANCELOT & MATH*T, 1985). In another paper (VELDHUIS et al., 1986) these results will be discussed in detail as well as their possible effect on the change in POC/PON ratio as observed by HICKEL (1984) during a Phaeocystis bloom. The extracellular material released may act as a carbon source for bacteria, and a peak in the bacterial numbers in area B was indeed found with a delay of two weeks after the peak of the Phaeocystis population (Fig. 13). This suggests that the exudates are degradable and LAANo BROEK et al., (1985) actually observed a high bacterioplankton production during the decline of the Phaeocystis bloom, which resulted in a maximum of the bacterial biomass 7 days after

the Phaeocystis peak. According to EBERLEIN et al., (1985), this delay between actual phytoplankton production and consumption by bacteria may be caused by antibiotic activity of the algae. We suggest that the abundance of the alga P. pouchetii in Dutch coastal waters depends on the amounts of nutrients available, based on a continuous input from rivers and advective mixing, while the inititation of the actual bloom may be the result of both the increasing irradiance and water temperature. A positive interference with the preceding diatom bloom cannot yet be proved (cf. BOALCH, 1984). The end of the bloom is probably initiated by phosphate limitation, as found earlier by VAN BENNEKOM et al., (1975), resulting in a change in the physiology of the Phaeocystis population, viz. an increase in the proportion of microflagellates (survival?) and a sudden decrease in large single cell and colony numbers. A further reduction of cell numbers might also be due to severe grazing by tintinnids, as was recently found by ADMIRAAL & VENEKAMP (1986). 5. REFERENCES ADMIRAAL, W. & L.A.H. VENEKAMP, 1986. Significance of Tintinnid grazing during blooms of Phaeocystis pouchetii (Haptophyceae) in Dutch coastal waters.--Neth. J. Sea Res. 20: 61-66. ATKINSON, L.P., G.A. PAFFENHOFER & W.M. DUNSTAN, 1978. The chemical and biological effect of a Gulf stream intrusion off St. Augustine, Florida.--Bull. mar. Sci. 28: 667-679. BENNEKOM, A.J. VAN, W.W.C. GIESKES & S.B. TIJSSEN, 1975. Eutrophication of Dutch Coastal Waters.-Proc. R. Soc. (B) 189: 359-374. BOALCH, G.T., 1984. Recent blooms in the western English Channel. ICES Special Meeting on the causes, dynamics and effects of exceptional marine blooms and related events. Ag: 1-6. BOUGARD, M., 1979. Etude bibliographique sur le phytoflagelle Phaeocystis. Institut de biologie maritime et regionale de Wimereux. Universite de sciences et de technique de Lille: 1-30. CADI~E, G.C. & J. HEGEMAN, 1974. Primary production of phytoplankton in the Dutch Wadden Sea.--Neth. J. Sea Res. 8: 240-259. - - - - , 1979. Phytoplankton primary production, chlorophyll and composition in an inlet of the western Wadden Sea (Marsdiep).--Neth. J. Sea Res. 13: 224-241. - - - - , 1986. Seasonal and annual variation of Phaeocystis pouchetii (Haptophyceae) in the westernmost inlet of the Wadden Sea during the 1973 to 1985 period.--Neth. J. Sea Res. 20: 29-36. CHU, S.P., 1946. The utilization of organic phosphorus

SPRING BLOOM OF PHAEOCYSTIS

by phytoplankton.--J, mar. biol. Ass. U.K. 26: 285-295. COLIJN, F., 1982. Light absorption in the waters of the Ems-Dollard estuary and its consequences for the growth of phytoplankton and microphytobenthos.--Neth. J. Sea Res. 16." 196-216. - - - - , 1983. Primary production in the Ems-Dollard estuary. University of Groningen: 1-123 (Ph.D. Thesis). CREUTZBERG, F. & H. POSTMA, 1979. An experimental approach to the distribution of mud in the southern North Sea.--Neth. J. Sea Res. 13:99-116. EBERLEIN, K., M.T. LEAL, K.D. HAMMER & W. HICKEL, 1985. Dissolved organic substances during a Phaeocystis bloom in the German Bight.--Mar. Biol. 89: 311-316. EL-SAYED, S.Z., D.C. BIGGS & O. HOLM-HANSEN, 1983. Phytoplankton standing crop, primary productivity, and near surface nitrogenous nutrient fields in the Ross Sea, Antarctica.--Deep Sea Res. 39: 871-886. EPPLEY, R.W., 1977. The growth and culture of diatoms. In: D.WERNER. The biology of diatoms. Botanical Monographs, 13. Blackwell Scientific Publications, Oxford: 24-64. FEDEROV, V.D. & N.G. KUSTENKO, 1972. Interregulation of marine planktonic diatoms in mono and mixed cultures.--Oceanologia 12" 111-122. FOSTER, D., D. VOLTOLINA,C.D. SPENCER, I. MILLER & J. BEARDALL, 1982. A seasonal study of the distribution of surface state variables in Liverpool Bay. IV. The spring bloom.--J, exp. mar. Biol. Ecol. 58: 19-31. GIESKES, W.W.C. & A.J. VAN BENNEKOM, 1973. Unreliability of the 14C method for estimating primary productivity in eutrophic Dutch coastal waters.--Limnol. Oceanogr. 18: 494-495. GIESKES, W.W.C. & G.W. KRAAY, 1975. The phytoplankton spring bloom in Dutch coastal waters of the North Sea.--Neth. J. Sea Res. 9: 166-196. - - - - , 1977. Primary production and consumption of organic matter in the southern North Sea during the spring bloom of 1975.--Neth. J. Sea Res. 11: 146-167. GUILLARD, R.R.L. & J.A. HELLEBUST, 1971. Growth and production of extracellular substances by two strains of Phaeocystis pouchetii.--J. Phycol. 7: 330-338. HALLEGRAEFF, G.M., 1983. Scale-bearing and Loricate Nanoplankton from East Australian Current.-Botanica Mar. 26: 493-515. HICKEL, W., 1984. Seston in the Wadden Sea of Sylt (German Bight, North Sea).--Neth. Inst. Sea Res., Publ. Ser. 10: 113-131. HOBBLE, J.E., R.J. DALEY & S. JASPERS, 1977. Use of Nucleopore filters for counting bacteria by fluorescence microscopy.--Arch. Mikrobiol. 33: 1225-1228. IVERSON, R.L., T.E. WHITLEDGE & J.J. GOERING, 1979. Chlorophyll and nitrate fine structure in the southern Bering Sea shelf break front.--Nature, Lond. 281: 664-666. JONES, P.G.W. & J.M. HAQ, 1963. The distribution of

47

Phaeocystis in the eastern Irish Sea.--J. Cons. perm. int. Explor. Mer 28: 8-20. KASKIN, N.J., 1963. Materials on the ecology of Phaeocystis pouchetii (Harlot) Lagerheim, 1893 (Chrysophyceae). I1. Habitat and specifications of biogeographical characteristics.--Okeanologiya, Moscow 3: 697-705. KORNMANN, P., 1955. Beobachtungen von PhaeocystisKulturen.--Helgolander wiss. Meeresunters. 5: 218-233. LAANBROEK, H.J., J.C. VERPLANKE, P.R.M. DE VISSCHER & R. DE VUYST, 1985. Distribution of phyto- and bacterioplankton growth and biomass parameters, dissolved inorganic nutrients and free amino acids during a spring bloom in the Oosterschelde basin, the Netherlands.--Mar. Ecol. Progr. Ser. 25: 1-11. LANCELOT, C., 1983. Factors affecting phytoplankton extracellular release in the Southern Bight of the North Sea.--Mar. Ecol. Progr. Ser. 12: 115-121. - - - - , 1984. Metabolic changes in Phaeocystispoucheti (Harlot) Lagerheim during the spring bloom in Belgian coastal waters.--Est, coast Shelf Sci. 18: 593-600. LANCELOT, C. & S. MATHOT, 1985. Biochemical fractionation of primary production of phytoplankton in Belgian coastal waters during short- and longterm incubation with 14C-bicarbonate. I1. Phaeocystis poucheti colonial population.--Mar. Biol. 86" 227-232. LEE, A., 1970. The currents and water masses of the North Sea.--Oceanogr. Mar. Biol. Ann. Rev. 8: 33-71. LEWIS, M.R. & J.C. SMITH, 1983. A small volume, short incubation time method for measurement of photosynthesis as a function of incident irradiance.--Mar. Ecol. Progr. Ser. 13: 99-102. LORENZEN, C.J., 1967. Determination of chlorophyll and phaeopigments: spectrophotometric equations. --Limnol. Oceanogr. 12" 343-347. PALMISANO, A.C. & C.W. SULLIVAN, 1985. Pathway of photosynthetic carbon assimilation in sea-ice microalgae from McMurdo Sound, Antarctica.-Limnol. Oceanogr. 30: 674-678. PARKE, M., J.C. GREEN & I. MANTON, 1971. Observations on the fine structure of zoids of the genus Phaeocystis (Haptophyceae).--J. mar. biol. Ass. U.K. 61: 927-941. SAVAGE, R.E., 1930. The influence of Phaeocystis on the migrations of the herring.--Fishery Invest., Lond. Ser. II 12: 5-14. SCHERFFEL, A., 1900. Phaeocystis globosa nov. spec. nebst einigen Betrachtungen Liber die Phylogenie niederer, insbesondere brauner Organismen.-Wiss. Meersesunters. Helgoland (N. F.) 4: 1-28. STRICKLAND, J.D.H. & T.R. PARSONS, 1972. A practical handbook of seawater analysis.--Bull. Fish. Res. Bd Can. 167: 1-310. TIJSSEN, s.g. & A. EIJGENRAAM, 1982. Primary and community production in the Southern Bight of the North Sea deduced from oxygen concentration variations in the spring of 1980.--Neth. J. Sea Res. 16: 247-259.

48

M.J.W. VELDHUIS, F. COLIJN & L.A.H. VENEKAMP

UTERMOHL, H., 1958. Zur Vervolkommung der quantitativen Phytoplankton Methodik.--Mitt. int. Verein. theor, angew. Limnol. 9." 1-38. VELDHUIS, M.J.W. & W. ADMIRAAL, 1985. Transfer of photosynthetic products in gelatinous colonies of Phaeocystis pouchetii and effect on the measurement of excretion rate.--Mar. Ecol. Progr. Ser. 26: 301-304. VELDHUlS, M.J.W., W. ADMIRAAL & F. COLIJN, 1986. Chemical and physiological changes of

phytoplankton during the spring bloom dominated by Phaeocystis pouchetii (Haptophyceae): observations in Dutch coastal waters of the North Sea.--Neth. J. Sea Res. 20: 49-60. WEISSE, T., N. GRIMM & P. MARTENS, 1984. Phaeocystis pouchetii blooms in the German Wadden Sea area off Sylt. ICES Special Meeting on the causes, dynamics and effects of exceptional marine blooms and related events. D10: 1-20.

(received 13-12-1985, revised 25-2-1986)