Effects of N:P:Si Ratios and Zooplankton Grazing on Phytoplankton Communities in the Northern Adriatic Sea. 11. Phytoplankton Species Composition

AQUATIC MICROBIAL ECOLOGY Published July 16 Vol. 18: 55-65.1999 Aquat Microb Ecol

Effects of N:P:Si ratios and zooplankton grazing on phytoplankton communities in the northern Adriatic Sea. 11. Phytoplankton species composition

Per Carlsson*, Edna Graneli

University of Kalmar. Department of Marine Sciences. POB 905. S-391 29 Kalmar. Sweden

ABSTRACT: Development of phytoplankton biomass and species composition in northern Adriatic Sea natural plankton communities was investigated in 2 spring/summer (May and June) enclosure experiments. The enclosures (100 1 plastic cylinders) were subjected to different concentrations/ratios of nitrate, phosphate and silicate in order to obtain a situation where one of these nutrients would limit phytoplankton biomass in different treatments. The initial phytoplankton community in both experiments was dominated by small (both by cell numbers and biomass) autotrophic flagellates. In the May experiment the small autotrophic flagellates made up more than 50% of the initial biomass; this was 95% in June. The duration of the experiments were 7 and 10 d, respectively. A surplus of nitrogen, phosphorus and sllicon favored the development of some fast-growing diatoms. Phosphorus deficiency induced higher phytoplankton biomass than expected from Redfield ratios (Redfield 1958), probably due to fast recycling of phosphorus compared to nitrogen. Despite low silicon concentrations in the silicon-deficient treatments, growth of &atoms was high in the May experiment suggesting a low silicon demand for the dominating small diatom species. The diatom Rhizosolenia fragilissima was particularly favored under phosphorus-deficient conditions whereas under nitrogen deficiency another diatom (Chaetoceros sp.) increased in biomass. Small flagellates were favored by either nitrogen deficiency (May) or by silicon deficiency (June). The increasing dominance of small flagellates in the natural communities during the transition from spring to summer, together with decreasing concentration of inorganic nitrogen, indicates that shortage of inorganic nitrogen can be important for the structure of northern Adriatic phytoplankton communities in this period.

KEY WORDS: Adriatic Sea. Phytoplankton species composition . Diatoms . Flagellates

INTRODUCTION sometimes species that have previously been missing or present in very low numbers can unexpectedly The composition of phytoplankton communities con- develop high abundance and form a bloom. The suc- tinuosly changes such that different species become cession of phytoplankton may be caused by changing abundant at different times. This process of continuous physical, chemical or biological factors such as grazing community reorganization is often termed 'succession' by zooplankton. Nutrient availability and the competi- (Smayda 1980). The succession of phytoplankton com- tive ability of different phytoplankton species to utilize munities is often quite predictable so the same species nutrients at low concentrations are considered to be dominate in the same waters at the same time year important factors leading to succession (Tilman 1977, after year (Edler 1979b, Smayda 1980). However, Sommer 1983). Others suggest, however, that competition for nutrients seldom occurs, since the planktonic system could be considered as being in a non-equilib- rium state (Harris 1986).

0 Inter-Research 1999 56 Aquat Microb Ecol 18. 55-65, 1999

For most marine coastal waters and inland seas nitro- zooplankton. The enclosures consisted of l00 1 white gen (N) is found to be the nutrient which increases polyethylene cylinders with lids. The cylinders were phytoplankton biomass when added In bioassay immersed in a swimming pool supplled with running experiments (Ryther & Dunstan 1971, Howarth 1988, water in order to keep the temperature inside the Graneli et al. 1990, Oviatt et al. 1995). A few cases cylinders close to the temperature of the surrounding have been reported where phosphorus (P) has been sea (15 to 18°C in May 1994, 21 to 24OC in June 1993). found to limit phytoplankton production (Berland et al. The pool was covered with a black plastic net (mesh 1980, Smith 1984). Phosphorus has been suggested to size approximately 5 mm). The lids and the plastic net be limiting in maiine coastal waters only when large together decreased the light intensity by 65 to 70%, nutrient loads with high N:P ratios reach coastal waters and prevented photoinhibition of the phytoplankton. (Howarth 1988). Phosphorus has been suggested to be The light intensity (photon flux [PAR] at 20 cm depth) the most limiting nutrient for phytoplankton primary in the cylinders was very variable (130 to 1200 pm01 production in the northern Adriatic Sea, since bioassay m-' S-'), depending on the degree of cloudiness (mea- experiments have shown a marked stimulation of sured during the primary production incubations phytoplankton growth when P was added (Pojed & which were performed for 2 h around noon). Kveder 1977, Mingazzini et al. 1992). In addition, 80% After filling the cylinders with 100 1 of seawater, of inorganic N:P ratios found in the surface waters sug- samples were taken from all the cylinders for irnmedi- gests that P is limiting phytoplankton growth (Chiau- ate analyses of nutrients (NO,, NH,, PO: anc! SiO,), dani et al. 1980). chlorophyll a (chl a), primary production and water Due to the higher N and P input to coastal areas, the was filtered for later analyses of particulate organic ratios for N and P in relation to silicon (Si) can be carbon (POC), nitrogen (PON) and phosphorus (POP) higher than normal in coastal waters (Wulff & Rahm (see Graneli et al. 1999). Based on the concentrations 1988, Sanden et al. 1991). A higher availability of N found for the different nutrients in the collected water, and P in coastal waters would cause the utilization of additions of NO,, PO, and SiOz were made to the dif- more Si, decreasing the concentration of Si in the ferent cylinders in order to obtain different nutrient water. This has been found to occur in the Baltic Sea ratios. Nutrients were added either as one initial pulse for over 20 yr (Wulff & Rahm 1988). Thus, in coastal (June 1993 experiment) or as daily pulses to reach a areas receiving a large input of N and P, such as the certain concentration (May 1994 experiment) (see northern Adriatic Sea, a situation may develop where Graneli et al. 1999). Each treatment was performed in Si is in shortage compared to available N and P, and triplicate. Iron, EDTA and trace metals (Cu, Zn, CO,Mn this can lead to a succession from diatoms to non-Si- and MO) were added at concentrations corresponding requiring flagellates (Schelske & Stoermer 1972, to 1/20 of the culture medium 'E', described by Guillard Smayda 1990, Conley & Malone 1992, Egge & Aksnes & Ryther (1962), in order to prevent any limitation of 1992). phytoplankton growth by these substances. For the Two enclosure experiments were performed to study same reason, vitamins (B12, biotin and thiamin) were how different ratios/concentrations of N, P and Si added according to Schone & Schone (1982) (as 1/20 of affected phytoplankton biomass and species composi- the original description). tion in natural phytoplankton communities from the The water in the cylinders was filtered once more northern Adriatic Sea. In the experiments we also through a 100 pm nylon net after 3 d in the experiment studied the chemical composition and polysaccharide during May 1994. This was done in order to remove the production by the phytoplankton and these results are copepodites that had developed from nauplii/eggs that presented in Graneli et al. (1999). were present in the initial 100 pm filtered water. This filtration procedure effectively prevented a copepod population from developing in the cylinders, as had METHODS happened in the May 1993 and June 1993 experiments (Turner et al. 1999). During 14 to 21 June 1993 and 7 to 16 May 1994, Samples were taken daily for analyses of nutrients land-based enclosure experiments were performed (No3,NH,, PO4 and SiOz) and chl a concentration (see with northern Adriatic seawater. The construction of Graneli et al. 1999 for details). Samples for identifica- this land-based enclosure system is descnbed in Ols- tion and counting of phytoplankton cells were taken son et al. (1992) and Graneli et al. (1999). The water daily and fixed in acid Lugol's solution. Later, only the containing the natural phytoplankton communities samples from the initial day and other selected days was pumped from 1 to 2 m depth from a station 15 km (among them, the day with the highest chl a concen- off the east coast of northern Italy, and filtered through tration) were counted with a Nikon TMS inverted a 100 pm mesh size nylon net in order to remove meso- microscope uslng the method described by Utermohl Carlsson & Graneli: Effects of nutrients and zooplankton grazing on phytoplankton. I1 57

(1958). At least 50, but often more than 400, cells were Table 1. Calculated carbon content of the dominant phyto- counted (depending on the abundance in the samples) plankton species/groups. Linear dimensions of at least 10 for each phytoplankton species/group, giving standard cells of each category were measured and cell volumes were calculated according to Edler (1979). To convert pm3 cell-' to deviations of 28 % or +l0 %, respectively. The dimen- * pg C cellv', the conversion factors 0.13 for dinoflagellates sions of at least 10 cells of each species/group were (Smetacek 1975) and 0.11 for the other categories were used measured for calculation of plasma volume of diatoms (Strathmann 1967) and cell volume of other species, following stereomet- ric formulas in Edler (1979b). To convert pm3 cell-' to pg C cell-', the conversion factors 0.13 for dinoflagellates (Smetacek 1975) and 0.11 for all other species June 1993 Prorocentrum micans were used (Strathmann 1967). Prorocen trum minimum Protopendmium steinii Nitzschia sp. 1 RESULTS Rhizosolenia fragilissima Flagellates 6 to 10 pm Flagellates 3 to 6 pm Nutrients and chl a May 1994 Chaetoceros sp. Results for nutrients and chl a are presented in detail Nitzschia clostenum Nitzschia sp. 2 in the previous paper (Graneli et al. 1999, in this issue). Rhizosolenia fragilissima Cyclotella sp. Flagellates 5 to 10 pm Cell carbon (determined microscopically by cell counts and calculated plasma volumes) ment (0.2 pm01 P 1-' d-l) (mean: 3200 pg C I-'), than in Carbon content was calculated for the dominating the high-N treatment (4 pm01 N 1-' d-l) (mean: 2450 pg species by measurement of the linear dimensions C 1-'). This was despite the fact that the daily additions (Table 1). This was done in order to make a comparison of nutrients to these 2 treatments should have been of the biomass of the different species dominating almost comparable according to their ratio (4/0.2 = 20), under different nutrient conditions instead of just com- which is close to the Redfield ratio of 16. Also, phyto- paring cell numbers. plankton biomass expressed as both POC and chl a In May 1994, the initial phytoplankton community concentration was higher in the low-P treatment than was dominated by small flagellates (5 to 10 pm) that in the high-N treatment (see Graneli et al. 1999). made up 54 % of the biomass (Fig. 1).Diatoms made up In the June 1993 experiment, initial phytoplankton C 45% of the initial biomass and dinoflagellates com- was dominated by smaller (3 to 6 pm) flagellates, prised only 1 % of the initial biomass. Some species which made up 77% of the initial biomass. Larger reached their maximum biomass on Day 6 of the flagellates (6 to 10 pm) comprised 18% of the initial experiment, while others increased until Day 10. On biomass, while dinoflagellates and diatoms only Day 6, diatoms dominated the biomass in all treat- accounted for 5% (Fig. 2). During the experiment, ments (between ?? and 97% of the biomass). In the smaller flagellates still dominated the biomass but low-level Si-deficient treatment (1 pm01 Si 1-' d-l) small diatoms also became important and made up 20% of flagellates made up a significantly larger proportion the biomass in the nutrient-sufficient treatment by Day (23 %) of the biomass than in the other treatments (p c 5, when maximum biomass was attained in most of the 0.05, ANOVA, Fishers PLSD). Also, in the in the 4 pm01 treatments (see Graneli et al. 1999). In the June 1993 Si 1-' d-' treatment, the flagellates made up a high pro- experiment, phytoplankton biomass did not become portion of the total biomass (14 %), but not significantly appreciably higher in the P-deficient treatment than in higher. On Day 10, the biomass of flagellates had the N-deficient treatment. In the P-deficient treatment, decreased in the Si-deficient treatments and made up the biomass of diatoms also increased and comprised only 2 to 3 % of the biomass, while they still increased 35 % of the biomass on Day 5. In the Si-deficient treat- in the low-level N-deficient treatment (1 pm01 N 1-' ment, the smaller flagellates (3 to 6 pm) became totally d-l), comprising 20 % of the biomass on Day 10, which dominant (75 % of the biomass on Day 7), while dia- was significantly more than in any other treatment (p < toms only comprised 2 % of the biomass in this treat- 0.05, ANOVA, Fishers PLSD). Dinoflagellates never ment at the end of the experiment. The maximum bio- made up more than 1 % of the biomass during this mass of flagellates was significantly higher in the experiment. The biomass became significantly higher Si-deficient treatment than in the other treatments (p < (p c 0.05, ANOVA, Fishers PLSD) in the low-P treat- 0.005, ANOVA, Fishers PLSD). % of cell carbon

P 0 N0 o 8

Initial 7

1 0 Nef E

Si-del4 Si-def 4 Nutr sul S P- Nutr sul S Nutr sul S Nulr suf U) L ~utrsul 20 -h, 1

0 N VI I Initial Initial - Initial

Si-del4

Nutr sul S Nutr sul S

Nutr suf 20 Nutr suf 20 Carlsson & Graneli: Effects of nutrients and zooplankton grazing on phytoplankton. I1 59

Prorocentrummicans 1 Nituchia sp. l I flagellates 3-6 pm 50 T T I I5- - 10 - -

5 - I,

Prorocentrumminimum I flagellates 6-10 pm I I Rhizosoleniafragilissima I

initial 20 Day 5 7 Day 7

Fig. 2. Dominant phytoplankton species/groups during the June 1993 expenment (as % of total cell carbon calculated from cell volumes). P-def: phosphorus-deficient treatment; N- def: nitrogen-deficient treatments; Si-def: silicon-deficient treatments; Nutr suf: nutnent-sufficent treatments See Graneli et al. (1999) for details on nutrient adbtions. (Mean i SD, n = 3)

Phytoplankton species composition Cyclotella species and a small solitary Chaetoceros species (Fig. 1). In the treatments with the highest In the May 1994 experiment, diatoms and small fla- nutrient additions, N. closterium became dominant gellates were the most abundant components of the (more than 40 X 103 cells ml-l), except in the high-N phytoplankton community. Dinoflagellates were very treatment (4 pm01 N 1-' d-l), where instead the small scarce, with 13 cells ml-' of Protoperidinium steinii solitary Chaetoceros sp. became dominant (Fig. 3). and <2 cells ml-' of Prorocentrum micans, which were This genus was also dominant in all the low-level the most common dinoflagellates. Thus, dinoflagel- nutrient-addition treatments. Small flagellates were lates are not further discussed in the treatment of the most important in the low-N treatment (average 12 X May 1994 results. Initially, the community was com- 103 cells ml-l). In the treatment with a low addition of posed of mainly small flagellates and the diatoms Rhi- Si (1 pm01 Si 1-' d-l), Si deficiency was not apparent zosolenia fragilissima, Nitzschia closterium, a small until the last 2 d of the experiment, and therefore did cell carbon (pg I-' )

Initia tInitia P-def 0.

Nutr suf F=- Nutr suf Nutr suf ~utrsuf 2h I Nulr suf ,% Nutr suf 0

N 0 8 g g I l I Initiat, Initia -- P-def 0.7 H 2 P-def 0. G' P-del 0.b 2 0, rh N-def t3 E. N-def 43 001 8 N-def 00. Si-def ts Y g --.2: Si-def 4Uo) C' Si-def 4 Si-del - Nutr suf 9 I Nutr suf Nutr suf 1 Nutr suf 2V3 Nutr suf 1 Nutr SUS -1 Carlsson & Graneli: Effects of nutrients and zooplankton grazing on phytoplankton II 6 1

JUNE 1993 " 7 Prorocenlrum micans

F h 40 I Prorocenlrurn minimum 1 flagellates 6-10 pm I m

initial Proroperidiniurnsteinii ^' 1 Day 5 Day 7

Fig. 4. Cell carbon (pg 1-l) for the dominant phytoplankton species/groups during the June 1993 experiment. See Table 1 for carbon content per cell. Treatments as in Fig. 2. (Mean * SD, n = 3)

not cause any significant decrease in the dominance of spp., and 2 diatom species (Nitzschia sp. 1 and Rhi- diatoms. zosolenia fragilissima) increased in biomass (Fig. 4). At In the June 1993 experiment, small unidentified fla- the end of the experiment, the small flagellates domi- gellates (3 to 6 pm) and flagellates (6 to 10 pm; cryp- nated in the Si-deficient treatment, while there were tomonads, haptophyceans and unidentified flagellates) only a few diatom cells in this treatment. The diatom dominated the initial phytoplankton community, both species increased to very high cell numbers (s40X 103 in terms of cell numbers and carbon biomass (Fig. 2). cells ml-' for Nitzschia sp. 1) in the nutrient-sufficent During the experiment, dinoflagellates, such as Proro- treatment. By Day 5, both R. fragilissima and Nitzschia centrum micans, P. minimum and Protoperidinium sp. 1 had reached high cell numbers in the P-deficient 62 Aquat Microb Ecol 18: 55-65, 1999

treatment. In this treatment, however, the cell number cessional stage (dinoflagellates and small autotrophic of the diatoms decreased between Days 5 and 7. The flagellates). This coincided with a lower concentration autotrophic dinoflagellate P. minimum also reached of inorganic N in the initial water used in the June higher cell numbers in the P-deficient treatment than experiment compared with the May experiment (see in the N-deficient treatment (p < 0.05, ANOVA, Fishers Graneli et al. 1999). PLSD). In both experiments, diatoms from a few genera became the most abundant phytoplankton in the treatments when the small flagellates did not continue to Possible effects of zooplankton on phytoplankton dominate, whereas dinoflagellates were always quite species composition in enclosures scarce. One diatom species (Rhizosolenia fragilissima) was favored under P-deficient conditions in both the During the June 1993 experiment, abundant cope- May 1994 and June 1993 experiments, while N defi- pod nauplii (5 to 35 nauplii I-') were initially present in ciency allowed another diatom species (Chaetoceros the cylinders, despite attempts to remove zooplankton sp.) to increase in biomass in the May 1994 experi- by screening with 100 pm mesh (Turner et al. 1999, in ment. Small flagellates were favored by either Si defi- this issue). Possibly, these nauph passed the mesh as ciency (June 1993) or by N deficiency (May 1994), and eggs and hatched into nauplii within the first 24 h of a surplus of N, P and Si enhanced the development of incubation. By Day 4 of the experiment, the number of certain fast-growing diatoms (Nitzschia spp.) in both Acartia and Oithona copepodites in enclosures in- May 1994 and June 1993. creased substantially (10 to 25 copepodites I-'). Filtra- The concentrations of the nutrients presumed to be tion rates determined for Acartia copepodites during limiting for production of phytoplankton biomass were the 1993 experiment were either undetectable or low low only during the last days of the June 1993 experi- (~0.2m1 copepod-' h-'), possibly because phytoplank- ment, since nutrients had been added as a single initial ton cell numbers were extremely high, inhibiting cope- pulse. This means that all phytoplankton species had pod feeding (Turner et al. 1999). In order to avoid the access to all nutrients in surplus during the first part of problem with possible grazing impact on phytoplank- this experiment, and it is therefore not surprising that ton species succession during the experiments, the there were no large differences in biomass of the dif- water in the cylinders was filtered a second time ferent species between treatments. In the May 1994 through 100 pm mesh size nylon net after 3 d in the experiment, however, the pulsed addition of small May 1994 experiment. This filtration effectively amounts of nutrients each day, instead, created a situ- stopped any development of copepods. In view of the ation where the phytoplankton was subjected to low low grazing activity during the June 1993 experiment, levels of a deficient nutrient over a longer time. This and the removal of grazers by the second filtration dur- was also reflected in the larger differences in the final ing the May 1994 experiment, it appears that copepod species dominance between treatments in this experi- feeding did not have any substantial impact upon ment. phytoplankton species succession in either of the Silicon concentrations never decreased below experiments. 0.55 pm01 I-'. This was probably the amount of Si that was left when the diatoms had taken up as much of the added Si as they were able to do. At this concentration, DISCUSSION the diatoms probably did not have maximum growth rates, even though the calculated growth rates were The experiments show that species composition of quite high. The pulsed addition of Si in the Si-deficient the phytoplankton communites was significantly treatment in the 1994 experiment permitted the domi- affected by the nutrient manipulations. The initial nant diatoms to grow at p = 0.7 to 1.0,i.e. 1.0 to 1.4 dou- phytoplankton community in both experiments was bling~d-'. A high growth rate is also indicated by the dominated by small autotrophic flagellates (both in P0C:chl a ratios, which were always below 100 terms of cell numbers and biomass). The diatom taxa (Graneli et al. 1999), indicating healthy, growing cells present in the initial community were similar in both (Goldman 1980). Reported half-saturation constants for experiments and the dominant diatoms were of small growth of marine diatoms are in the range of 0.02 to size (like the small solitary Chaetoceros sp. and the 0.5 pm01 1-' (Paasche 1980). Diatoms produce less-sili- Cyclotella sp.) (Table 1). However, there was a clear cified cell walls at increasing Si deficiency, but can distinction between the initial communities, with the maintain their growth rates even at quite low Si con- May community having a typical spring character with centrations (Paasche 1980). A smaller cell size may also more diatoms, compared with the June community, be beneficial for Si assimilation at low concentrations which had more species characteristic of a later suc- (Paasche 1973), and the diatom species growing well Carlsson & Graneli: Effects of nutrients and zooplankton grazing on phytoplankton. I1 63 -- - in our enclosures can be considered as 'small' species been found in other Mediterranean areas (Estrada (the solitary Chaetoceros species valve diameter was 5 1985). Since these smaller flagellates kept their domi- to 6 pm and the Cyclntc~llaspecies valve diameter was nance in the N-deficient treatments in the May exper- approximately 3 pm). Silicon concentration in samples iment, while diatoms became more dom~nantin the from northern Adriatic surface and intermediate water other treatments, the natural phytoplankton communi- layers are 4.7 ? 1.5 and 2.6 ? 0.9 pm01 1-' during sum- ties in the northern Adriatic Sea may well be deficient mer periods (Franco & Michelato 1992). This is consid- in available N during the summer period. Moreover, erably higher than the level of 0.55 pm01 I-' where small flagellates decreased in importance in the P-defi- diatoms were able to deplete silicate concentrations in cient treatments in the May experiment and were very the water, while still maintaining high growth rates in scarce at the end of the experiment. Our speculation our experiments. It is also higher than reported half that N could be important for the phytoplankton suc- saturation constants. Thus, diatoms in these waters cession in the northern Adriatic Sea is also supported should not have reduced growth rates due to lack of Si. by the increasing dominance of flagellates in the It has been reported that marine diatom communites spring-to-summer transition observed in the initial on average require N and Si in equal amounts water used in our experiments, and by Estrada (1985) (Brzezinski 1985). However, optimum Si-to-P-uptake for other parts of the Mediterranean, simultaneously ratios have a large range for different diatom species with decreasing concentrations of inorganic N in the (from 96:l to 1:l for freshwater diatoms, Kilham & Kil- water (see Vollenweider et al. 1992, Graneli et al. ham 1984). Diatoms with a low Si:P demand would 1999). need very small amounts of Si compared to N, assum- Nitrogen and Si deficiency were the main factors ing that their N:P demand is 16:l.It is also argued that limiting diatom growth in our experiments, even most marine diatoms have lower demands for Si than though growth of diatoms was also quite high in the Si- freshwater species (Paasche 1980, Sommer 1988, Con- deficient treatments. Small flagellates appeared to be ley et al. 1989). Therefore, it is possible that in the Si- favored by N deficiency, perhaps by decreased compe- deficient treatments, which received the same quantity tition with diatoms in these treatments. The few auto- of Si (moles) as N received in the N deficient treat- trophic dinoflagellate species present in the June 1993 ments, the high resulting biomass of diatoms de- experiment (Prorocentrum micans and P. minimum) pended on the dominating diatoms having a low grew best in the P-deficient treatments, but never be- demand for Si compared to N (in the Si-deficient treat- came dominant in any treatment. This suggests that ments, both N and P were in surplus). the autotrophic dinoflagellates were less-competitive A succession from diatoms to small flagellates in Si- species than the diatoms and the small flagellates. The and N-deficient enclosures has also been observed by heterotrophic dinoflagellate Protoperidinium steinii Shollhorn & Craneli (1996) and by Escavarage et al. did not show any different response to different treat- (1994). ments, and it grew quite well in all treatments. This The low-phosphate-addition (0.2 pm01 P 1-' d-l) treat- could be an effect of the heterotrophic feeding mode of ment in the May 1994 experiment resulted in much this species. Many Protoperidinium species have been higher maximum chl a concentrations than expected shown to feed upon diatoms, using a pseudopod (pal- from Redfield ratios, since the biomass (as chl a) was lium) (Gaines & Taylor 1984, Jacobsen & Anderson higher (approximately double) that in the N-deficient 1986), and the increase in diatoms in all treatments treatment where 4 pm01 1-' d-' of nitrate was added. would have supplied the P. steinii cells with an unlim- This could have been an effect of a faster recycling of P ited food supply, irrespective of the treatment. than of N. Short recycling times for P (

caused the phytoplankton community to become tems. Plenum Press, New York, p 247-277 totally dominated by fast-growing diatoms. The phyto- Franco P, Michelato A (1992) Northern Adriatic Sea: oceanog- raphy of the basin proper and of the western coastal zone. plankton biomass (as chl a, POC: Graneli et a1 1999; or In: Vollen\veider RA, Marchett~R, Viviani R (eds) Marine as calculated cell C: this paper) became considerably coastal eutrophication. Elsevier, Amsterdam. p 35-62 higher when phosphate was added than when a com- Gaines G. Taylor FJR (1984) Extracellular digestion in marine parable amount (Redfield ratio) of inorganic N was dinoflagellates. J Plankton Res 6:1057-1061 added. Also, small flagellates tended to grow better Goldman JC (1980) Physiological processes, nutrients availability and the concept of relative growth rate in marine phyto- than diatoms at N-deficient conditions in the May plankton ecology. Brookhaven Symp Biol31:179-194 experiment. This, together with increasing dominance Graneli E, Wallstrom K, Larsson U, Graneli W, Elmgren R of small flagellates coinciding with decreasing inor- (1990) Nutrient Lunitation of primary production in the ganic N concentrations in the initial samples (from Baltic Sea area. Ambio 19:142-151 spring to summer), reported monitoring data (Vollen- Graneli E. Carlsson P, Turner JT, Tester P, Bechemin C, Daw- son R, Funari E (1999) Effects of N:P:Si: ratios and zoo- weider et al. 1992) and the faster recycling of P com- plankton grazing on phytoplankton cornrnunltles in the pared to N prompts us to speculate that the availability northern Adriatic Sea. I. Nutrients, phytoplankton bio- of inorganic N may be important for both the biomass mass, and polysaccharide production. Aquat Microb Ecol production and species succession in the natural 18:3?-54 Gulllard RRL, Ryther JH (1962) Studies of marine planktonic phytoplankton communities in the northern Adriatic diatoms I. 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Editorial responsibdity: John Dolan, Submitted: September 22, 1998; Accepted: October 29, 1998 Villefranche-sur-Mer. France Proofs received from au thor(s): July 12, 1999