Open Access

Dinoflagellates and ciliates at Helgoland Roads, North Sea

  • Martin Günther Joachim Löder1Email author,
  • Alexandra Claudia Kraberg1,
  • Nicole Aberle1,
  • Silvia Peters1 and
  • Karen Helen Wiltshire1
Helgoland Marine Research201166:242

https://doi.org/10.1007/s10152-010-0242-z

Received: 19 July 2010

Accepted: 27 December 2010

Published: 19 January 2011

Abstract

A monitoring programme for microzooplankton was started at the long-term sampling station “Kabeltonne” at Helgoland Roads (54°11.3′N; 7°54.0′E) in January 2007 in order to provide more detailed knowledge on microzooplankton occurrence, composition and seasonality patterns at this site and to complement the existing plankton data series. Ciliate and dinoflagellate cell concentration and carbon biomass were recorded on a weekly basis. Heterotrophic dinoflagellates were considerably more important in terms of biomass than ciliates, especially during the summer months. However, in early spring, ciliates were the major group of microzooplankton grazers as they responded more quickly to phytoplankton food availability. Mixotrophic dinoflagellates played a secondary role in terms of biomass when compared to heterotrophic species; nevertheless, they made up an intense late summer bloom in 2007. The photosynthetic ciliate Myrionecta rubra bloomed at the end of the sampling period. Due to its high biomass when compared to crustacean plankton especially during the spring bloom, microzooplankton should be regarded as the more important phytoplankton grazer group at Helgoland Roads. Based on these results, analyses of biotic and abiotic factors driving microzooplankton composition and abundance are necessary for a full understanding of this important component of the plankton.

Keywords

DinoflagellatesCiliatesNorth SeaMonitoringHelgoland RoadsSeasonality

Introduction

Marine research has a long tradition on Helgoland. Water temperature has been measured at the Helgoland Roads long-term station “Kabeltonne” (54°11.3′N; 7°54.0′E) since 1873 (Wiltshire and Manly 2004), and biological, chemical and physical parameters have been recorded continuously on a work-daily basis since 1962 (Franke et al. 2004). This makes the Helgoland long-term data series one of the longest and most detailed aquatic data sets. Unique to this data set are the phytoplankton species numbers counted work-daily to species level wherever possible (Wiltshire and Dürselen 2004). Since 1975, the time series also includes meso- and macrozooplankton determined to species level three times per week (Greve et al. 2004). Thus, the time series provides an excellent basis for analyses of long-term trends including changes evinced in the North Sea pelagic system over the recent decades (Schlüter et al. 2008; Wiltshire et al. 2008). Furthermore, it is a very important basis for the parameterisation and validation of mathematical ecosystem models and is invaluable in biodiversity and global change considerations (Wirtz and Wiltshire 2005). However, one important group of planktonic organisms is under-represented in the long-term series so far—the microzooplankton. Although data on heterotrophic dinoflagellates exist in the data set, they were recorded with varying degrees of accuracy (Wiltshire and Dürselen 2004) and did not always mirror the diversity in species composition (Hoppenrath 2004). Long-term data on ciliates, another crucial microzooplankton group, are totally lacking at Helgoland Roads.

The term microzooplankton refers to the size fraction of heterotrophic planktonic organisms between 20 and 200 μm. Consisting of a diverse array of protozoa and metazoa, its numerically most important components are heterotrophic dinoflagellates and ciliates (Capriulo et al. 1991). Recent research, for example, by Landry and Calbet (2004), demonstrated the fundamental importance of microzooplankton as phytoplankton grazers. They showed that grazing by microzooplankton can be as high as 60–75% of the daily phytoplankton production. Furthermore, results indicate that microzooplankton tends to surpass mesozooplankton as primary consumers (Sherr and Sherr 2007). A meta-analysis of Calbet and Landry (2004) revealed that microzooplankton grazing can be responsible for 60% of phytoplankton mortality in coastal and estuarine environments (comparable to Helgoland Roads in terms of chlorophyll a concentration). We realised from observations that microzooplankton could also potentially be the most important grazer group in waters at Helgoland. Therefore, the aim of this study was to supplement the regular plankton monitoring series at Helgoland with an intensive monitoring of the microzooplankton. Investigations into species composition and seasonality of this important functional grazer group (dinoflagellates and ciliates) on a more regular basis will provide vital baseline data for studies of long-term changes in the microzooplankton community and the pelagic system at Helgoland.

Materials and methods

A 2.5-year microzooplankton monitoring programme has been carried out at Helgoland Roads to investigate the abundance of dinoflagellates and ciliates in the Southern North Sea. This monitoring hoped to establish a higher taxonomic resolution and to improve the evaluation of biomass for single taxa of microzooplankton.

From January 2007 until June 2009, samples were taken once a week at the “Kabeltonne” site (54°11.3′N; 7°54.0′E) at Helgoland. These data supplemented the routine sampling programme, which is carried out week-daily and for which plankton samples are fixed with a weak neutral Lugol’s solution (final concentration 0.5%) (Wiltshire et al. 2008). Although dinoflagellates are counted within the long-term programme, the taxonomic focus lies on phytoplankton groups such as diatoms. Due to the time-consuming counting procedure for phytoplankton and the high frequency of samples (work-daily), rare, small or uncommon dinoflagellate taxa are inevitably neglected or categorised into size classes. The present study investigated such under-represented species more intensely during the 2.5-year microzooplankton monitoring. Apart from three ciliates that have recently been included in the counting programme (Myrinecta rubra 1999, Laboea strobila 2007, Mesodinium pulex 2008), no ciliate species had continuously been recorded previously at Helgoland. Therefore, the new microzooplankton monitoring presented here was to provide completely new information on ciliate biomass and seasonality patterns at a hitherto unavailable taxonomic resolution.

The loss of microzooplankton species due to fixative problems has often been discussed in the literature (Stoecker et al. 1994). Thus, we diverged from the neutral fixative used for the long-term monitoring and used acidic Lugol’s solution (final concentration 2%, Throndsen 1978), as this is the standard fixative used in most studies on microzooplankton composition. The concentration we used has been proven to be the best compromise for both conserving higher concentrations of ciliates and preventing shrinkage of cells (Stoecker et al. 1994). A subsample of 250 mL was fixed immediately. Samples were stored in the cold and dark, and then 50 mL of the sample were settled for 24 h and counted under an inverted microscope (Zeiss Axiovert 135) using the Utermöhl method (Utermöhl 1958, Lund et al. 1958). At least half of the surface of the sedimentation chamber or the whole chamber was counted out at 200-fold magnification, thus reducing counting biases against rare species. Identification of naked dinoflagellates and especially of ciliates in Lugol’s solution-preserved samples is often difficult below genus level (Johansson et al. 2004), even with the modified fixation method applied here. Therefore, problematic ciliates and dinoflagellates were identified to genus level or, otherwise, pooled into size-dependent groups and “morphotypes”, based on their similar shape. Mixotrophy of the ciliates was not measured; thus, we have no exact data on the percentage of mixotrophic ciliates in the samples. However, to date, all mixotrophic ciliates have been shown to be phagotrophic (Sherr and Sherr 2002) and consequently all ciliates except Myrionecta rubra could be considered heterotrophic (Johansson et al. 2004). The latter species acts essentially as a phototroph (Montagnes et al. 2008), but as recent studies have shown that it also has phagotrophic capabilities (Park et al. 2007), we thus recorded it as mixotrophic.

As most chloroplast-bearing dinoflagellates are also capable of mixotrophic nutrition via phagotrophy (Du Yoo et al. 2009), these were considered to be potential grazers with more or less marked phagotrophic capabilities. The identification of dinoflagellates was primarily based on Dodge (1982), Tomas (1996) and Hoppenrath et al. (2009). Ciliates were determined based on Kahl (1932), Carey (1992) and Montagnes (2003).

As an additional new feature compared to the regular long-term series, each taxon recorded during counting was documented by an image (archived online at http://planktonnet.awi.de). These images, used for subsequent biovolume estimations, were also a useful tool for the documentation of rare and prior unrecorded species and for subsequent taxon assignments.

After measurement of the linear dimensions of the cells in the images, the biovolume of each taxon was calculated using the geometric models described by Hillebrand et al. (1999). The biovolume was converted into carbon using the conversion factor given by Putt and Stoecker (1989) for ciliates and Menden-Deuer and Lessard (2000) for dinoflagellates. The carbon content of the large “gelatinous” dinoflagellate Noctiluca scintillans was estimated according to the biovolume-carbon relationship given by Tada et al. (2000) after correction for shrinkage due to fixation (Beran et al. 2003). Carbon concentrations [μgC L−1] of dinoflagellates and ciliates are hereinafter also referred to as biomass or carbon biomass.

In vivo fluorescence as a proxy for phytoplankton biomass is measured on a work-daily basis (Algae Analyser, BBE Moldaenke, Kiel, Germany) as part of the routine monitoring at Helgoland Roads. These data were used as a rough indicator for autotrophic biomass and for the purpose of illustration of phytoplankton food availability and are presented in the results.

For the evaluation of the microzooplankton monitoring data, we compared them with the available data of the Helgoland Roads long-term data set on plankton. After evaluation of the literature on the quality of this data set (Wiltshire and Dürselen 2004) and the results of an unpublished revision of the data by S. Peters and M. Scharfe, two species that cannot be confused with other taxa were identified for the comparison: the dinoflagellate Noctiluca scintillans and the ciliate Myrionecta rubra.

Results and discussion

2.5-year microzooplankton monitoring

During the 2.5-year monitoring programme, 122 different taxa of dinoflagellates and ciliates were recorded (Tables 1, 2). Each group of organisms contributed roughly 50% to the total number of taxa.
Table 1

Dinoflagellate taxa and their seasonality as well as maximum cell concentrations, the mean biovolume and mean carbon content of each taxon as recorded during the 2.5 years of microzooplankton monitoring

Dinoflagellates

Assigned trophy

Observed seasonality

Maximum (cells L−1)

Months with maxima

Biovolume (μm³ cell−1)

Carbon (pg cell−1)

Order Peridiniales

 Diplopsalis lenticula

HT

Jan–Dec

1,800

May

68,147

6,909

 Heterocapsa cf. niei

MT

Jan–Dec

135,270

May

273

75

 Heterocapsa cf. rotundata

MT

May–Sep

5,700

Jun

1,077

231

 Protoperidinium bipes

HT

Jan–Dec

2,360

May

7,079

1,081

 Protoperidinium brevipes

HT

Feb–Dec

1,080

Apr

17,106

2,227

 Protoperidinium cf. claudicans

HT

Apr–Oct

120

Oct

88,488

8,557

 Protoperidinium cf. conicum

HT

Apr–Dec

240

May/Aug

82,966

8,117

 Protoperidinium cf. divergens

HT

Jan–???

20

Jan

88,804

8,582

 Protoperidinium cf. leonis

HT

Mar–Oct

1,720

Jul

50,915

5,442

 Protoperidinium cf. minutum group

HT

May–Dec

1,920

Jul

20,206

2,553

 Protoperidinium cf. obtusum

HT

Jun–Oct

200

Aug

146,909

12,961

 Protoperidinium cf. pyriforme group

HT

Mar–Jan

4,520

May

16,085

2,118

 Protoperidinium cf. subinerme

HT

May–Dec

220

May

121,344

11,082

 Protoperidinium denticulatum

HT

Mar–Nov

80

Jun/Sep

40,351

4,498

 Protoperidinium depressum

HT

May–Nov

80

Jul

513,443

36,117

 Protoperidinium excentricum

HT

Apr–Dec

40

Apr/Sep

49,635

5,329

 Protoperidinium ovatum

HT

Mar–Oct

280

Apr

134,256

12,039

 Protoperidinium pellucidum

HT

Mar–Jun

3,560

May

68,392

6,929

 Protoperidinium pentagonum

HT

May–Dec

40

May/Jul/Aug

700,146

46,561

 Protoperidinium sp. 20–30 μm

HT

Jan–Dec

1,120

Sep

8,567

1,264

 Protoperidinium sp. 30–40 μm

HT

Mar–Aug

560

May/Aug

31,686

3,690

 Protoperidinium thorianum

HT

Mar–Nov

220

Mar

119,459

10,941

 Pyrophacus horologicum

MT

Jun–Sep

80

Sep

56,845

5,955

 Scrippsiella/Pentapharsodinium sp.

MT

Jan–Dec

74,965

Aug

11,680

1,630

Order Gymnodiniales

 Akashiwo sanguinea

MT

Apr–Dec

56,480

Oct

50,539

5,409

 Amphidinium crassum

HT

Apr–Jan

1,460

Jun

5,089

825

 Amphidinium cf. sphenoides

HT

Aug–Feb

60

Aug/Dec

3,215

566

 Lepidodinium chlorophorum

MT

Jul–Jan

483,402

Aug

3,823

653

 Gymnodinium sp. 20 μm

MT

Jan–Dec

1,600

Nov

2,817

508

 Gymnodinium sp. 30 μm

MT

Jan–Dec

1,280

Jul

13,343

1,817

 Gymnodinium sp. 50 μm

MT

Mar–???

20

Mar

43,000

4,738

 Gyrodinium calyptoglyphe

HT

Jan–Dec

180

Jan

11,875

1,652

 Gyrodinium/Gymnodinium spp. <  15 μm

HT

Jan–Dec

74,965

Oct

733

169

 Gyrodinium sp. 20 μm

HT

Jul–Apr

34,578

Oct

1,014

220

 Gyrodinium sp. 20–30 μm

HT

Jan–Dec

5,160

Oct

3,896

663

 Gyrodinium sp. 30–50 μm

HT

Jan–Dec

7,280

Jul

8,774

1,289

 Gyrodinium sp. 50–75 μm

HT

Feb–Dec

5,560

Apr

28,746

3,407

 Gyrodinium sp. 75–100 μm

HT

Feb–Dec

1,320

Apr

54,520

5,755

 Gyrodinium sp. 100–150 μm

HT

Mar– Nov

2,080

May

178,637

15,212

 Katodinium sp. < 15 μm

HT

Jan–Dec

30,705

Aug

472

118

 Katodinium sp. 20 μm

HT

Jan–Dec

5,256

Jun

1,417

290

 Katodinium glaucum

HT

Jan–Dec

10,400

Aug

5,599

892

 Nematodinium sp.

HT

Jun–Dec

560

Nov

16,428

2,155

 Polykrikos kofoidii

HT

May–Nov

940

Oct

126,028

11,431

 Torodinium robustum 35 μm

MT

Jan–Dec

1,440

Apr

5,750

912

 Torodinium robustum 60 μm

MT

Jan–Dec

620

Aug

16,342

2,145

 Warnowia sp.

HT

Oct–Jul

4,560

May

10,799

1,528

Order Gonyaulacales

 Ceratium furca

MT

Apr–Jan

300

May

34,730

3,978

 Ceratium fusus

MT

Jan–Dec

4,520

Jul

20,830

2,617

 Ceratium horridum

MT

Sep–Jun

340

Jan

65,256

6,668

 Ceratium lineatum

MT

May–Jan

5,740

Jun

30,563

3,583

 Gonyaulax cf. spinifera

MT

Jun–Aug

280

Aug

22,327

2,770

 Peridiniella cf. danica

HT

Apr–Jan

12,172

Jun

1,424

291

Order Prorocentrales

 Mesoporos sp.

MT

Jan–Dec

1,360

Aug

3,709

637

 Prorocentrum balticum

MT

Jan–Dec

32,780

Jun

655

154

 Prorocentrum micans

MT

Jan–Dec

3,960

Jul

10,414

1,483

 Prorocentrum triestinum

MT

Jul–Dec

56,432

Aug

2,106

401

Order Noctilucales

 Noctiluca scintillans

HT

May–Jan

820

Jun

166,670,105

308,671

 Spatulodinium pseudonoctiluca

HT

Apr–Aug

20

Apr/Aug

960,073

60,300

Order Dinophysiales

 Dinophysis sp.

MT

Jan–Dec

1,560

Aug

20,320

2,564

Table 2

Ciliate taxa and their seasonality as well as maximum cell concentrations, the mean biovolume and mean carbon content of each taxon as recorded during the 2.5 years of microzooplankton monitoring

Ciliates

Assigned trophy

Observed seasonality

Maximum (cells L−1)

Months with maxima

Biovolume (μm³ cell−1)

Carbon (pg cell−1)

Order Strombidiida

 Cyrtostrombidium sp. 70 μm

HT

Jan–Dec

480

Apr

9,845

1,871

 Cyrtostrombidium sp. 160 μm

HT

Apr–Jan

80

Oct

170,893

32,470

 Laboea strobila

HT

Feb–Nov

2,240

Mar

91,865

17,454

 Strombidium capitatum

HT

Feb–Oct

1,120

Apr

99,785

18,959

 Strombidium cf. acutum

HT

Jan–Dec

3,020

Apr

43,563

8,277

 Strombidium cf. conicum

HT

Mar–Sep

360

May

24,877

4,727

 Strombidium cf. emergens

HT

Jan–Aug

1,080

Apr

35,923

6,825

 Strombidium cf. epidemum 30 μm

HT

Jan–Dec

24,840

Apr

6,465

1,228

 Strombidium cf. epidemum 35 μm

HT

Jan–Oct

1,320

Aug

8,862

1,684

 Strombidium cf. lynii

HT

Jan–Dec

400

Jan

36,968

7,024

 Strombidium cf. tressum

HT

Mar–Sep

2,640

Apr

9,694

1,842

 Strombidium sp. 20 μm

HT

Jan–Dec

1,640

May

4,977

946

 Strombidium sp. 25 μm

HT

Feb–Sep

1,680

Jul

2,463

468

 Strombidium sp. A 30 μm

HT

Jan–Dec

540

Apr

5,893

1,120

 Strombidium sp. B 30 μm

HT

Sep–May

200

May/Oct

4,157

790

 Strombidium sp. 35 μm

HT

Jan–Dec

580

Aug

8,244

1,566

 Strombidium sp. 40 μm

HT

Jan–Dec

2,480

May

7,296

1,386

 Strombidium sp. 50 μm

HT

Jan–Sep

100

Aug/Sep

9,390

1,784

 Strombidium sp. 60 μm

HT

Feb–Dec

1,200

Jul

19,294

3,666

 Strombidium sp. 100 μm

HT

Jan–Dec

120

Apr

105,853

20,112

 Tontonia gracillima

HT

Feb–Dec

280

Apr/May/Jun

25,089

4,767

Order Choreotrichida

 Leegaardiella cf. ovalis

HT

Jan–Dec

380

Feb

5,594

1,063

 Leegaardiella cf. sol

HT

Jan–Dec

780

Apr

22,301

4,237

 Lohmanniella oviformis

HT

Nov–Jul

2,260

Mar

4,725

898

 Rimostrombidium sp.

HT

Feb–Sep

320

Apr

100,779

19,148

 Strobilidium cf. neptunii

HT

Feb–Nov

160

May/Jun

54,726

10,398

 Strobilidium cf. sphaericum

HT

Jul–???

40

Jul

74,475

14,150

 Strobilidium cf. spiralis

HT

Apr–???

40

Apr

18,578

3,530

 Strobilidium sp. 15 μm

HT

May–Nov

10,160

Aug

1,061

202

 Strobilidium sp. 45 μm

HT

May–Aug

400

Aug

38,186

7,255

 Strombidinopsis sp. 90 μm

HT

Dec–Apr

40

Dec/Jan/Mar

94,898

18,031

 Strombidinopsis sp. 120 μm

HT

Jul–Oct

120

Aug

103,546

19,674

Order Tintinnida

 Eutintinnus sp. 30 μm

HT

Jun–Oct

240

Oct

4,169

792

 Eutintinnus sp. 60 μm

HT

Aug–???

120

Aug

32,695

6,212

 Favella ehrenbergii

HT

Jul–Oct

280

Sep

100,917

19,174

 Salpingella sp.

HT

Oct–Jan

260

Nov

1,953

371

 Stenosemella sp.

HT

Nov–Jun

6,440

May

10,722

2,037

 Tintinnid sp. 30 μm

HT

Jan–Dec

1,800

Jun

1,496

284

 Tintinnid sp. 70 μm

HT

Sep–???

40

Sep

58,219

11,062

 Tintinnidium cf. balechi

HT

Jan–Dec

1,360

Jan

4,114

782

 Tintinnopsis cf. radix

HT

Aug–Oct

80

Oct

27,489

5,223

 Tintinnopsis sp.

HT

Mar–Jan

660

Nov

4,279

813

Order Cyclotrichiida

 Askenasia regina

HT

Aug–Oct

380

Oct

172,422

32,760

 Askenasia sp.

HT

Apr–Sep

60

Jun

269,492

51,203

 Mesodinium pulex

HT

Jan–Dec

1,600

Aug

2,258

429

 Mesodinium sp. 20 μm

HT

May–Mar

680

Aug

4,102

779

 Mesodinium sp. 45 μm

HT

May–Sep

160

Jul/Aug

50,965

9,683

 Myrionecta rubra 15 μm

MT

Jan–Dec

24,960

Apr

2,356

448

 Myrionecta rubra 35 μm

MT

Jan–Dec

23,560

Jun

21,637

4,111

Order Haptorida

 Cyclotrichium sp.

HT

Mar–Oct

380

Apr

595,288

113,105

 Didinium gargantua

HT

Jun–Aug

20

Jun/Aug

68,770

13,066

 Spathidium sp.

HT

Mar–Nov

500

Jun

5,864

1,114

Order Prorodontida

 Balanion comatum 10–15 μm

HT

May–Jan

4,426

Jun

443

84

 Balanion comatum 15–25 μm

HT

Jan–Nov

1,880

Jun

2,356

448

 Tiarina fusus

HT

Jun–Dec

1,520

Aug

20,425

3,881

Order Euplotida

 Euplotes sp.

HT

Jan–Dec

1,040

Aug

7,561

1,437

Subclass Scuticociliatia

 Scuticociliates 10–30 μm

HT

Jan–Dec

2,240

Apr

1,595

303

 Scuticociliates 30–50 μm

HT

Apr–Jan

1,320

Aug

17,641

3,352

Sessile ciliates

 Acineta sp.

HT

Apr–Aug

60

Aug

35,298

6,707

 Vorticella sp.

HT

Jan–Dec

620

May

6,729

1,278

Miscellaneous

 Strombidium/Strobilidium spp. < 10 μm

HT

Jan–Dec

3,043

Jun

347

66

 Strombidium/Strobilidium spp. < 15 μm

HT

Jan–Dec

19,360

Jun

805

153

Sixty dinoflagellate taxa were recorded. Thirty-nine of them could be regarded as truly heterotrophic because they lacked chloroplasts, and the remainder was considered to be mixotrophic (Table 1). The ciliates found comprised 62 taxa. Due to their phagotrophic feeding capabilities, all ciliates were considered heterotrophic, with the exception of Myrionecta rubra (mixotrophic).

Heterotrophic dinoflagellates were always present in carbon concentrations between 0.5 and 272 μgC L−1, and mixotrophic dinoflagellates in carbon concentrations between 0.2 and 422 μgC L−1. During the 2.5-year period, the most important orders of dinoflagellates in terms of carbon biomass were mixotrophic Gymnodiniales (31%), followed by Noctilucales (25%), heterotrophic Gymnodiniales (17%) and mixotrophic (14%) as well as heterotrophic Peridiniales (7%) (Fig. 1, left panel). Prorocentrales, Gonyaulacales and Dinophysiales played only a minor role from a carbon biomass perspective (1–3%).
Fig. 1

Proportion of different dinoflagellate (left panel) and ciliate groups (right panel) during the 2.5 years of monitoring based on their carbon biomass contribution. MT mixotrophic, HT heterotrophic

Dinoflagellates closely followed the chlorophyll a development in spring, and biomass started to increase from March onwards (Fig. 2). Peaks in biomass often coincide with those of chlorophyll a or succeeded them, suggesting close coupling between prey availability and predator biomass.
Fig. 2

Carbon biomass (μgC L−1) of mixotrophic (MT) and heterotrophic (HT) dinoflagellates during the time of a 2.5-year weekly monitoring programme at Helgoland Roads in comparison with chlorophyll a concentration (μg L−1) measured on a work-daily basis via in situ fluorescence as a regular parameter of the long-term series

Maximum values always occurred during the summer months (June–August) when Noctiluca scintillans, Gyrodinium spp. and Protoperidinium spp. occurred together. Especially during this period, we detected high fluctuations in chlorophyll a and dinoflagellate biomass (summer 2007/2008 and spring 2009), suggesting high growth and mortality rates. However, these patterns did not reflect natural growth or mortality and could be traced back to variations in water bodies due to, for example, tidal currents and changing wind directions which were visible in abrupt changes in salinity and nutrients (data not shown). Towards winter and in tandem with decreasing chlorophyll a concentrations, heterotrophic dinoflagellate biomass reached its minimum suggesting close coupling with phytoplankton food availability. Outliers in biomass of heterotrophic dinoflagellates in December 2007 and January 2008 stem from the presence of single cells of N. scintillans. During the investigation period, mixotrophic dinoflagellates (Fig. 2) usually played a minor role compared to heterotrophic species (0.2–30 μgC L−1). Only in summer 2007 did they form an intense bloom from end of July to mid of October, thereby greatly exceeding the biomass of heterotrophic dinoflagellates (Fig. 2) and reaching values up to 422 μgC L−1. The bloom was first composed mainly of Lepidodinium chlorophorum as well as Scrippsiella/Pentapharsodinium sp. and Prorocentrum triestinum in lower densities. From mid September onwards, the bloom consisted mainly of Akashiwo sanguinea. During the rest of the sampling period, mixotrophic dinoflagellates were usually present in much lower concentrations than heterotrophic ones.

Ciliated protozoa were present throughout the time of monitoring with concentrations varying between 0.2 and 106 μgC L−1 (Fig. 3). In terms of carbon biomass, the ciliate order Strombidiida played the most important role during the monitoring programme being responsible for more than half of the biomass (51%), followed by M. rubra (23%) and then Choreotrichida (7%) and Haptorida (6%) (Fig. 1, right panel). Cyclotrichiida, Tintinnida and Prorodontida played a certain role (2–4%). The remaining ciliate groups were of negligible importance from a biomass perspective (0.4–1%).
Fig. 3

Carbon biomass (μgC L−1) of the ciliate Myrionecta rubra and the sum of the remaining ciliates during the time of a 2.5-year weekly monitoring programme at Helgoland Roads in comparison with chlorophyll a concentration (μg L−1) measured on a work-daily basis via in situ fluorescence as a regular parameter of the long-term series

Ciliates showed a different succession pattern when compared to dinoflagellates. Although they also generally followed the development of chlorophyll a in spring, they responded with an earlier and steeper increase to enhanced food availability (Fig. 3). Maxima were again found earlier in the year (March–early June) compared to dinoflagellates and mainly comprised Strombidiida (Laboea strobila, S. capitatum, S. cf. acutum, S. cf. emergens, S. cf. epidemum, S. cf. lynii and S. cf. tressum) and Cyclotrichium spp. As for the dinoflagellates and chlorophyll a, we sometimes detected high fluctuations in ciliate biomass (i.e. spring 2007/2009) due to variations in water bodies that did not reflect natural growth or mortality rates.

During the summer months, heterotrophic ciliate biomass often fluctuated synchronised with chlorophyll a concentration (summer 2007); during autumn (October 2007, September 2008), ciliate peaks followed those of autotrophic biomass. Towards winter, ciliate biomass also decreased in parallel with declining chlorophyll a concentrations. Interestingly, the first ciliate peak in 2007/2008 even occurred before the peak of the phytoplankton spring bloom.

Apart from three sampling dates during winter, the mixotrophic species M. rubra was present throughout the whole year usually in concentrations of up to 25 μgC L−1. It gained in importance during late spring and summer where it sometimes surpassed the biomass of the remaining ciliates. Maximum concentrations of this ciliate were found in spring 2007 (25 μgC L−1, small cells) and in June 2009 (97 μgC L−1, large cells).

Status of long-term monitoring on dinoflagellates and ciliates at Helgoland Roads

The revision and quality analysis of the long-term data set on plankton by Wiltshire and Dürselen (2004) showed that quality control was very arduous and is an ongoing process. Reasons which hampered the evaluation were both methodological in nature (e.g. fixation procedures or new microscope optics) and due to the frequent change of analysts during certain periods of the time series. The personal element involved in the recognition of microplankton species can never be eliminated completely, and especially for the dinoflagellates, it became evident that there was a large difference in the taxonomic knowledge between the ten different analysts. The revision also revealed that several taxa that have been recorded continuously since 1962 can be used without any restriction (12 diatom and 6 dinoflagellate taxa) and that others can be used with only minor restrictions (7 diatom and 2 dinoflagellate taxa) (for detailed account see Wiltshire and Dürselen 2004).

Here, we focus on the long-term data of dinoflagellates and ciliates as these two groups were the major interest of this study. A new revision of the long-term data in 2008 showed that only a restricted number of 9 dinoflagellate taxa were recorded continuously since the start of long-term monitoring and that these can be used without limitation (M. Scharfe and S. Peters, unpublished). These comprised different Ceratium species (C. furca, C. fusus, C. horridum, C. lineatum, C. tripos), Prorocentrum micans, the groups Gyrodinium spp. and Protoperidinium spp. as well as the species Noctiluca scintillans. Compared with the microzooplankton monitoring reported here, the 9 taxa of the long-term data set that can be used without limitation represented on average only 61% (3–94%) of the dinoflagellate biomass recorded during the 2.5 years.

Ciliates represented 3–96% of the total microzooplankton biomass recorded during the 2.5 years of monitoring. Their mean biomass contribution of 36% shows the importance of this microzooplankton group. Nevertheless, no ciliate species was recorded before 1999 when the long-term plankton monitoring started to include Myrionecta rubra. In the year 2007 Laboea strobila and 2008 Mesodinium pulex were additionally counted in the samples. However, these three ciliate taxa represented on average only 30% (0–86%) of the ciliate biomass recorded during the microzooplankton monitoring at Helgoland Roads.

Comparison of the two monitoring programmes

Due to their important contribution to planktonic biomass when concerning our data (Fig. 1) and due to the availability of long-term quality-checked cell concentration data on both species, we chose the dinoflagellate Noctiluca scintillans and the ciliate Myrionecta rubra for comparison of the 2.5-year data set with the data of the long-term series. As the long-term data series provided only rough carbon biomass values for those two species (Wiltshire and Dürselen 2004), we used cell numbers [n L−1] for comparisons.

Noctiluca scintillans (Fig. 4a) has continuously been recorded in the long-term data since 1962. It is the largest heterotrophic dinoflagellate species (usually > 500 μm) at Helgoland Roads. This species cannot be overlooked, and its characteristic appearance prevents confusion with other dinoflagellate species. N. scintillans usually occurred in higher densities from May to September with only rare observations in the other months of the year. One exception was the year 1965 where it was recorded only on 2 days at very low densities. Maxima were found in summer (June–August) reaching concentrations of up to 22.500 cells L−1.
Fig. 4

Mean daily cell concentration of (a) the dinoflagellate Noctiluca scintillans (n L−1) during the years 1962–2009 and (b) the ciliate Myrionecta rubra (n × 10³ L−1) during the years 1999–2009 of long-term monitoring at Helgoland Roads

Myrionecta rubra (Fig. 4b) has been recorded since 1999. This bloom-forming ciliate can be found in different size classes (Montagnes et al. 2008), and at Helgoland Roads, the size classes ~15 μm and ~35 μm were recorded during the microzooplankton monitoring. No differentiation in size classes was made in the long-term monitoring. It showed an all year-round occurrence at Helgoland Roads with minimal cell concentrations in wintertime. Frequently, two distinct maxima were found within the year: a lower spring maximum and a pronounced summer maximum where cell concentration partly rose up to over 1.1 × 106 cells L−1. In the recent years (2007–2009), M. rubra concentration was generally lower than in previous years. Interestingly, when looking at the data of the first 2 years in which this species has been counted, it became obvious that M. rubra cells were only recorded during a narrow window in the summer months, while in the following years it occurred year-round. This pattern is due to the two size classes of M. rubra. The smaller size class is more abundant in winter and spring than the bigger one; thus, it can easily be overlooked especially by an inexperienced analyst who has just started to count M. rubra. This was the case in the year 1999.

The comparison of the data of the weekly microzooplankton monitoring with the data of the work-daily counts (Figs. 5, 6) revealed that despite small differences, the lower resolution in the microzooplankton monitoring could nevertheless describe the seasonal patterns of distribution in both species. Discrepancies between both monitoring programmes were more pronounced in N. scintillans (Fig. 5a, b), where especially the maximum values of the years 2007 and 2009 were not reflected in the weekly samples. M. rubra (Fig. 6a, b) concentration from the microzooplankton monitoring mirrored the long-term data quite well. The most obvious outlier was in April 2007 where the microzooplankton monitoring recorded much higher concentrations of the small size class of M. rubra. This was due to methodological differences: besides the different counting frequencies, deviations in the records of both species most probably resulted from differences in counting methodology. While in the long-term monitoring, lower volumes are settled during blooms (usually 25 mL) and often tracks are counted for the smaller species (as here for M.rubra), at least half of the sedimentation chamber was counted during the microzooplankton monitoring and 50 mL were always used for sedimentation. Therefore, patchy settlement in a counting chamber will not have such a great effect as in the long-term monitoring. In conclusion, despite minor differences, data on N. scintillans and M. rubra of both monitoring programmes were well-matched and showed that the less frequent microzooplankton monitoring was suited for describing seasonal dynamics of dinoflagellates and ciliates.
Fig. 5

Comparison of cell concentration data on Noctiluca scintillans (n L−1) between the 2.5 years of microzooplankton monitoring (a) and the long-term monitoring (b)

Fig. 6

Comparison of cell concentration data on Myrionecta rubra (n L−1) between the 2.5 years of microzooplankton monitoring (a) and the long-term monitoring (b)

Ecological implications of the microzooplankton monitoring data

Our seasonal results for ciliates are comparable to results from monitoring programmes in the North Sea (Brussaard et al. 1995), Baltic Sea (Smetacek 1981; Johansson et al. 2004) and the Gulf of Maine (Montagnes et al. 1988) where distinct spring peaks were also seen. As they can respond more quickly to increasing phytoplankton concentrations, ciliates play a key role during spring (Riegman et al. 1993) and form an earlier peak than dinoflagellates. The majority of ciliates is, with few exceptions (Smetacek 1981; Aberle et al. 2007), restricted to the availability of smaller prey (Jonsson 1986; Tillmann 2004) consisting mainly of flagellates (Kivi and Setälä 1995), and their seasonal co-occurrence can be linked to that fact. Heterotrophic dinoflagellates are generally directly related to the availability of larger phytoplankton prey (Hansen 1991) and often occur at high concentrations during the course of diatom blooms (Sherr and Sherr 2007) especially during spring blooms (Stelfox-Widdicombe et al. 2004). Hansen (1991) reported a close relationship between dinoflagellate concentration and prey availability, and this was also shown by our results.

Microzooplankton can be both prey and competitor for mesozooplankton. At Helgoland Roads, small calanoid copepods can be regarded as direct competitors of ciliates and dinoflagellates for phytoplankton food. Their concentration ranges between 2 and 10 individuals L−1 over the year, with highest values during the summer period (Greve et al. 2004). The mean carbon content (annual mean 2007, n = 45) of the abundant small calanoid copepod Temora longicornis (Greve et al. 2004) was 9.5 μg carbon per female (K. L. Schoo, unpublished) at Helgoland Roads. Assuming a maximum carbon content of 10 μg per copepod combined with the maximum concentrations given by Greve et al. (2004) would therefore result in a maximum copepod carbon biomass of 100 μg L−1 (June/July). This value was surpassed by microzooplankton biomass, especially during the spring bloom. At this time, the combined effects of a faster metabolism and higher productivity (Fenchel and Finlay 1983; Montagnes and Lessard 1999) enables microzooplankton to have an undelayed direct response to increases in prey availability (Johansson et al. 2004; Aberle et al. 2007) when compared to its copepod competitors. Therefore, it is hardly surprising that recent studies have shown that microzooplankton does not only compete with copepods for the same resources (Aberle et al. 2007) but that it may exert a stronger grazing pressure on phytoplankton than copepods (Sherr and Sherr 2007) especially during bloom events. Indeed, the results of microzooplankton grazing experiments conducted during the spring bloom 2009 confirmed the dominant role of microzooplankton as phytoplankton grazers at Helgoland Roads when compared to copepods (Löder 2010).

We found that during the summer months, ciliate biomass was generally lower when compared to dinoflagellate biomass. Only with their decreasing concentrations at the end of summer did ciliate biomass reach the same importance as dinoflagellate biomass again. However, ciliates are the first microzooplankton grazers which react to enhanced food availability in spring when the concentration of small flagellated prey increases at Helgoland. Such an earlier onset of ciliate blooms can be directly linked to their higher growth rates when compared to dinoflagellates (Hansen 1992; Strom and Morello 1998). On the other hand, they are generally more restricted to the availability of particular prey types (Tillmann 2004), especially flagellates, than dinoflagellates (Jeong 1999). Therefore, ciliates can respond more rapidly to enhanced food concentrations than dinoflagellates, but their potential of surviving starvation periods is low (Jackson and Berger 1985) compared to dinoflagellates (Hansen 1992; Menden-Deuer et al. 2005). Consequently, ciliates can be classified as rapid-reaction food specialists and dinoflagellates more as generalists with longer response times but greater persistence. This implies rapid responses to increasing food concentrations but also quick declines of ciliate concentration as a direct response to decreasing prey concentration as was especially seen during spring at Helgoland. Ciliate maxima should therefore occur only when their appearance is coupled with the sufficient availability of adequate prey. When food availability increases in spring and ciliate predators achieve reproduction rates equal to those of their prey or even higher (Riegman et al. 1993), the effective grazing of ciliates could sometimes even prevent their preferred prey (e.g. flagellates) from blooming. This is most likely the explanation for the ciliate peaks in spring 2007 and 2008, while simultaneously autotrophic biomass stays more or less constant. These ciliate peaks occurred prior to the chlorophyll a peak of the real phytoplankton spring bloom which consisted mainly of larger diatoms of no prey significance for ciliates (Gifford 1988). Such size-differentiated microzooplankton grazing control by ciliates, promoting diatom spring blooms of larger species, has already been reported elsewhere for the North Sea (Riegman et al. 1993; Brussaard et al. 1995).

Another factor potentially influencing abundances of both ciliates and dinoflagellates is predation, for example, by copepods. Microzooplankton contributes substantially to copepod diets and is often positively selected by them (Nejstgaard et al. 1997; Fileman et al. 2007). The capacity of microzooplankton to synthesise highly unsaturated fatty acids and sterols makes them good-quality food for copepods (Klein Breteler et al. 1999; Tang and Taal 2005). Especially when phytoplankton prey is nutrient-limited, rendering it a low-quality food, microzooplankton predators are able to dampen stoichiometric constraints of their prey to a certain extent (Malzahn et al. 2010) and are therefore of better nutritional value for copepods compared to phytoplankton. The selective predation of copepods on microzooplankton during the course of the spring bloom 2009 at Helgoland Roads confirmed the important role of microzooplankton as food source for mesozooplankton as well as the role of copepods as controlling factor for microzooplankton (Löder 2010).

We showed that microzooplankton is an important component of the food web at Helgoland Roads. Due to its temporarily very high biomass occurence and presence throughout the year, it can probably be regarded as the most important phytoplankton grazer group. Microzooplankton is an important food source for higher trophic levels such as copepods at Helgoland. As the routine plankton monitoring at Helgoland Roads has a broader focus on diverse phytoplankton organism groups, it cannot resolve the diversity of microzooplankton. Given its key role in the food web, we recommend the long-term implementation of microzooplankton, especially dinoflagellates and ciliates, into the Helgoland Roads long-term sampling programme. Further multivariate statistical analyses are necessary to evaluate the biotic and abiotic factors that drive microzooplankton composition and abundance patterns. Using the data of the Helgoland Roads long-term series, such analyses will further enhance our in-depth understanding of microzooplankton occurrence in the North Sea.

Notes

Declarations

Acknowledgments

This study was part of a PhD thesis within the Food Web Project at the Alfred Wegener Institute for Polar and Marine Research, and we are grateful for the funding. Furthermore, we want to thank the crew of the research vessels Aade for providing samples, Kristine Carstens for her help in the laboratory and Mirco Scharfe for his evaluation of the species lists of the long-term series. Last but not least—we thank the whole team of the AWI Food Web Project for their collegiality.

Authors’ Affiliations

(1)
Biologische Anstalt Helgoland, Alfred Wegener Institute for Polar and Marine Research

References

  1. Aberle N, Lengfellner K, Sommer U (2007) Spring bloom succession, grazing impact and herbivore selectivity of ciliate communities in response to winter warming. Oecologia 150(4):668–681PubMedView ArticleGoogle Scholar
  2. Beran A, Guardiani B, Tamberlich F, Kamburska L, Fonda Umani S (2003) Carbon content and biovolume of the heterotrophic dinoflagellate Noctiluca scintillans from the Northern Adriatic Sea. Paper presented at the Proceedings of the CESUM-BS 2003, Varna. UNESCO, ParisGoogle Scholar
  3. Brussaard CPD, Riegman R, Noordeloos AAM, Cadee GC, Witte H, Kop AJ, Nieuwland G, Vanduyl FC, Bak RPM (1995) Effects of grazing, sedimentation and phytoplankton cell lysis on the structure of a coastal pelagic food web. Mar Ecol Prog Ser 123(1–3):259–271View ArticleGoogle Scholar
  4. Calbet A, Landry MR (2004) Phytoplankton growth, microzooplankton grazing, and carbon cycling in marine systems. Limnol Oceanogr 49(1):51–57View ArticleGoogle Scholar
  5. Capriulo GM, Sherr EB, Sherr BF (1991) Trophic behaviour and related community feeding activities of heterotrophic marine protists. In: Reid PC, Turley CM, Burkill PH (eds) Protozoa and their role in marine processes. Springer, Berlin, pp 219–265View ArticleGoogle Scholar
  6. Carey PG (1992) Marine interstitial ciliates: an illustrated key. Chapman & Hall, London, New YorkGoogle Scholar
  7. Dodge JD (1982) Marine dinoflagellates of the British Isles. Her Majesty’s Stationery Office, LondonGoogle Scholar
  8. Du Yoo Y, Jeong HJ, Kim MS, Kang NS, Song JY, Shin W, Kim KY, Lee K (2009) Feeding by phototrophic red-tide dinoflagellates on the ubiquitous marine diatom Skeletonema costatum. J Eukaryot Microbiol 56(5):413–420PubMedView ArticleGoogle Scholar
  9. Fenchel T, Finlay BJ (1983) Respiration rates in heterotrophic, free-living protozoa. Microb Ecol 9(2):99–122View ArticleGoogle Scholar
  10. Fileman E, Smith T, Harris R (2007) Grazing by Calanus helgolandicus and Para-Pseudocalanus spp. on phytoplankton and protozooplankton during the spring bloom in the Celtic Sea. J Exp Mar Biol Ecol 348(1–2):70–84View ArticleGoogle Scholar
  11. Franke HD, Buchholz F, Wiltshire KH (2004) Ecological long-term research at Helgoland (German Bight, North Sea): retrospect and prospect–an introduction. Helgol Mar Res 58(4):223–229View ArticleGoogle Scholar
  12. Gifford DJ (1988) Impact of grazing by microzooplankton in the Northwest Arm of Halifax Harbor, Nova Scotia. Mar Ecol Prog Ser 47(3):249–258View ArticleGoogle Scholar
  13. Greve W, Reiners F, Nast J, Hoffmann S (2004) Helgoland Roads meso- and macrozooplankton time-series 1974 to 2004: lessons from 30 years of single spot, high frequency sampling at the only off-shore island of the North Sea. Helgol Mar Res 58(4):274–288View ArticleGoogle Scholar
  14. Hansen PJ (1991) Quantitative importance and trophic role of heterotrophic dinoflagellates in a coastal pelagial food web. Mar Ecol Prog Ser 73(2–3):253–261View ArticleGoogle Scholar
  15. Hansen PJ (1992) Prey size selection, feeding rates and growth dynamics of heterotrophic dinoflagellates with special emphasis on Gyrodinium spirale. Mar Biol 114(2):327–334View ArticleGoogle Scholar
  16. Hillebrand H, Dürselen C-D, Kirschtel D, Pollingher U, Zohary T (1999) Biovolume calculation for pelagic and benthic microalgae. J Phycol 35(2):403–424View ArticleGoogle Scholar
  17. Hoppenrath M (2004) A revised checklist of planktonic diatoms and dinoflagellates from Helgoland (North Sea, German Bight). Helgol Mar Res 58(4):243–251View ArticleGoogle Scholar
  18. Hoppenrath M, Elbrächter M, Drebes G (2009) Marine phytoplankton: selected microphytoplankton species from the North Sea around Helgoland and Sylt. Kleine Senckenberg-Reihe 49. E. Schweizerbart’sche Verlagsbuchhandlung (Nägele u. Obermiller), StuttgartGoogle Scholar
  19. Jackson KM, Berger J (1985) Survivorship curves of ciliate protozoa under starvation conditions and at low bacterial levels. Protistologica 21(1):17–24Google Scholar
  20. Jeong HJ (1999) The ecological role of heterotrophic dinoflagellates in marine plankton community. J Eucaryot Microbiol 46:390–396View ArticleGoogle Scholar
  21. Johansson M, Gorokhova E, Larsson U (2004) Annual variability in ciliate community structure, potential prey and predators in the open northern Baltic Sea proper. J Plankton Res 26(1):67–80View ArticleGoogle Scholar
  22. Jonsson PR (1986) Particle size selection, feeding rates and growth dynamics of marine planktonic oligotrichous ciliates (Ciliophora: Oligotrichina). Mar Ecol Prog Ser 33:265–277View ArticleGoogle Scholar
  23. Kahl A (1932) Urtiere oder Protozoa. I Wimpertiere. 3 Spirotricha. In: Dahl F (ed) Die Tierwelt Deutschlands und der angrenzenden Meeresteile, vol 25. Gustav Fischer, JenaGoogle Scholar
  24. Kivi K, Setälä O (1995) Simultaneous measurement of food particle selection and clearance rates of planktonic oligotrich ciliates (Ciliophora: Oligotrichina). Mar Ecol Prog Ser 119:125–137View ArticleGoogle Scholar
  25. Klein Breteler WCM, Schogt N, Baas M, Schouten S, Kraay GW (1999) Trophic upgrading of food quality by protozoans enhancing copepod growth: role of essential lipids. Mar Biol 135(1):191–198View ArticleGoogle Scholar
  26. Landry MR, Calbet A (2004) Microzooplankton production in the oceans. ICES J Mar Sci 61(4):501–507View ArticleGoogle Scholar
  27. Löder MGJ (2010) The role of heterotrophic dinoflagellate and ciliate grazers in the food web at Helgoland Roads, North Sea. Doctoral thesis, Jacobs University BremenGoogle Scholar
  28. Lund JWG, Kipling C, Cren ED (1958) The inverted microscope method of estimating algal numbers and the statistical basis of estimations by counting. Hydrobiologia 11(2):143–170View ArticleGoogle Scholar
  29. Malzahn AM, Hantzsche F, Schoo KL, Boersma M, Aberle N (2010) Differential effects of nutrient-limited primary production on primary, secondary or tertiary consumers. Oecologia 162(1):35–48PubMedView ArticleGoogle Scholar
  30. Menden-Deuer S, Lessard EJ (2000) Carbon to volume relationships for dinoflagellates, diatoms, and other protist plankton. Limnol Oceanogr 45(3):569–579View ArticleGoogle Scholar
  31. Menden-Deuer S, Lessard EJ, Satterberg J, Grünbaum D (2005) Growth rates and starvation survival of three species of the pallium-feeding, thecate dinoflagellate genus Protoperidinium. Aquat Microb Ecol 41(2):145–152View ArticleGoogle Scholar
  32. Montagnes DJS (2003) Planctonic ciliate project internet homepage: http://www.liv.ac.uk/ciliate/intro.htm, date: 19.12.2007, time: 13:56
  33. Montagnes DJS, Lessard EJ (1999) Population dynamics of the marine planktonic ciliate Strombidinopsis multiauris: its potential to control phytoplankton blooms. Aquat Microb Ecol 20(2):167–181View ArticleGoogle Scholar
  34. Montagnes DJS, Lynn DH, Roff JC, Taylor WD (1988) The annual cycle of heterotrophic planktonic ciliates in the waters surrounding the Isles of Shoals, Gulf of Maine: an assessment of their trophic role. Mar Biol 99:21–30View ArticleGoogle Scholar
  35. Montagnes DJS, Allen J, Brown L, Bulit C, Davidson R, Diaz-Avalos C, Fielding S, Heath M, Holliday NP, Rasmussen J, Sanders R, Waniek JJ, Wilson D (2008) Factors controlling the abundance and size distribution of the phototrophic ciliate Myrionecta rubra in open waters of the North Atlantic. J Eukaryot Microbiol 55(5):457–465PubMedView ArticleGoogle Scholar
  36. Nejstgaard JC, Gismervik I, Solberg PT (1997) Feeding and reproduction by Calanus finmarchicus, and microzooplankton grazing during mesocosm blooms of diatoms and the coccolithophore Emiliania huxleyi. Mar Ecol Prog Ser 147(1–3):197–217View ArticleGoogle Scholar
  37. Park JS, Myung G, Kim HS, Cho BC, Yih W (2007) Growth responses of the marine photosynthetic ciliate Myrionecta rubra to different cryptomonad strains. Aquat Microbial Ecol 48:83–90View ArticleGoogle Scholar
  38. Putt M, Stoecker DK (1989) An experimentally determined carbon:volume ratio for marine “oligotrichous” ciliates from estuarine and coastal waters. Limnol Oceanogr 34(9):1097–1103View ArticleGoogle Scholar
  39. Riegman R, Kuipers BR, Noordeloos AAM, Witte HJ (1993) Size-differential control of phytoplankton and the structure of plankton communities. Neth J Sea Res 31(3):255–265View ArticleGoogle Scholar
  40. Schlüter MH, Merico A, Wiltshire KH, Greve W, von Storch H (2008) A statistical analysis of climate variability and ecosystem response in the German Bight. Ocean Dyn 58(3–4):169–186View ArticleGoogle Scholar
  41. Sherr EB, Sherr BF (2002) Significance of predation by protists in aquatic microbial food webs. Antonie Van Leeuwenhoek Int J Gen Mol Microbiol 81(1–4):293–308View ArticleGoogle Scholar
  42. Sherr EB, Sherr BF (2007) Heterotrophic dinoflagellates: a significant component of microzooplankton biomass and major grazers of diatoms in the sea. Mar Ecol Prog Ser 352:187–197View ArticleGoogle Scholar
  43. Smetacek V (1981) The annual cycle of proto-zooplankton in the Kiel Bight. Mar Biol 63(1):1–11View ArticleGoogle Scholar
  44. Stelfox-Widdicombe CE, Archer SD, Burkill PH, Stefels J (2004) Microzooplankton grazing in Phaeocystis and diatom-dominated waters in the southern North Sea in spring. J Sea Res 51:37–51View ArticleGoogle Scholar
  45. Stoecker DK, Gifford DJ, Putt M (1994) Preservation of marine planktonic ciliates–losses and cell shrinkage during fixation. Mar Ecol Prog Ser 110(2–3):293–299View ArticleGoogle Scholar
  46. Strom SL, Morello TA (1998) Comparative growth rates and yields of ciliates and heterotrophic dinoflagellates. J Plankton Res 20(3):571–584View ArticleGoogle Scholar
  47. Tada K, Pithakpol S, Yano R, Montani S (2000) Carbon and nitrogen content of Noctiluca scintillans in the Seto Inland Sea, Japan. J Plankton Res 22(6):1203–1211View ArticleGoogle Scholar
  48. Tang KW, Taal M (2005) Trophic modification of food quality by heterotrophic protists: species-specific effects on copepod egg production and egg hatching. J Exp Mar Biol Ecol 318(1):85–98View ArticleGoogle Scholar
  49. Throndsen J (1978) Preservation and storage. In: Sournia A (ed) Phytoplankton manual. UNESCO, Paris, pp 69–74Google Scholar
  50. Tillmann U (2004) Interactions between planctonic microalgae and protozoan grazers. J Eukaryot Microbiol 51(2):156–168PubMedView ArticleGoogle Scholar
  51. Tomas CR (1996) Identifying marine diatoms and dinoflagellates. Acedemic Press Inc., San Diego, New YorkGoogle Scholar
  52. Utermöhl H (1958) Zur Vervollkommnung der quantitativen Plankton-Methodik. Mitt Int Ver Theor Angew Limnol 9:1–38Google Scholar
  53. Wiltshire KH, Dürselen CD (2004) Revision and quality analyses of the Helgoland Reede long-term phytoplankton data archive. Helgol Mar Res 58(4):252–268View ArticleGoogle Scholar
  54. Wiltshire KH, Manly BFJ (2004) The warming trend at Helgoland Roads, North Sea: phytoplankton response. Helgol Mar Res 58:269–273View ArticleGoogle Scholar
  55. Wiltshire KH, Malzahn AM, Wirtz K, Greve W, Janisch S, Mangelsdorf P, Manly BFJ, Boersma M (2008) Resilience of North Sea phytoplankton spring bloom dynamics: an analysis of long-term data at Helgoland Roads. Limnol Oceanogr 53(4):1294–1302View ArticleGoogle Scholar
  56. Wirtz KW, Wiltshire K (2005) Long-term shifts in marine ecosystem functioning detected by inverse modeling of the Helgoland Roads time-series. J Mar Syst 56(3–4):262–282View ArticleGoogle Scholar

Copyright

© Springer-Verlag and AWI 2011