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Impact of a Dinophysis acuminata Bloom on the Copepod Acartia clausi: First Indications

Constantin Frangoulis
Epaminondas D. Christou
Ioanna Varkitzi
Soultana Zervoudaki
Isabel Maneiro
Camilla Svensen
Kalliopi Pagou
Georgia Assimakopoulou
Ioannis Hatzianestis
2 and
Edna Granéli
Hellenic Centre for Marine Research, Institute of Oceanography, Former American Base of Gournes, P.O. Box 2214, 71003 Heraklion, Greece
Hellenic Centre for Marine Research, Institute of Oceanography, P.O. Box 712, 19013 Athens, Greece
Facultad de Ciencias, Universidad de Vigo, Lagoas-Marcosende, E-36200 Vigo, Spain
Department of Arctic and Marine Biology, UiT—The Arctic University of Norway, N-9037 Tromsø, Norway
Marine Sciences Centre, Linnaeus University, 39182 Kalmar, Sweden
Author to whom correspondence should be addressed.
Water 2022, 14(14), 2204;
Submission received: 28 May 2022 / Revised: 17 June 2022 / Accepted: 6 July 2022 / Published: 12 July 2022
(This article belongs to the Special Issue Studies on the Diversity and Ecology of Marine Phytoplankton)


Faecal pellet production and content along with egg production of the dominant copepod species Acartia clausi were studied in the Thermaikos Gulf (NW Aegean Sea) during a pre-bloom and a bloom of the toxic dinoflagellate Dinophysis acuminata. Both faecal pellet production (6.8–8.6 ind−1 d−1) and egg production (15.8–47.6 ind−1 d−1) appeared unrelated to the D. acuminata bloom. Less than 11% of the copepod faecal pellets contained one or two D. acuminata cells, almost intact, whereas the other material in the pellets was broken into small pieces or amorphous shapes. The toxin outflux seemed to be insignificant when compared to the mean toxin concentration from the whole D. acuminata population. Finally, the potential grazing impact of A. clausi on D. acuminata during the study period was low.

1. Introduction

Harmful algal blooms (HABs) affect coastal marine ecosystems, on lower (plankton, bivalves) and higher trophic levels (fishes, birds and whales), as well as human health and cause large economical losses. In the Thermaikos Gulf (NW Aegean Sea), HABs result in substantial socio-economic impacts (economic losses of ~3 million euros every year), since the harvest of farmed mussels is banned for several weeks [1].
In the zooplankton–HAB blooms relationship there is a lack in our knowledge concerning the fate of toxic dinoflagellates ingested by zooplankton and outcomes appear situation-specific: redistribution in grazer tissues (e.g., [2,3]), eggs [4] or faecal pellets [5,6]. Faecal pellets could have a significant role in toxin transfer [6], as they are often the most important vector among all copepod products (reviews [7,8]).
Several studies indicate that phytoplankton toxicity is an adaptation of algae to escape grazing and toxic cells are selectively avoided by zooplankton when feeding on mixtures of different prey species (e.g., [9]). This avoidance is related to toxic phytoplankton affecting grazing, egg production and hatching rates (review by Turner and Tester [10]). Many studies on the harmful effects of phytoplankton on grazers have focused either on feeding activity (e.g., [5,11,12,13,14]) or on egg production and hatching rates (e.g., [15,16,17,18]). However, few studies have considered all these processes at the same time [4,14,19]), which is necessary if we are to fully evaluate the effects of harmful algae on grazers.
There is also little information on interactions between planktonic grazers and algae producing diarrhetic shellfish poisoning (DSP) toxins, due to unsuccessful attempts at cultivation of the Dinophysis Ehrenberg genus [20]. The main DSP toxins (Okadaic acid (OA) and Dinophysis toxins) are produced usually by dinoflagellates that belong to the genera Dinophysis spp. [21] and epibenthic species of the dinoflagellate genus Prorocentrum; however, only the latter have been grown in cultures. Therefore, although Prorocentrum species have been used widely in studies on the transfer and fate of OA (e.g., [22,23,24]), field studies on the pelagic component of the food web (i.e., Dinophysis species) are important, in particular during bloom conditions.
Some copepod species graze on Dinophysis spp. [5,6,19,25,26], while some others do not (e.g., [5,19,26,27]). For Dinophysis acuminata Claparède et Lachmann, some grazing experiments have concluded that it is eaten by Acartia clausi Giesbreeht [25], whereas others have not [5]. Only a few studies have investigated what happens after the copepod ingestion of Dinophysis spp. cells, by examining if the faecal pellets contain cells [6,19,26]. These studies have dealt with the copepods Temora longicornis feeding on Dinophysis spp. [26] or Temora longicornis, Calanus helgolandicus and Acartia sp. feeding on D. norvegica. [6,19]. Finally, D. norvegica cells were not observed in the pellets produced by Acartia sp. [6,19].
The present study is the first attempt to understand the impact of a D. acuminata bloom on A. clausi. For this purpose, we examined, for the first time, the A. clausi’s faecal pellet production, egg production, toxin egestion and the occurrence of D. acuminata cells in pellets during the presence of D. acuminata in the sea water. Thermaikos Gulf, an area with little information concerning HABs, was chosen as the study site. In this area, D. acuminata blooms have been recorded during late winter–early spring [28,29].

2. Materials and Methods

Samples were collected from the inner Thermaikos Gulf (40°30′86′′ N, 22°53′15′′ E; NW Aegean Sea, E Mediterranean) during the first week of March 2003 and March 2004. Seawater samples (volume: 0.5–1.0 L) were collected from 2, 10 and 15 m depths. After GF/F filtration, chlorophyll (Chl-a) was determined by fluorometric measurements of acetone extracts [30] in a TURNER Designs TD-700 fluorometer. For phytoplankton composition analysis, seawater was collected from 2, 5, 10 and 15 m depth. Samples were fixed with alkaline Lugol solution and stored at 4 °C until analysis. Phytoplankton identification and counting were performed using the Utermohl method [31]. Conversion from Dinophysis cells to carbon was done using a value of 1194 pg C cell−1 [32]. Conversion of Chl-a to carbon was done with a conversion factor C/Chl-a equal to 50 [33,34].
For OA determination, the method used was based on Zhou et al. [35]. The sample was extracted with aqueous 80% methanol; distilled water was added and extracted again with dichloromethane. The extracts were cleaned-up with SPE (Solid Phase Extraction on silica). The clean eluate was derivatized with a mixture of 3-bromomethyl-7-methoxy-1,4-benzoxazin-2-one (Fluka) and N-Ethyl-diisopropylamine solutions (0.1% in acetone). Analysis was performed with HPLC and fluorescence detection with isocratic conditions, and the mobile phase was acetοnitrile/water 65:35. The OA concentration was calculated using a calibration curve based on injections of standard OA solutions.
Zooplankton for identification was collected with oblique tows from the bottom (~15 m) to the surface, using a 200 µm WP-2 net with a non-filtering cod end. The content of the cod end was fixed immediately and preserved in a 4% buffered-formaldehyde sea-water solution. In the lab, all individuals were identified and counted in an aliquot (1/4 or 1/2) of the whole sample, which was obtained with a Folsom plankton sample splitter.
Copepods for the egg and faecal pellet production experiments were also collected by oblique tows within the 0–15 m layer, using a 200 μm WP-2 net equipped with a large non-filtering cod-end (10 L). On deck, the content of the cod end was diluted in a 25 L thermo-box containing seawater collected from the surface and 10 m depths, which was brought, within two hours, to the lab for estimation of the egg and pellet production.
There, A. clausi females were sorted under a dissecting microscope, and three to four undamaged individuals were transferred to each of ten 620 mL screwcap polycarbonate bottles filled with prescreened well-mixed seawater (150 μm) from the surface and 10 m depth. In addition, six bottles without animals were used as controls. All bottles (5 + 3 for eggs and 5 + 3 for pellets) were left for 24 h in ambient temperature and dim light photoperiod. After that, eggs and faecal pellets were collected using a sieve (60 and 20 μm for eggs and pellets, respectively) and counted.
Eggs were kept for another 48 h in filtered (GF/F) seawater to estimate hatching success. A. clausi faecal pellets were kept for examination of their content. Faecal pellets were placed for 2 h in 2% glutaraldehyde in seawater, rinsed three times with seawater and placed for 30 min in a solution of 0.5% OsO4 in seawater (all seawater used was filtered using GF/F). Faecal pellets were rinsed three times with filtered distilled water (0.45 µm) and were placed on glass plates covered with gelatine, after which they were dehydrated gradually from 30% to 100% ethanol. The samples were then dehydrated by CO2 critical point drying system and coated with Au-Pd or Pt (20 nm). Pellets were observed in a scanning electron microscope (SEM) under 20 kv accelerating voltage and their content recorded.

3. Results and Discussion

D. acuminata densities were low during the first period (March 2003) of this study (<100 cells L−1) whereas in the second period (March 2004) they reached 10,700 cells L−1. The 2003 period represents a pre-bloom situation as the bloom occurred from April to May. The 2004 period, represents a bloom situation, which occurred between February and March. This is consistent with the D. acuminata blooms period in the Thermaikos Gulf mostly occurring between late December and early May (as reported from 2000 to 2004) with densities varying from ~2000 to 85,000 cells L−1 [29,36]. Although the percentage of D. acuminata cells in both years was always less than 1% of the total phytoplankton density, in 2004 it made up to 18% of the total phytoplankton carbon (Table 1).
In 2003, mesozooplankton abundance included cladocerans (28–50%), appendicularians (30–42%) and copepods (6–12%); whereas in 2004 included lamellibranch larvae (28–64%), appendicularians (11–37%) and copepods (21–27%). A. clausi was the dominant copepod for both years, constituting approximately ~60% of the total copepods abundance (Figure 1). A. clausi is the typically dominant copepod in this area during winter and early spring [37,38].
The A. clausi egg production rate was much higher in 2004 than in 2003 (F = 5.48, p < 0.05, n = 8) indicating no or a not detectable effect by the higher density of D. acuminata recorded in 2004. Concerning hatching success, the lack of measurements in 2003 does not allow us to compare with the values obtained in 2004, which fall within the literature range for A. clausi feeding with non-toxic (e.g., [39,40,41] and toxic food (Alexandrium minutum: [4]). Clearly, the increase of the egg production rate in 2004 could be related to the food quality rather than the food quantity. This is supported by the fact that the faecal pellet production rate between the two periods was similar (Table 2), despite the decrease of phytoplankton density in 2004 (Table 1).
On the other hand, the relative densities of dominant phytoplankton groups between the two periods were comparable (Figure 2). The A. clausi pellets examined in both periods, contained essentially broken Chaetoceros sp. and Pseudonitchia sp. (covering approximately 80% of the surface examined, the rest being amorphous material), indicating a lack of any striking phytoplankton differences in the feeding conditions. Concerning the microzooplankton food component, it was essentially composed by tintinnids (90–150 µm) in 2003, whereas in 2004, small aloricate forms (mainly oligotrichida) dominated (70% being <50 μm) (Giannakourou, A., unpublished data).
In both periods, no tintinnid loricates were observed in A. clausi pellets. Our hypothesis was that the amorphous material of the pellets is originated essentially from oligotrichida forms, as A. clausi prefers oligotrichous ciliates, when feeding on a culture of mixtures of oligotrichous ciliates, dinoflagellates and diatoms [42]. Hence, the dominance of small oligotrichous ciliates in 2004 might sustain the much higher A. clausi egg production, masking, at the same time, a possible impact of the D. acuminata bloom.
However, beyond these speculations, a robust explanation for this increase cannot be safely formulated, as the A. clausi egg production rate is affected in opposite ways depending on the different food species and their mixture [40]. Finally, although the D. acuminata bloom reached up to 10,700 cells L−1 in 2004, it appeared that, without its dominance in the available food items, no impact on A. clausi egg and faecal pellet production could be identified.
No D. acuminata cells were found in the A. clausi pellets examined during the pre-bloom period (2003), which is clearly related to the low density of D. acuminata in the phytoplankton community in terms of both cells and carbon (Table 1). During 2004, 11% of the pellets, included one or two intact D. acuminata cells, which corresponds to an egestion rate of ~1.0 D. acuminata cell ind−1 d−1 (considering the pellet production rate in 2004; Table 2). This could suggest that these cells were occasionally ingested by A. clausi and could explain why grazing experiments at similar D. acuminata cell densities and percentages of the total phytoplankton density, as in the present study, showed a low ingestion rate, concluding that D. acuminata was not ingested by A. clausi [5].
The SEM micrographs (Figure 3) showed that all D. acuminata cells in the pellets were almost intact (only one slightly open), thus, incompletely digested. In contrast, the other material accompanying the intact D. acuminata cells (essentially Chaetoceros sp. and Pseudonitchia sp.) was broken into small pieces, and no D. acuminata or other dinoflagellate fragments were present, indicating a good digestion. Incomplete digestion of Dinophysis has been also found for Calanus helgolandicus feeding on Dinophysis norvegica [6,19] and Temora longicornis feeding on Dinophysis spp. [5,26].
The toxin outflux by A. clausi was calculated, during the bloom in 2004, when D. acuminata cells density was high and the species represented up to nearly 20% of the total phytoplankton biomass. For that purpose, we used the given A. clausi egestion rate (1.0 D. acuminata cell ind−1 d−1), the mean values of D. acuminata density, A. clausi abundance and measured D. acuminata cell toxicity (Table 1).
For the calculations, depth integrated values of D. acuminata density and A. clausi abundance were used (a 15 m water column considered as representative of the area). The resulting toxin outflux from the A. clausi population in the study area was close to 110 ng OA m−2 d−1 or lower depending on the retention of OA by A. clausi. This retention is probably low, as it is for the DSP toxins ingested by A. clausi [43] and as for Centropages typicus feeding on D. acuta [44]. The resulting toxin outflux is insignificant compared to the mean toxin concentration from the whole D. acuminata population in the Thermaikos Gulf (888 × 103 ng OA m−2).
The potential grazing impact of the dominant copepod A. clausi was estimated from literature values of its ingestion rate, feeding upon D. acuminata at similar conditions as in the present study. In such conditions (i.e., D. acuminata representing <1% of the phytoplankton cell numbers), the ingestion rate is low (2.7 ± 3.3 cells ind−1 d−1, [5]). Assuming that such a low ingestion rate is also the case in the Thermaikos Gulf, then the grazing impact of A. clausi on D. acuminata during the study period was low (close to 0.01% per day). This is probably also valid for other years.
In fact, maximum abundances of D. acuminata usually reported in Thermaikos Gulf, range from 50,000 to 85,000 cells L−1 [29,36,45], although patches with densities of D. acuminata as high as 1.0 × 106 cells L−1 were recorded in the port of Thessaloniki (Thermaikos Gulf) in April 2004 [29]. Within this range, even if A. clausi increases its ingestion rate up to ~200 cells ind−1 d−1 (which can happen above 30,000 cells L−1 of D. acuminata: [25]) and is present at the maximum density reported in the area (4500 ind m−3: [46]), the grazing impact would still be low (close to 1% per day).

4. Conclusions

Summarizing the outcomes of this study, the faecal pellet and egg production of the dominant copepod A. clausi was not associated with the D. acuminata bloom in Thermaikos Gulf. Despite the blooming D. acuminata densities, reaching 10,700 cells L−1 during the experiment (or 85,000 cells L−1 during the phytoplankton growth period of that year), it is hypothesized that A. clausi feeds upon other prey, such as ciliates. The literature ingestion rate values at similar conditions also indicate a low grazing impact on D. acuminata cells. Considering that D. acuminata was not dominant in the available food items, this could be also related to the differential digestion of the toxic cells.
As also indicated by the Dinophysis cells condition in the faecal pellets, it is suggested that the ingestion of toxic cells does not always mean their digestion and impact on the grazer, such as in egg production. In addition, the toxin outflux through the D. acuminata cells found in A. clausi faecal pellets was negligible compared to the toxin content of D. acuminata cells in the water column. Finally, the output of this study can significantly contribute as a base for future research on the interactions between planktonic grazers and algae producing DSP toxins, considering all available food items as well as food selectivity.

Author Contributions

Conceptualization C.F., E.D.C., I.M., K.P., C.S. and E.G.; methodology C.F., E.D.C., I.V., S.Z., I.M., G.A. and I.H.; software C.F.; validation C.F., E.D.C., I.V., S.Z., C.S. and E.G.; formal analysis C.F. and E.D.C.; investigation C.F., E.D.C. and K.P. All authors have read and agreed to the published version of the manuscript.


This work was supported by the European Commission (Research Directorate General-Environment Program-Marine Ecosystems), through the FATE project “Transfer and Fate of Harmful Algal Bloom (HAB) Toxins in European Marine Waters” (contract number EVK3-2001-00055, contract holder E. Granéli) as part of the EC EUROHAB cluster. Part of this work was supported by the JERICO-S3 project. This project has received funding from the European Union‟s Horizon 2020 research and innovation programme under grant agreement no. 871153.

Data Availability Statement

Not applicable.


The authors wish to thank G. Papas, C. Charalambous and C. Wexels Riser for their help in the field work and sampling, as well as, C. Pyrgaki, T. Kanelopoulos and V. Galanopoulos for their support in the chemical analyses and scanning electron micrographs. Thanks are also due to L. Kiousi for helpful comments.

Conflicts of Interest

All authors declare that they have no conflict of interest to disclose in the context of this study.


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Figure 1. The mean water column copepod abundance (ind m−3) during early March 2003 and March 2004 in Thermaikos Gulf.
Figure 1. The mean water column copepod abundance (ind m−3) during early March 2003 and March 2004 in Thermaikos Gulf.
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Figure 2. The mean phytoplankton composition (cells 104 L−1) during early March 2003 and 2004 in Thermaikos Gulf.
Figure 2. The mean phytoplankton composition (cells 104 L−1) during early March 2003 and 2004 in Thermaikos Gulf.
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Figure 3. Scanning electron micrographs of A. clausi faecal pellets content collected in the Thermaikos Gulf. (A,C): faecal pellets covered partially with the peritrophic membrane showing a Dinophysis acuminata cell magnified in micrographs (B,D), respectively.
Figure 3. Scanning electron micrographs of A. clausi faecal pellets content collected in the Thermaikos Gulf. (A,C): faecal pellets covered partially with the peritrophic membrane showing a Dinophysis acuminata cell magnified in micrographs (B,D), respectively.
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Table 1. The range of Chl-a, phytoplankton density and D. acuminata parameters over the sampling period.
Table 1. The range of Chl-a, phytoplankton density and D. acuminata parameters over the sampling period.
Period (March)20032004
Chl-a (μg L−1)4.1–5.30.2–2.7
Total phytoplankton density (×105 cells L−1)19.0–46.09.9–28.8
Range of D. ac. density (cells L−1)<100600 to 10,700
D. ac.% in total phytoplankton (% cells)<0.01<0.5
D. ac.% in total phytoplankton (% carbon)<0.061.7–18
OA in D. acuminata cells (pg cell−1)3.7–8.64.4–14.0
Table 2. The mean water column values of A. clausi parameters over the sampling period (mean ± SE).
Table 2. The mean water column values of A. clausi parameters over the sampling period (mean ± SE).
Period (March)20032004
faecal pellet production (pellets ind−1 d−1)6.8 ± 2.6 (n = 9)8.6 ± 2.8 (n = 3)
egg production rate (eggs ind−1 d−1)15.8 ± 5.4 (n = 7)47.6 ± 9.0 (n = 4)
egg hatching success (% d−1)Not measured69.1 ± 3.7 (n = 5)
D. acuminata cells per faecal pellet0.05 ± 0.2 (n = 30)0.11 ± 0.4 (n = 53)
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MDPI and ACS Style

Frangoulis, C.; Christou, E.D.; Varkitzi, I.; Zervoudaki, S.; Maneiro, I.; Svensen, C.; Pagou, K.; Assimakopoulou, G.; Hatzianestis, I.; Granéli, E. Impact of a Dinophysis acuminata Bloom on the Copepod Acartia clausi: First Indications. Water 2022, 14, 2204.

AMA Style

Frangoulis C, Christou ED, Varkitzi I, Zervoudaki S, Maneiro I, Svensen C, Pagou K, Assimakopoulou G, Hatzianestis I, Granéli E. Impact of a Dinophysis acuminata Bloom on the Copepod Acartia clausi: First Indications. Water. 2022; 14(14):2204.

Chicago/Turabian Style

Frangoulis, Constantin, Epaminondas D. Christou, Ioanna Varkitzi, Soultana Zervoudaki, Isabel Maneiro, Camilla Svensen, Kalliopi Pagou, Georgia Assimakopoulou, Ioannis Hatzianestis, and Edna Granéli. 2022. "Impact of a Dinophysis acuminata Bloom on the Copepod Acartia clausi: First Indications" Water 14, no. 14: 2204.

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