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MESO-SCALE DIVERSITY OF PLANCTONIC CILIATES ALONG A LATITUDINAL

AND PRODUCTIVITY GRADIENT IN THE EASTERN MEDITERRANEAN SEA
Magiopoulos I.1,2, Pitta P.1
1
2

Institute of Oceanography, Hellenic Centre for Marine Research, iordanis@her.hcmr.gr, vpitta@her.hcmr.gr,

Biology Department, University of Crete

Abstract
During April 2006, surface samples were collected at 28 stations at 10nm distance from each other along a latitudinal transect
from the North to the South Aegean Sea characterized by the influence of the Black Sea water in the North and a pronounced
oligotrophy towards the South. Ciliate abundance, size classes and tintinnid diversity were determined at all stations. Exceptionally high abundance values were measured (mean: 2300 ciliates l-1, max: 10740 ciliates l-1), by large higher than previously reported in this area. Ciliate total abundance in the South Aegean was lower than in the North. Nanociliates (<30m)
clearly dominated the ciliate community (52 to 95% of total abundance). The tintinnids community was characterised by a
large meso-scale variability in terms of species number and community composition. The quantitative and qualitative characteristics of the ciliate community were not consistently related to the productivity gradient of the investigated area but are
also explained by the complicated hydrography of the Aegean Sea induced by the input of the Black Sea and the Levantine
waters.

Keywords: ciliates, tintinnids, Aegean Sea, meso-scale, diversity.

1. Introduction
Pelagic ciliates play a crucial role in the pelagic environment since they are considered to constitute
the main link of the microbial to the classical food web. In addition, in the Eastern Mediterranean
where primary productivity and biomass are dominated by the pico- and nanosized phytoplankton
(Christaki et al., 2001,; Siokou-Frangou et al., 2002), planktonic ciliates are the main grazers since
copepods are unable to crop these size classes efficiently (Marshall, 1973).
Picoplankton is grazed by nano-sized protists (flagellates and ciliates) while nanoplankton is
grazed mainly by microsized ciliates (Pierce & Turner, 1992). Thus ciliates play a major role in
the transfer of energy and material through the pelagic food web (Beers & Stewart, 1967; Pierce &
Turner, 1992). Moreover in oligotrophic areas such as the E. Mediterranean the diverse trophic mode
and size classes of ciliates give them an additional advantage of different food resources.
The Aegean Sea is a complex marine environment with high variability. The southern part has
been characterized as one of the most oligotrophic areas of the Mediterranean Sea on the basis of
productivity and light attenuation (Ignatiades, 1998) whereas the north Aegean Sea is considered to
be more productive due to higher nutrient input affected by the Black Sea Waters passing through
the Dardanelles straits (Poulos et al., 1997).
In an attempt to address the possible impact of such a variable environment on the diversity of
planktonic ciliates, samples were taken at a meso-scale level along a latitudinal and productivity gradient in the Aegean Sea. To our knowledge, no other study exists on the ciliates meso-scale diversity
along such a diverse environment.

2. Materials and Methods

Samples were collected in April (1st to 5th) 2006 at 28 stations along a latitudinal transect from
the North to the South Aegean (from 40o to 36o N, Fig. 1) during the second PELAGIAL Project.
These stations had a distance of 10nm (18,52 km) from each other. All samples were collected from
the surface using a centrifuge pump and used for ciliate counting.
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Fig. 1: Map of the stations (from Google Earth).

For ciliate enumeration, 500 ml of whole water were preserved with acid Lugols solution (2%
final concentration) and stored at 4oC in the dark. An Olympus IX70 inverted microscope, equipped
for phase contrast microscopy, was used at 20x magnification.
Ciliates were distinguished in distinct categories: (1) Aloricate ciliates, (2) Tintinnids. Furthermore, aloricate ciliates were divided into different size classes (1) less than 18 m, (2) 18 to 30
m, (3) 30 to 50 m and (4) more than 50 m. Tintinnids were identified to species level based on
lorica shape and dimensions after Jrgensen (1924) and Balech (1959). The aloricate cell size and
the tintinnid length and diameter were measured with an ocular micrometer and converted into cell
volumes using appropriate geometric formulae (Peuto Moreau, 1991).
Multivariate analysis was performed on the species abundance data, using a non-metric
multidimensional scaling (MDS, Field et al., 1982) using the PRIMER software package. Similarities
among samples were calculated by means of the Bray-Curtis index (Bray and Curtis, 1957) and a
log(x+1) transformation was applied on the abundance data prior to the analysis in order to normalize
the data and to avoid skew ness. Tintinnid diversity was calculated using the Shannon-Wienner
Diversity Index H (Shannon and Weaver, 1949).

3. Results
3.1 TOTAL CILIATE COMMUNITY AND SIZE CLASSES

Total ciliate density ranged from 386 to 10752 cells l-1. A decrease in total ciliate abundance was
found from north to the south, with extremely high values around station 9, at which a ciliate bloom
was observed (Fig. 2). This bloom was due to nanociliates (50% of ciliate community) (< 18m)
followed by larger ciliates (18 to 30 m). In general, aloricate species smaller than 18 m were by
far the dominant size class. Their abundance varied from 148 to 8166 cells l-1 and they accounted
for 36 to 76% of total abundance followed by larger ciliates (18 30 m, 14 to 36% ; 30 50 m,
3 42% ; >50 m, 0.2 6% ; tintinnids, 0.2 14%).

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Fig. 2: Abundance of tintinnids and four size classes of aloricate ciliates along the transect sampled.

3.2 TINTINNIDS

Tintinnids also presented a noticeable change in abundance along the north to south transect, from
4 to 310 cells l-1 (Fig. 3). A total number of 2000 specimens were counted and identified, belonging
to 24 genera and 38 species. Common tintinnid species were Salpingella curta (63% of the total
tintinnid abundance, found in 25 stations), Eutintinnus tubulosus (10%, 23 stations), Steenstrupiella
steenstrupii (5%, 15 stations) and Codonellopsis pusilla (5%, 11 stations). Important differences
were found in the tintinnid community composition between stations as the Shannon Wiener diversity
index increased from North to South (Fig. 3).

Fig. 3: Tintinnid abundance along the transect sampled compared to Shannon-Weiner diversity index.

The Bray-Curtis similarity index was used to compare the tintinnid community composition
between consecutive stations. This comparison resulted in three distinct areas in the Aegean Sea,
North, Central and South Aegean Sea (Fig. 4). The MDS Analysis (Fig. 5) verified the separation of
the three areas.

Fig. 4: Comparison of the tintinnid community composition between consecutive stations using the Bray-Curtis similarity
index.

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Fig. 5: MDS diagram which compares the stations in terms of tintinnid community composition.

The tintinnid community was very diverse in terms of morphology and size. Tintinnid community
length, diameter and biovolume increased from North to the South. The community biovolume
varied from 1103 to 20391 m3 (Fig. 6).

Fig. 6: The biovolume of tintinnids along the transect sampled.

4. Discussion
4.1 TOTAL CILIATE COMMUNITY AND SIZE CLASSES

Total ciliate abundance was the highest ever reported in this area with a mean value of 2300
cells l-1. Previous studies in the North and South Aegean Sea during the same season (March and
April 1997) report much lower abundances ranging from 100 to less than 2000 cells l-1 (Pitta and
Giannakourou, 2000). The total ciliate abundance of the present study was also higher compared to
the rest of the Mediterranean (Pitta et al., 2001) and the Catalan Sea (Dolan & Marrase, 1995).
According to the results of the present study, the southern stations presented low abundances
relative to the northern ones, this being in agreement with Pitta and Giannakourou (2000).
Nanociliates (<18 m) were by far the dominant size class in the majority of stations as has been
also found in other studies (Lynn et al., 1991, Revelante and Gilmartin, 1983). In previous studies
from the area under investigation nanociliates were the dominant size class in the N. Aegean Sea
(Pitta and Giannakourou, 2000) whereas at the S. Aegean stations the larger ciliates (1830 m)
were dominant. In contrast, Dolan and Marrase (1995) found that nanociliates constituted only the
8% of the ciliate community in the Western Mediterranean. Nanociliates accounted for 23% of the
integrated abundance along a Tran Mediterranean transect with species less the 30 m being the
dominant ciliate size class (Pitta et al., 2001).
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The nanociliate dominance in the Aegean Sea may be explained by its oligotrophic character. In
oligotrophic areas, the phytoplankton is dominated by the pico- and nano- size fractions. This has
been found in the Levantine Basin (Li et al., 1993) as well as in other oligotrophic regions (Gieskes
et al., 1979; Platt et al., 1983). The scarcity of resources may force the system towards a web of
smaller organisms, not only the autotrophic ones but also their predators such as ciliates.

4.2 TINTINNID COMMUNITY

Tintinnid abundance decreased from North to the South. The analysis of the tintinnids community
structure indicated that the Aegean Sea can be separated in three main areas, the North, Central and
South Aegean Sea. The South Aegean Sea (stations S1 to 19) was characterized by medium tintinnid
abundances (26 tintinnids l-1) and higher diversity compared to the other areas. In the South Aegean,
species of the genus Eutintinnus (E. tubulosus and E. lusus) were common and also Steenstrupiella
steenstrupii and Salpingella curta.
The Central Aegean Sea (stations 18 to 11) presented the lowest values of tintinnid abundance
(10 cells l-1) and low diversity. Salpingella curta dominated in most stations (there is a negative
correlation between S. curta abundance and Shannon-Weiner Diversity Index) combined with the
lack of a noticeable presence of any other tintinnid species (except few E. tubulosus in half of the
stations).
In the North Aegean Sea, Salpingella curta was found in high abundances some of them indicating
a bloom of that species. As a consequence, the North Aegean Sea stations showed high tintinnid
abundance and variable diversity. Other common species were Eutintinnus tubulosus, Codonellopsis
pusilla, Stenosemella nivalis and two Tintinnopsis species.
The increase in tintinnid community lorica length from North to the South Aegean Sea can
be explained by the distribution of common tintinnid species along the transect. At the northern
part of the transect, the smaller tintinnid species dominated, whereas at the southern part, species
of the much larger genera Eutintinnus and Steenstrupiella dominated. We assume that this may
be explained by the ability of larger tintinnids to filter higher water masses which gives them an
advantage in an oligotrophic environment compared to smaller ones. Furthermore, size can also
convey the advantage of lower minimum food requirements in terms of bulk concentrations relative
to smaller ciliates (Rassoulzadegan, 1993).

5. Acknowledgements
The authors would like to acknowledge support by HCMR in the framework of the project
PELAGIAL as well as the captain and the crew of the R/V Aegeo for their assistance during the
sampling.

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