tintinnids assemblages and abiotic forcing cycles in a coastal ionian site, central mediterranean

33 Pages·2007·0.58 MB·English

JOURNALOFPLANKTONRESEARCH j VOLUME29 j NUMBER6 j PAGES495–508 j 2007
Temporal succession of tintinnids in
the northern Ionian Sea,
Central Mediterranean
RAFFAELLASITRAN1,ALESSANDROBERGAMASCO2,FRANCODECEMBRINI2ANDLETTERIOGUGLIELMO1*
1DIPARTIMENTODIBIOLOGIAANIMALEEDECOLOGIAMARINA,UNIVERSITA` DIMESSINA,SALITASPERONE31,98166MESSINA,ITALYAND D
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2CNR-ISTITUTOPERL’AMBIENTEMARINOCOSTIERO,SEZIONEDIMESSINA,SPIANATAS.RAINERI86,I-98122,MESSINA,ITALY w
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*CORRESPONDINGAUTHOR:[email protected] ed
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ReceivedDecember7,2006;acceptedinprincipleMarch1,2007;acceptedforpublicationApril13,2007;publishedonlineMay18,2007 h
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Communicatingeditor:K.J.Flynn ://a
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Vertical distribution, abundance, diversity and community structure of tintinnid assemblages were em
investigated at monthly intervals at one fixed station in the coastal Ionian Sea, Central ic
.o
Mediterranean, between March 2003 and May 2004. A total of 79 species belonging to 23 up
genera were identified; Dadayiella ganymedes, Steenstrupiella steenstrupii, Craterella torulata and .co
m
Stenosemella nivalis contributed up to 50% of the tintinnid abundance. Two main changes in /p
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species composition as well as abundance were recorded, one in May and the other in November– n
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December. In general, species richness remained unchanged along the watercolumn (7 +1 species t/a
at each depth) while about 40% of the overall richness (31 species of 79) was represented by rtic
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species that were found only once. H’ ranged from 1.3 to 2.7, with the maximum values from -a
b
September to January (H’ 2.3–2.7) generally at the deep chlorophyll maximum depth. A cluster stra
analysis showed that both abundance and diversity were strongly influenced by the hydrological c
t/2
characteristics of the site. Tintinnid diversityappeared to be positively linked to salinity (Spearman 9
/6
0.47, P,0.01) while negatively to chlorophyll. Our findings support the idea that the rapid /4
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shifts between the two dominant lorica oral diameter size-classes (29 and 34mm) could be con- 5
/1
sidered a sensitive indicatorof changes between coastal and pelagic ecosystems. Our data on tintin- 49
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nid assemblages are coherent with those found along a longitudinal transect in the Mediterranean 7
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and contribute to the knowledge of tintinnid diversity and richness in a peculiar oceanographic b
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coastal area of the Central Mediterranean Sea, a crucial point in the W- to E- tintinnid g
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biogeography. e
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INTRODUCTION Mediterranean, tintinnids are believed to be one of the ril 2
main consumers of the primary production (41%, Pitta 01
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Among microzooplankters (20–200mm), tintinnids rep- et al., 2001;Fonda Umani and Beran, 2003;Calbet and
resent a relativelyeasily identifiable taxon. Classification Landry, 2004) and their crucial role in the food web is
criteria based on theirlorica morphology made possible widely acknowledged (Capriulo and Carpenter, 1983;
the development of extensive systematic monographies Pierceand Turner,1992).
since the beginning of 20th century (Jo¨rgensen, 1924; Density, structure and diversity of tintinnid commu-
Kofoid and Campbell, 1929). nities have often been found to be somehow correlated
Though representing only a small part of the plank- with chemical, physical and biological features of the
tonic ciliate community (less than 10% of biomass, watercolumn.Hence,thetintinnidassemblagecancon-
Dolan, 2000), in an oligotrophic system dominated by tributetoacharacterizationofawatermassandongoing
pico- and nanoplanktonic fractions such as the Central dominating processes. For example, separation of niches
doi:10.1093/plankt/fbm032,availableonlineatwww.plankt.oxfordjournals.org
#TheAuthor2007.PublishedbyOxfordUniversityPress.Allrightsreserved.Forpermissions,pleaseemail:[email protected]
JOURNALOFPLANKTONRESEARCH j VOLUME29 j NUMBER6 j PAGES495–508 j 2007
following an increase of vertical structure of the water long-shore stationary current and the formation of
column is considered as a basic mechanism stimulating small-scale cyclonic gyres (Adragna and Salusti, 1990).
an increase of diversity of the tintinnid assemblages Both these features are constrained within the shelf
(Cariou et al.,1999;Dolan, 2000).At the Mediterranean zone by the general circulation of the Western Ionian
scale, the West-to-East increase in species richness, and Sea and the coastal geomorphology that exhibit a
in taxonomic and morphological diversity of tintinnids narrow shelf and very steep slopes. In the euphotic
have been correlated to the decrease in chlorophyll a layer, several water masses can be traced. The surface
concentrations and the deepening of the deep chloro- layer (0–30m) is dominated by the Ionian Surface
phyllmaximum(DCM)(Dolan,2000). Water (ISW) whereas lower salinity ((cid:2)38.45) character-
Local scale studies have dealt with tintinnid assem- izes the water underneath: this latter is formed in
blages in both coastal and pelagic areas particularly in the Straits of Messina by mixing processes between the D
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the Western Mediterranean (Catalan Sea, Dolan and Tyrrhenian Surface Water (TSW) (s (cid:2)27.9) and the w
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Marrase´, 1995; Bay of Villefranche, Cariou et al., 1999 upwelled Levantine Intermediate Water (LIW) (st load
and Go´mez and Gorsky, 2003;Gulf of Naples, Scotto di (cid:2)28.9) and flows then southward along the Sicilian e
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Carlo et al., 1985; Modigh and Castaldo, 2002), the coast (Bohm et al.,1987). fro
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Adriatic (Gulf of Trieste, Cabrini et al., 1989) and the The study site (Fig. 1) is located along the Eastern h
NorthernIonianSea(GulfofTaranto,SalentoPeninsula, coastofSicilywhereaMarineProtectedAreawasestab- ttp
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Moscatello et al., 2004).For those sites where long-term lished in 1989 in front of Acicastello (5km north of ://a
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observations of the tintinnid assemblages are available, Catania).Recently,specificstudieshavebeencarriedout a
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dominantspeciesexhibitedrecurrentpatternsofpresence in the area dealing with benthic biodiversity (Cantone em
and a link with trophic conditions has been suggested etal.,2003),planktoniccommunitycycles(Minutolietal., ic.o
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(ModighandCastaldo,2002;Go´mezandGorsky,2003). 2005) and the link between coastal and pelagic systems p
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In the Eastern Mediterranean previous works refer to (Bergamasco et al., 2005).In the area, the thermohaline o
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the Aegean Sea (Mihalatou and Moustaka-Gouni, structure of thewatercolumn is influenced by two main /p
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2002), Levantine waters (Abboud-Abi Saab, 1989; processes:horizontaladvectionalongthecoastandverti- n
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Lakkis, 2001) and North African coasts (Bay of Tunis, cal mixing. The former is linked to the mixed waters t/a
Daly Yahia et al., 2001).No information is available for originating in the Messina Straits: their density is (cid:2)28.4 rtic
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the Western Ionian Sea while studies on tintinnid popu- s and in summer these nutrient-rich waters flow south- -a
t b
lations have been performed in nearby areas, the ward in a sub-surface position (layer 30–50m). The stra
SouthernThyrrhenianSeaandintheStraitsofMessina latter drives the system towards a perfect homothermic c
t/2
wherestructureandcompositionoftintinnidcommunity structure (158C) typical of winter conditions. At the end 9
/6
were found to reflect the hydrodynamic functioning of of summer, the water column is completely invaded by /4
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thispeculiarecosystem(SparlaandGuglielmo,1994). deeperandsaltier(38.6)wateroftheWesternIonianSea 5/1
This work aims at describing the tintinnid commu- (Galletta et al., 2005). This condition is confirmed by 49
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nity in a coastal site of the Central Mediterranean high nutrient concentrations, mainly nitrates (.5.0mM), 7
7
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(Western Ionian Sea) highlighting the most interesting coming from below the nutricline. These two processes b
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aspects linked to the hydrological parameters. The tin- induceinthecoastalareaaconditiontypicalofapelagic g
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tinnid assemblages are studied in terms of abundance system, where the zooplanktonic component exhibits a es
and diversity in relation to the water column structure great species variability (Guglielmo, 1976; Guglielmo t o
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and seasonal cycle. The main objective was to identify etal.,1995). 04
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“key” species and/or associations of species and to link p
them to the cycles of the abiotic forcings that drive the ril 2
Sampling and laboratory procedures 0
ecological processes. The results are then compared 1
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with similar findings in other Mediterranean coastal Conductivity-temperature-depth (CTD) and water
ecosystems. sampling were performed monthly from March 2003 to
May 2004 at a coastal station called Acicastello
(37832.25’N 15809.02’E, water column depth (cid:2)100m)
located 1nmoffshore.
METHOD
Vertical profiles were recorded with a SEA BIRD 9/
11plus CTDequipped with sensors of temperature, con-
Study site
ductivity, pressure, Beckman/YSI for dissolved oxygen
For the Eastern coast of Sicily, mesoscale studies on and Turner SCUFAII for chlorophyll a fluorescence.
hydrodynamics described the presence of a southward WatersampleswerecollectedusingNiskinbottlesatthree
496
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R.SITRANETAL. TINTINNIDSINTHENORTHERNIONIANSEA
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Fig.1. ThedotindicatesthepositionofthestudysitealongtheSiciliancoastoftheIonianSea(CentralMediterranean).Themainpathsof n
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themesoscalehydrodynamicfeatureshavebeensketchedaccordingtoMalanotte-Rizzolietal.,1997andLermusiauxandRobinson,2001(AIS: t/a
AtlanticIonianStream;MRV:MessinaRiseVortex). rtic
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-a
b
depths according to the fluorescence profiles: surface presence/absence of each species and its average LOD, stra
layer (10m), DCM layer (35–50m) and below-DCM for each sample the community Average LOD and the c
t/2
layer (70m). In the period of a mixed water column, communityMedian LOD were calculated (43 samples). 9
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intermediatesampleswerecollectedat50mdepth. Chlorophyll a concentrations (Chl a) were measured /4
9
A 10L sample for each depth was immediately con- as index of phytoplankton biomass. One liter of water 5/1
centrated to 200mL by slowly and gently pouring the from the Niskin bottle was filtered immediately on 49
4
water through a 10mm-mesh (Fonda Umani and Whatman filters (GF/F 47mm) and stored at 2208C 7
7
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Milani, 1990). Concentrated water samples were then until analysis. The material on the filters was extracted b
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fixed with Lugol’s solution (2% final concentration) and in acetone (90%) and placed in a spectrofluorometer g
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stored indarkglass bottles. (Varian mod. Cary Eclipse). Readings were made at es
Subsamples of 100mL were settled for 24h in stan- 430 and 668nm (Lazzara et al., 1990). A calibration t o
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dard sedimentation chambers and enumeration of tin- curve was obtained by dilutions of pure chlorophyll a 04
tinnids was performed according to Utermo¨hl (1958), (Anacystisnidulans,Sigma). Ap
with an inverted phase-contrast LEICA microscope at Nutrient concentrations (NH4þ, NO32, NO22, PO42) ril 2
0
200(cid:3) magnification equipped with a micrometer. were measured in all samples; samples were filtered and 1
9
Tintinnids were identified using lorica external mor- immediately frozen (2208C). Analyses were performed
phology and dimensions and species descriptions found by a spectrophotometer Varian mod. Cary 50 on the
in Kofoid and Campbell (1929), Balech (1959), sample quickly defrozen according to Aminot and
Tre´gouboff and Rose (1957), Rampi and Zattera Chassepied (1983), Strickland and Parson (1972) and
(1982), Laval-Peuto and Brownlee (1986). Lorica oral Parsonet al. (1984).
diameters (LODs) were measured with an ocular
micrometer. Abundance, richness and Shannon diver-
Data analysis
sity H’ were calculated for each sampling depth and for
the water column as a whole by averaging (abundance) The statistical analyses of the data were performed with
or pooling (species) the data. On the basis of the the Statgraphics package (Legendre and Legendre,
497
JOURNALOFPLANKTONRESEARCH j VOLUME29 j NUMBER6 j PAGES495–508 j 2007
1984).One-way ANOVAwas employed to test for differ-
ences between depths, seasons and clusters of data after
a suitable transformation to ensure the homogeneity of
the variances. A jack-knife estimation of expected
species richness as a function of the number of samples
(Magurran, 1988) was performed with the Biodiversity
Professional software (McAleece et al., 1997) from the
Scottish Association for Marine Scienceweb site http://
www.sams.ac.uk/research/software/). Primer 5 (Clarke
and Gorley, 2001) was used to study the changes in tin-
tinnid assemblages with time (cluster analysis, similarity D
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percentages). Abundance data were normalized to the w
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total abundance and [log(1þx)]-transformed. loa
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Correlations among abiotic (T, S, nutrients) and e
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biotic (Chl a, abundance, species richness, Shannon fro
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dthivreeersitsyamfoprlintgintdinenptidhss) bvyariaanbalelysziwngerePetaersstoend’sfocroetfhfie- F(ki-gm.ea2n.sCmluesttheroidza;tiSoqnuaorfedtheEuTcl/idSeapnairdsistoafncteh)e. T43hreweatgerrousapmspalrees https
cients and Spearman’s rank coefficients to measure identified: (i) salinity below 38.4 (water originated in the Straits of ://a
Messina); (ii) salinityabove 38.4 and low temperature (Ionian Water) c
linear and non-linear monotonic relationships, respect- a
and(iii)salinityabove38.4andhighertemperatures(ISW). d
ively. Since the former is not recommended for usewith em
skewed data, possible links between variables were eval- ic.o
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uated and possibly confirmed by using the latter, which p
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is less sensitive to outliers and therefore more robust. (Period II) resulted in lower chlorophyll values o
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(0.1mgChl-a L21 on average) and a further increase of /p
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nitrates (.5mM) due to the mixing with deeper water, n
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rising from belowthe nutricline (Fig.4). t/a
RESULTS In the study period, inorganic nitrogen and phos- rtic
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phorus concentrations were generally high. Ammonium -a
Hydrological features exhibited concentrations close to 1mM (0.83+0.66 bstra
In summer, the 0–100m layer showed a typical seaso- mM) with increases in summer (max 3.35mM in c
t/2
nal trend in the thermohaline structure with higher August at 50m). Nitrate concentrations (2.76+ 9
/6
values of temperature and salinity at surface (27.848C 1.45mM) always exceeded 3mM near the seabed, /4
9
and 38.94); temperature decreased with depth to a whereas in the uppermost layers they reached the 5/1
minimum of 14.938C and salinity showed a relative maxima in winter (max 6.02mM in November). 49
4
minimum of 38.45 at intermediate depths (30–60m) Orthophosphates were higher and more variable at 7
7
2
and a slight increase towards the seabed (38.54). In 10m (0.35+0.26mM, with max 0.99mM in August) b
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winter, Tand S values were low at surface (14.28C and than along the column (0.29+0.19mM), where con- g
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38.67) and the water column was completely mixed. centrations increased in winter (max 0.76mM, es
Isopycnic lines were mainly influenced by temperature November 50m). ANOVA and statistical tests (Fisher’s t o
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in the topmost 30m layer and by salinity underneath; a LSD and Kruskal–Wallis) on nutrient concentrations by 04
summer pycnocline can be distinguished in the layer season showed significant differences for autumn versus Ap
between 20and 70m (27.0–28.5 st) (Fig.2). winter phosphate concentrations(averages and medians, ril 2
0
During the year, different periods could be described P,0.05), for summer versus autumn/winter 1
9
(Fig. 3). From September to January (Period I), in per- ammonium (medians, P,0.05) and for spring versus
fectly mixed conditions the water column is dominated autumn nitrates (averages, P,0.05) whereas differences
by Ionian deepwaters whereas in summer, from May to along thewatercolumn were statistically not significant.
August (Period III) it is influenced by the waters orig- Throughout the year of study, average concentrations
inating in the Straits of Messina. Due to the surface of chlorophyll a were rather low (0.10–0.20mgL21)
heating, they are buoyant in the 30–50m layer (28.4 with a minimum at surface (0.05mgL21) and a
s), where the DCM was located with maximum chlor- maximum (0.45mgL21) at 40m of depth, both occur-
t
ophyll concentrations (up to 0.5mgChl-a L21) associ- ring in July. Vertical profiles showed a recurrent
ated with very high nitrate concentrations (.1mM). maximum between 35 and 50m (.0.4mgChl-a L21)
Homogenization of the water column in late winter in spring-summer which disappeared from October to
498
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Fig. 3. T/S diagram of the 15 monthly CTD profiles collected at Acicastello site in the period march ‘03–may ‘04. Three periods are /6
identifiedaccordingtotheT/Ssignaturesofthewatermasses(seetextforexplanation).WatersofprobableoriginintheStraitsofMessinawere /49
foundinsummerinthe30–50mlayer. 5/1
4
9
4
7
7
2
January, when the values were homogeneous around than 10 species and very few cells per liter were b
0.1mgChl-a L21. recorded in June–August whereas late-autumn maxima, y g
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with more than 20 species were recorded in e
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November–December. After a clear decrease in winter, t o
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Tintinnid abundance and richness increasing values were again recorded in spring. 0
4
Tintinnid abundances ranged from 0 to 58 cell L21 In general, species richness remained unchanged Ap
with an average of 9.3 cell L21. Small differences of withinthe column (7+1 sp.at eachdepth) and showed ril 2
averages and medians were recorded along the column an overall average of 14+6 sp. within the water 01
9
but were not significant (ANOVA, P.0.05). Maximum column (Fig. 6); statistical tests (ANOVA, Fisher’s LSD)
abundances occurred in May 2003, due an increment on the species richness data suitably log-transformed for
of the most frequently observed species Dadayiella gany- standardization highlighted a significant difference
medes (45 cell L21) and in December in the intermediate to occur only between summer and autumn averages
layer, associated to a very high species richness (Fig. 5). (P,0.01).
The comparison of monthly tintinnid species richness The suitability of the sampling strategy (method,
(pooled along the watercolumn) and abundances (aver- effort, etc.) in terms of species richness actually caught
aged for the three sampling depths) revealed similar was evaluated through a jack-knife analysis of the
patterns along the year with highest values in cumulative richness as a function of the number of
late-autumn and spring. Summer minima, with less samples.An underestimate of about 30% was observed.
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JOURNALOFPLANKTONRESEARCH j VOLUME29 j NUMBER6 j PAGES495–508 j 2007
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Fig. 5. Trends of abundance and species richness of tintinnids at fro
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Acicastello from march ‘03 to may ‘04. Abundances were averaged h
uponthethreeconsidereddepthsandstandarddeviationisindicated; ttp
richnessispooledalongthecolumn. s
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Fig. 6. Average species richness, average number of genera and /6
Shannon Index H’ found at Acicastello site, Ionian Sea, Central /49
Mediterranean(n¼15).ErrorbarsshowStandarddeviations. 5/1
4
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4
Fig. 4. Concentrations of N and P nutrients and chlorophyll a at 7
common species, i.e. species exhibiting a number of 7
Acicastello site during the observation period. Modified from 2
Bergamascoetal.(2005). specimens greater than 1% of the overall community, by
were only 17. Analysis of similarity based on tintinnid gu
e
abundances aggregated by genera and [log(1þ st o
x)]-transformed showed that key genera were Dadayiella, n
Structure, composition and occurrence 0
of tintinnid assemblages Eutintinnus and Undella. Table II presents the occurrence 4 A
Duringthestudyperiod,79speciesoftintinnidsbelong- oTfotheelucmidoasttefrtehqeuelinntkspbeectwieesernanthkeedobbyseirnvcerdeaLsiOngDLvOaDri-. pril 2
0
ing to 23 genera were identified; 50% of the specimens 1
ations of tintinnids and the trophic interactions in the 9
belonged to the species D. ganymedes, Steenstrupiella steen-
planktonic compartment the temporal changes of the
strupii, Craterella torulata and Stenosemella nivalis. Four
chlorophyll (averaged for the three sampling depths)
genera constituted the bulk of the population with
and the Median LOD of the tintinnid community were
about 60% of the specimens; 34 species were rare (5%
compared (Table II,lower panel).
overall). Table I presents the tintinnid species list with
the indication of the frequencyof occurrence (on atotal
of 43 samples) and maximum abundance. About 40%
Diversity
of the overall richness (31 species of 79) was represented
by species that were found only once: 20 of them in Shannon diversity index H’ (natural logarithm) was cal-
autumn-winter and 11 in spring-summer. Conversely, culated considering an overall sample obtained by
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R.SITRANETAL. TINTINNIDSINTHENORTHERNIONIANSEA
Table I: Tintinnid species observed at Table I: Continued
Acicastello during the study period
Maximum Salpingacantha
Frequency abundance Salpingacanthasp. 2 0.5
Tintinnida (NNtot543) (cellsL21) Salpingella
Salpingellacurtac 6 2.1
Tintinnidaindet. 4 1.0 Salpingellaacuminata 3 1.6
Acanthostomella Salpingellaglockento¨geric 10 2.1
Acanthostomellalata 2 0.8 Salpingelladecurtata 6 1.1
Acanthostomellaconicoidesc 3 5.8 Salpingellasp. 5 0.5
Acanthostomellanorvegica 1 0.5 Stenosemella
Amphorella Stenosemellaventricosa 2 0.3
Amphorellaquadrilineataminor 1 1.6 Stenosemellanivalisc 13 6.6 Do
Amphorellasp. 4 1.1 Steenstrupiella w
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Steenstrupiellagracilisc 5 2.1 lo
Cyttarocylis Steenstrupiellasteenstrupiic 8 15.7 ad
Cyttarocyliscassis 1 0.5 e
Steenstrupiellasp. 5 1.1 d
CCoytdtoanroacryialiseucecryphalus 1 0.5 Tintinnopsis from
Codonariacistelluta 1 1.1 Tintinnopsisberoidea 2 1.1 h
Codonella Tintinnopsiscampanula 1 0.5 ttp
CCooddoonneellllaaagmalepahorella 14 01..51 TTiinnttiinnnnooppssiisscboamlticparessa 31 20..13 s://a
c
Codonellasp. 6 0.5 Tintinnopsisradix 1 0.3 ad
Codonellopsis Tintinnopsislindeni 2 0.5 em
Codonellopsisschabi 5 1.1 Tintinnopsisplagiostomac 3 4.7 ic
Codonellopsismonacensis 1 1.6 Tintinnopsisrotundata 2 0.5 .o
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Codonellopsispusilla 1 0.3 Tintinnopsiscylindrica 2 0.5 p
Craterella Tintinnopsissp. 2 1.1 .co
Craterellaarmillac 3 8.9 m
Craterellaoxyura 1 0.5 Undella /pla
Craterellatorulatac 15 10.0 Undellaclaparedei 6 1.1 n
Craterellaurceolata 1 0.5 Undellacleveic 11 3.7 kt/a
Craterellasp. 4 0.8 UUnnddeellllaapsuebrpcuasuidllaataacuta 11 00..33 rticle
Dadayiella Undellaostenfeldi 1 0.5 -a
Dadayiellacuspisc 5 2.1 Undellaangustior 1 0.5 bs
Dadayiellaganymedesc 34 44.7 Undellasubcaudatasubcaudatac 10 1.6 tra
DDaicdtyaoyiceyllsatapachytoecus 1 1.1 UUnnddeellllaopsspis. 3 0.7 ct/29
DDiiccttyyooccyyssttaaemleitgraansc 84 21..16 UUnnddeellllooppssiissmspa.rsupialis 11 01..51 /6/49
Dictyocystasp.c 9 2.6 5/1
Xystonella 4
Epiplocylis Xystonellatreforti 1 0.5 94
Epiplocylisacuminata 2 1.1 Xystonellasp. 1 1.1 77
Epiplocylisblanda 1 0.5 Xystonellopsis 2 b
EEpuitpinloticnynluissundella 1 1.1 XXyyssttoonneellllooppssiissbcyramnadttiica 11 00..55 y gu
Eutintinnuselegans 1 0.5 Xystonellopsisparadoxa 3 1.6 es
Eutintinnusfraknoii 4 0.7 t o
Eutintinnusapertus 2 0.3 Maximum abundance (cell L21) and frequency (times) areindicated for n 0
Eutintinnuslususundae 3 1.1 eachspecies.Superscriptcindicatesthecommonspecies. 4
A
Eutintinnustubulosus 5 0.5 p
Eutintinnusmacilentus 1 0.5 ril 2
Eutintinnusstramentus 2 0.5 pooling the species present each month along the water 0
Eutintinnussp.c 7 1.1 19
column. It ranged between 1.3 and 2.7, with an
Parundella average of 2.1+0.5 (Fig. 7); maximum values were
Parundellalohmanni 1 0.5
reachedin the period from September to January (H’(cid:4)
Parundellaaculeata 2 1.6
Protorhabdonella 2.3–2.7) whereas in the remaining months they span in
Protorhabdonellacurtac 14 6.8 the range 1.3–2.0. Lowest values were found in spring
Protorhabdonellasimplex 2 0.5
2003 when the tintinnid community was dominated by
Protorhabdonellasp. 1 0.3
few relatively abundant species and in August due to
Rhabdonella
the extremely low number of species. Looking at the
Rhabdonellainflata 1 0.5
diversity at each depth, higher values of H’ were gener-
(continued) ally found at the DCM depth, then in the below-DCM
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Table II: Occurrence of the common (indicated by an asterisk) and most frequent (present in
at least 10% of samples) tintinnid species at Acicastello
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p
.c
o
m
/p
la
n
k
t/a
rtic
le
-a
b
SpeciesarerankedupontheirLOD(LoricaOralDiameter).Thelowerpanelshowsthetemporalchangesinthechlorophyllandthe s
Median LOD of the tintinnid community. Averages for the three sampling depths were considered. Error bars show Standard tra
c
deviations. t/2
9
/6
/4
layer and the lowest diversity was recorded at surface; Relationships between abiotic and 9
5
however, these differences were not statistically signifi- biotic parameters /14
9
cant (ANOVA). 4
For each sample Pearson’s and Spearman Rank corre- 7
7
2
lation coefficients were calculated to test the relationships b
y
between physical and chemical parameters and some g
u
quantitative aspects of the tintinnid assemblages (abun- es
dance, species richness, Shannon diversity index) t o
n
(TableIII).Thoughabundancesdidnotshowanysignifi- 04
cant linear correlation with the physico-chemical par- Ap
ameters, species richness and diversity were weakly ril 2
0
correlated with nutrient concentrations, positively with 1
9
nitrates and phosphates (Pearson 0.32–0.34, P,0.05)
and negatively with ammonia; only this last appeared a
morerobustlink(Spearman 20.34to 20.38,P,0.05).
Furthermore tintinnid diversity appeared to be posi-
tively linked to salinity (Spearman 0.47, P,0.01),
which in turn was negatively correlated to chlorophyll
(Spearman 20.63, P,0.01).
Correlations (Pearson and Spearman) between com-
munity average and median LODs and chlorophyll
Fig. 7. Shannon diversity index H’ (natural log) of the monthly
tintinnidassemblages. were tested and were not significant. Though the
502
j
R.SITRANETAL. TINTINNIDSINTHENORTHERNIONIANSEA
Table III: Correlation coefficients among abiotic and biotic parameters
T S NH NO PO Chlaa Abundance Richness ShannonH’
4 3 4
T — 0.53* 0.10 20.11 0.25 20.18 0.12 0.24 0.23
S 0.51** — 20.20 0.21 0.13 20.63* 0.02 0.28 0.47*
NH4 0.30 20.13 — 20.32 20.04 0.30 20.22 20.34** 20.38**
NO3 20.11 0.24 20.26 — 20.12 20.25 0.18 0.29 0.35
PO4 0.13 0.14 20.17 0.03 — 20.17 0.21 0.24 0.25
Chla 20.19 20.50* 0.33** 20.29 20.17 — 20.07 20.22 20.30
Abundance 20.05 20.13 20.22 0.01 0.04 20.09 — 0.85* 0.53*
Richness 20.02 0.21 20.34** 0.32** 0.33** 20.23 0.61* — 0.85*
ShannonH’ 0.06 0.37** 20.44* 0.33** 0.34** 20.24 0.24 0.84* —
D
The upper triangular half of the matrix shows Spearman Rank Correlations, the lower half shows Pearson’s correlation. Abundance, richness and o
w
ShannonH’refertotintinnids. n
*P,0.01;**P,0.05;n¼36. lo
a
d
e
d
chlorophyll was significantly higher at the DCM-layer mixing processes. In this period, Salpingella glockento¨geri fro
m
than in the deep layer (Kruskal–Wallis, P,0.05) none was frequently recorded as well as relatively high h
of the community measures exhibited the same ten- numbers of C. torulata. These two species identified this ttps
dency. Conversely, the community median LOD in the group, which also included several species of very ://a
c
a
Period III (summer months)—34mm—was significantly similar abundance and frequency of occurrence d
e
higher than the Period I (autumn-winter months)— (Dictyocysta elegans, Salpingella decurtata, Undella clevei, m
ic
29mm (Fisher LSD,P,0.05). Dadayiella cuspis, Undella subcaudata subcaudata, Salpingella .o
u
curta and Codonellopsis.schabi). p.c
o
Cluster II includes most of the spring samples, where m
Cluster analysis the constant presence of P. curta and the alternating /plan
blooms of S. steenstrupii, Stenosemella nivalis and A. coni- k
Tniodtaesstsefmorbldaigffeesrewnictehsriensptehcetctoomtipmoesitaioncluosftetrheantianltyisnis- csoaimdepslessta,ncdharoauctt.erCizleudstebry IthIIe idnocmluidneasncaellotfhtehesucmonmtreorl t/article
(Bray-Curtis similarity index) was performed by consid- of lateral transport processes. The genus Eutintinnus and -ab
s
ering the overall abundance of each species along the particularly the species E. tubulosus together with the tra
column. The three main clusters closely reflect the species Codonella galea identify this group. ct/2
hydrological features of the site (Fig. 8). Cluster I groups 9/6
the autumn-winter months, characterized by a homo- /4
9
5
geneous water column and the dominance of vertical /1
4
9
DISCUSSION 4
7
7
2
Large fluctuations in abundance, species richness and b
y
diversity of the tintinnid fauna occurred during the g
u
period of investigation. Two main changes in species es
composition as well as in abundance were recorded, t o
n
one in spring and the other in late autumn. This obser- 04
A
vation has been reported also for other Mediterranean p
sites (Kimor and Golandsky-Baras, 1981; Abboud-Abi ril 2
0
Saab, 1989; Gomez and Gorsky, 2003; Urrutxurtu, 1
9
2004). The maximum abundance found in May 2003
was characterized by low diversity (H’¼1.3–1.4)
despite a high species richness (23 species pooled along
the column). In spring, all samples were characterized
by Protorhabdonella curta accompanied by the occasional
presence of relatively high numbers of a few other
Fig. 8. Bray-Curtis cluster analysis of tintinnid species occurrence.
Data were pooled along the column, standardized and species such as D. ganymedes and S. steenstrupii. These tin-
log-transformed. Period I: autumn-winter, well-mixed water column, tinnid species have very similar sized LODs ranging
dominance of pelagic waters; Period II: spring, blooms; Period III:
from about 27 to 35mm. Our data confirmed previous
summer, stratification of the water column and dominance of
longshoreadvectionfromtheStraitsofMessina. results of Dolan et al. (2002)that tintinnid diversity was
503
JOURNALOFPLANKTONRESEARCH j VOLUME29 j NUMBER6 j PAGES495–508 j 2007
negatively correlated to chlorophyll a in the water belonging to 25 genera were reported and tintinnid
column. In contrast, the same authors found a strong abundances ranged from 47 to 234 ind L21 at 20m
relationship between tintinnid morphological diversity depth and from 52 to 145 ind L21 at 50m depth
and phytoplankton cell size (ESD). Dolan et al. (2002) (Sparla and Guglielmo, 1994). However, our results
suggested that the co-occurrence of tintinnid species confirm Stenosemella nivalis as the most abundant species
with similar lorica diameters could be explained by in the surface layer along the coast of the Ionian Sea in
different preferences among algae of similar size. Thus, the Straits of Messina (Sparla and Guglielmo, 1994).
considering that the size of the prey most efficiently fil- On the other hand, similarly to our findings, low abun-
tered to be about 25% of oral diameter (Dolan et al, dance and tintinnid diversity were reported in summer
2002), the tintinnid species recorded in spring would also for theGulf of Elat (Kimorand Golandsky,1977).
prey most efficiently on food within the range of 6.7– Tintinnid assemblages found in this coastal Ionian D
o
8.7mm diameter. In March, a diatom bloom was siteover15monthsofstudysuggestamodelofcommu- w
n
recorded dominated by Chaetoceros and Pseudo-nitzschia nity where resources are rather evenly distributed. A loa
d
species and high abundance of phytoflagellates clear dominance by a single genus was never observed e
d
(Minutoli et al., 2005). In the same month, both tintin- and only two genera represented more than 10% of the fro
m
nid abundance and species richnesswere very lowwhile overall community (Dadayiella and Craterella). Though the h
diversity was high (H’¼2.2). cumulative richness rose to a plateau well before the ttp
s
Tintinnids are an important link in marine plankton end of the period, the 79 found species cannot be ://a
c
food webs (Verity, 1985;Alder, 1995)and have been fre- assumed as a good proxy of the true richness of the a
d
quently mentioned as important grazers on nanoflagel- study area. An underestimate of about 30% between em
lates (Dolan and Coats, 1990; Paranjape, 1990; Sherr the observed (79) and the potential (109) richness ic.o
u
and Sherr, 1994). However, tintinnids have been pointed out by the jack-knife analysis could be assigned p
.c
reported to show a wide food plasticity (detritus, pico- to the sampled volume (10L) and the observation of o
m
plankton, bacterioplancton, microplanktonic diatoms, only 100mL, which does not allow for the collection of /p
la
dinoflagellates) in different ecosystems and/or under very rare species (Modigh and Castaldo, 2002). An n
k
food stress conditions (Hargraves, 1981;Capriulo, 1982; underestimate could also be due to the monthly t/a
Stoecker and Guillard, 1982; Stoecker et al., 1984; sampling frequency, which is presumably too coarse to rtic
le
Capriulo et al., 1986;Kopylov and Turmantseva, 1987; describe the quick dynamics of such assemblages. The -a
b
Bernard and Rassoulzadegan, 1993) and this feature comparison of each monthlyassemblage shows in fact a stra
might explain the lack of a clear link between chloro- very high species turnover, i.e. the number of species c
t/2
phyll concentrations and tintinnid abundance, diversity that changes between two subsequent samplings was 9
/6
and species richness. In any case, a general inability of high as compared to the total number of species. In /4
9
tintinnids to feed on colonial diatoms and to consume particular during autumn-winter, the species compo- 5/1
large prey has been demonstrated (Hansen, 1991). It is sition of the community changed almost completely 49
4
thus possible that tintinnids fed primarily on the nano- every month. 7
7
2
flagellates that were very abundant in all seasons and The correlations found between tintinnid species rich- b
y
alongthewatercolumn (Minutoli et al.,2005). ness and diversity and nitrates, phosphates and salinity g
u
The second period (September 2003–January 2004) suggest that the temporal succession of species was es
was characterized both by higher abundances and stronglyinfluenced by the input of differentwater masses t o
n
higher species diversity (H’¼2.3–2.4) than those during the period of investigation. In the intermediate 04
A
observed in spring. Many tintinnid species of similar layer, which hosts the DCM for most of the year, a rela- p
abundance were recorded having a very wide range of tively low phytoplanktonic biomass (up to 0.4mgChl-a ril 2
LOD (12–65mm). However, the two species, Salpingella L21 on average) is associated with high nutrient concen- 01
9
glockento¨geri and C. torulata, that characterized the tintin- trations whose origin depends on the influence of deep
nid community in this season had a very similar LOD waters. From May to August, the biological processes of
(23–24mm). Again, this could be related to nanoflagel- uptake and regeneration balance the nitrogen com-
lates being very abundant at all depths (Minutoli et al., pounds and sequester the inorganic phosphorous.
2005). Conversely from September to Januaryoxidized nitrogen
In this study, both tintinnid abundance and species forms reach very high concentrations (.5mM) due to
diversity were extremely low during the summer inputs from below the nutricline and the lack of uptake
months, which is in sharp contrast to previous findings by biological components. This high-nutrient low-
in the Straits of Messina. In June–July 1990, in the chlorophyll (HNLC) condition is well known in the open
Ionian basin of the Straits of Messina 62 species sea where it depends on several factors such as the lack
504