Download Zooplankton assemblages and influence of

Journal of Plankton Research Vol.20 no.5 pp.847-870, 1998
Zooplankton assemblages and influence of environmental
parameters on them in a Mediterranean coastal area
Ioanna Siokou-Frangou, Evangelos Papathanassiou, Alain Lepretre1 and Serge
Frontier1
National Centre for Marine Research, Ag.Kosmas, 16604 Athens, Greece and
1
Laboratoire d'Ecologie Numerique (URA CNRS1363), Universite de Lille,
59655 Villeneuve d'Ascq, France
Abstract. Temporal dynamics of zooplankton communities and assemblages, as well as the influence
of environmental factors on them, were studied in Saronikos Gulf (Aegean Sea, Greece). Different
multivariate techniques (hierarchical clustering, multidimensional scaling and correspondence
analysis) were applied on a 2 year data set of zooplankton species composition, based on samples
collected at five stations of the study area. A clear discrimination of two communities was revealed,
the first one in the semi-enclosed polluted northern part (Elefsis Bay) and the second in Saronikos
Gulf proper. Within the latter community, five assemblages were distinguished: (i) the coastal winter
assemblage characterized by Ctenocalanus vanus, Oithona similis, Clausocalanus pergens and Fritillaria pellucida; (ii) the psychrophilic assemblage influenced by the open sea and characterized by
Oithona plumifera and Clausocalanus jobei; (iii) the spring assemblage characterized by Evadne
nordmanni and Cenlropages typicus; (iv) the coastal thermophilic assemblage characterized by Penilia
avirostis, Evadne tergestina and Temora stylifera; (v) the thermophilic assemblage influenced by the
open sea and characterized by Clausocalanus furcatus. Both zooplankton and environmental data
were treated by multiple correspondence analysis which revealed the importance of some environmental factors on zooplankton community composition (eutrophication-pollution, temperature,
water mass circulation, hydrology and topography).
Introduction
Several studies have dealt with differentiation of zooplankton communities
related to environmental variability using multivariate techniques (Collins and
Williams, 1982; Viitasalo, 1992; Laprise and Dodson, 1994; Suarez-Morales and
Gasca, 1996). Among environmental factors affecting the spatial and temporal
structure of zooplankton communities, physical ones play a major role in coastal
areas (Amanieu etai, 1989). In the Mediterranean Sea, the phytoplankton assemblages show a coherent distribution, in time or space, that can be related to
environmental conditions (Estrada, 1982). Regarding zooplankton, analogous
studies have led into defining distinct faunal groups in the temporal scale or in
the spatial scale in coastal areas (Cataletto et al., 1995; Ragosta et al., 1995), as
well as in the open sea (Dallot et al., 1988; Kouwenberg, 1994; Siokou-Frangou et
al., 1997). Nevertheless, an overall (temporal and spatial) approach to this aspect
could provide important information on coastal ecosystem functioning.
Saronikos Gulf (Figure 1) was chosen as a case study area because it offers a
variety of habitats due to its morphology and hydrology. According to the
description given by Siokou-Frangou et al. (1995), four subareas are distinct
within the gulf: (i) Elefsis Bay, a semi-enclosed shallow area highly submitted to
anthropogenic influence; (ii) the inner gulf with clear neritic character; (iii) the
outer gulf, in large communication with the Aegean Sea; (iv) the western basin
© Oxford University Press
847
LSiokou-Frangou et al.
SARONIKOS
GULF
30-
1 yz<'
23°
Epidavros -"ru^>:
basin
10'
20'
40'
50'
24'
Fig. 1. Positioning of sampling stations.
characterized by the presence of the deep Epidavros trench. These areas are
occupied by different water masses (Hopkins and Coachman, 1975). The outer
gulf is in large communication with the Aegean Sea, which provides source water
to Saronikos Gulf (Hopkins and Coachman, 1975). During winter, the vertical
mixing of the water column and the small differences in water density in the horizontal scale facilitate the movement of the Gulf water masses as a result of the
influence of the wind or the general circulation of the Aegean Sea (Christianidis,
1991). According to Laskaratos and Kaltsounidis (1989), water circulation is wind
driven and its main patterns are presented in Figure 2. During winter and
summer, with dominant south winds, and in the May-September period, with
north winds, an anticyclonic pattern is observed in the inner gulf and a cyclonic
pattern in the western basin (Figure 2a), whereas between November and February, when strong north-northeast winds dominate, the inner gulf and the western
basin are characterized by a cyclonic water circulation pattern (Figure 2b).
During March, April and October, wind strength is moderate and one or other
of the above patterns prevails, depending on wind direction.
Previous studies in the area refer to biomass annual cycle and distribution
(Yannopoulos, 1976a,b), to cladoceran and copepod species composition and
distribution in the upper 0-2 m layer (Moraitou-Apostolopoulou, 1974; Kiortsis
and Moraitou-Apostolopoulou, 1975), as well as to individual copepod species
biology (Christou and Verriopoulos, 1993a,b). The study of the annual cycle of
zooplankton abundance, species composition and diversity in the 0-20 or 0-50 m
848
Zooplankton assemblages and environmental parameters
(a)
30-
23°
10*
20'
30'
«0'
50'
2<°
(b)
30-
Fig. 2. Water circulation in Saronikos Gulf (according to Laskaratos and Kaltsounidis, 1989).
(a) May-September, N winds; winter-summer, S winds, (b) November-February, N winds.
layer of the above-mentioned areas has revealed differentiations related to the
features of each area (Siokou-Frangou et al, 1995; Siokou-Frangou, 1996). The
present study goes a step further by examining whether the zooplankton composition of each area corresponds to distinct communities and/or assemblages in the
Gulf, their structure and temporal dynamics, as well as the influence of environmental factors on them. Furthermore, several multivariate approaches were used
to provide complementary information for evaluating the stability of the results
found (Ignatiades etai, 1992).
Method
Samples were collected at five stations positioned in four distinct areas of
Saronikos Gulf (Figure 1): Elefsis Bay (SI), western basin (S2 and S3), inner gulf
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LSiokou-FTangou el al.
(S4) and outer gulf (S5). Sampling was performed in the 0-20 m layer at station
SI (maximum depth 28 m), in the 0-15 m at station S2 (maximum depth 17 m),
and in the upper 50 m layer at stations S3 (maximum depth 400 m), S4 (80 m) and
S5 (125 m). The 0-50 m layer represents the upper euphotic layer in most seasons
and, on the other hand, the lower part of the thermocline in Saronikos Gulf is
positioned at 50 m (Christianidis, 1991). The gulf was surveyed approximately
every month from January 1984 to December 1985. Sampling was not performed
in February 1984 at all stations, in May 1984, October 1984 and May 1985 at
station S2, in May and October 1984 and in May, June and November 1985 at
station S3, in May, June and July 1984 and August 1985 at station S5. Samples
were collected by double-oblique hauls of a WP-2 net (200 um), and between
10:00 and 16:00 h, in order to eliminate differences attributed to nycthemeral
migrations. Species identification concerned copepods, cladocerans and appendicularians; specimen counts were made in aliquots varying from 1/10 to 1/2 of
each sample. Temperature, salinity, nutrients and chlorophyll a concentrations
were measured synchronously with the zooplankton sampling (Barbetseas, 1986;
Friligos, 1986; Gotsis, 1986).
Two classification and two ordination methods were applied on the samples X
species (and groups) data matrix, in order to verify affinities among sites. Correspondence analysis (CA; Benzecri, 1979) and an ascending hierarchical clustering
based on the x2 distance were used (Benzecri, 1984). A hierarchical clustering and
a non-metric multidimensional scaling (MDS) based on the Bray-Curtis similarity matrix were also employed (Field et al, 1982). For the two latter methods,
the average linkage technique was performed and the data were transformed by
sqr(x). To find out possible relationships between zooplankton and environmental parameters, multiple correspondence analysis (Benzecri, 1979) was
applied to species (and groups) abundances and temperature, salinity, nutrients
and chlorophyll a depth-integrated values of the sampled water column. For each
variable (species abundance or environmental parameter), raw data were classified into three classes representing high, median and low values. The most important species (as revealed by the CA performed previously) were analysed by
multiple correspondence analysis.
Results
Similarities among stations: communities and assemblages
Fluctuations of dominant species and groups were presented by Siokou-Frangou
et al (1995) and Siokou-Frangou (1996). Temporal fluctuations of temperature,
salinity, phosphates, nitrates, silicates and chlorophyll a depth-integrated values
of the sampled water column are presented in Figures 3 and 4, based on data given
by Barbetseas (1986), Friligos (1986) and Gotsis (1986).
The multivariate analyses were performed on data of each single year (due to
the difficulties in manipulating large data matrices), except for the CA and the x2
distance-based hierarchical clustering on the data set of the Saronikos Gulf
proper (Elefsis Bay excluded).
850
Zooplankton assemblages and environmental parameters
Temperature
10'—'—'—'—'—'—'—'—'—'—'—'—'
J F M A M J J A S O N D J F M A M J J A S O N D
1984
Salinity
39.5
39 -
38.5,:
38 -
37.5 -
37'
•
'
'
'
'
i
i
i
i
i
i
•
i
i
J F M A M J J A S O N D J F M A M J J A S O N D
1984
1985
S1
->-Sa
-»-S3
-e-34
- * S5
Fig. 3. Temporal fluctuations of temperature and salinity depth-integrated values in the sampled
water column (data from Barbetseas, 1986).
851
00
Nitrates
81
-»- 82
-*
S4
•><S6
M A M J J A 8 O N D J F M A M J J A 8 O N D
A M J J A 8 O H 0
Fig. 4. Temporalfluctuationsof nitrates, phosphates, silicates and chlorophyll a depth-integrated values in the sampled water column [data from Friligos (1986)
and Gotsis (1986)].
1985
i.J
1984
J F M A M J J A 8 O N D J F M A U J J A 8 O N D
Chlorophyll-a
J.J'J*
Phosphates
A M J J A S O N O
mgCM-«/m3
Silicates
198b
mg.lPO4/m3
mgttSIO4/n3
1984
J F M A M J J A a O N O J F M A M J J A S O N D
mgtlNOS/mS
a
.a.
e
I
Zooplankton assemblages and environmental parameters
All stations data. The dendrogram derived from cluster analysis of the 1984 data
(Figure 5) can be partitioned into two major groups at low similarity level (20%):
the Elefsis Bay samples constitute the first group, whereas all the samples
collected in the Saronikos Gulf proper constitute the second one. At a higher
similarity level (50%), five groups could be distinguished. Group I includes
samples collected in Elefsis Bay (SI) from January until May. Samples from the
same area collected between July and December form group II. Group HI
concerns samples from stations S2, S3, S4 and S5 between January and May;
samples collected at station S2 in June, July and September, at S4 from June to
October, and at S5 in September were joined in group IV. Group V includes
samples collected from June until September at S3, in October at S5 and in
November-December at all stations of the Saronikos Gulf proper (S2, S3, S4, S5).
MAIN SARONIKOS
GULF
ELEFSIS
SAY
Fig. 5. Dendrogram issued from the hierarchical clustering of data collected in 1984 using the
Bray-Curtis similarity index. The letter of each abbreviation denotes the sampling month: J = January,
F = February, etc. The number denotes station: 1 = SI, 2 = S2, etc.; e.g. Jl = January station SI.
853
LSiokou-Frangou el al.
MAIN SARONIKOS
ELEFSIS BAY
Fig. 6. MDS plot in two dimensions issued from the analysis of data collected in 1984. Delimitation
of groups is based on the hierarchical clustering grouping at the 20% level (dotted line) and at the
50% level (solid line). Symbols are as indicated in Figure 5.
The same general picture, revealing the discrimination of Elefsis Bay (SI) from
the Saronikos Gulf proper and the seasonal variability of zooplankton, is apparent in the MDS plot based on the same data matrix (Figure 6).
Correspondence analysis (CA) revealed a polarized picture in the plane of the
first two axes (Figure 7): samples collected between January and May in Elefsis
Bay (station SI), characterized by the copepod Acartia clausi, are clearly
discriminated from those of the Saronikos Gulf proper along the first axis. Samples
collected in Elefsis Bay in the June-December period are also discriminated, but
they are positioned close to those collected at station S4 from June until August.
These samples are characterized by the presence of the cladocerans Penilia
avirostris and Evadne tergestina. The seasonal fluctuation in the zooplankton in the
Saronikos Gulf proper is clear along the second axis, which is correlated to temperature (r = 0.766, P < 0.001); along this axis, the warm months (June-September)
and the species P.avirostris and Temora stylifera have positive scores, whereas the
cold months (January-April) and the species Clausocalanus pergens, Centropages
typicus, Ctenocalanus vanus and Evadne nordmanni have negative scores.
The same analyses were also performed on the 1985 data and revealed a clear
distinction of Elefsis Bay samples from those of the Saronikos Gulf proper. Since
all analyses revealed mainly the differentiation of the Elefsis Bay samples from
those of the Saronikos Gulf proper, we could assume that two different communities occupied the two areas.
This strong difference masked any differences among the stations of the
Saronikos Gulf proper (in the MDS and CA plots); therefore, it was considered
worthwhile to perform the same analyses only on the data sets of the gulf proper.
Saronikos Gulf (Elefsis Bay excluded). The positioning of the 1984 samples in
the MDS plot along a 'horseshoe' is similar to that of Figure 6, but dissimilarities
854
Zooplankton assemblages and environmental parameters
(a)
01
51 N1
01
JTI1
jia
Au1
JU
Au2S«S5
Au5
•S2-S3 N3
O5 N5 N 2
02
0A
05
03
axis 1-
Jl3
A3
AS
J5
J3
M<
J1 Mo1
M1 A1
A4
M3
M5
M2
(b)
p<m
axis 2.
ala
pop
elf
act
ctv
dp
axis 2.
Fig. 7. Correspondence analysis ( 1 x 2 plane) of data collected in 1984. (a) Ordination of samples.
Symbols are as indicated in Figure 5. (b) Ordination of species, acl = Acartia clausi, ala = Acartia lalisetosa, cet = Centropages typicus, clf= Clausocalanus furcalus, dp = Clausocalanus pergens, ctv = Ctenocalanus vanus, evn = Evadne nordmanni, evt = Evadne lergestina, pea = Penilia avirostris, pop = Podon
polyphemoides, ppa = Paracalanus parvus, tes = Temora stylifera.
among stations are more clear. The 'horseshoe' positioning is also revealed in the
MDS plot of the 1985 data (graph not shown here). In plots of 1984 data (Figure
6) and 1985 data, samples collected at station S4 in March-April and in
June-August, and at station S2 in some months of these periods, occupy the edges
of the 'horseshoe' and are distinguished from samples collected in the same
periods at stations S3 and S5. A similar positioning of stations is obtained in the
855
LSiokou-FVangou el at.
1 x 2 plane of the CA of the 1984 data set and in the 1 x 3 plane of the 1985 data
set. The first axis is correlated to temperature (r = 0.94, P < 0.001 for 1984 data;
r = 0.9, P < 0.001 for 1985). The second or the third axis (according to the year)
distinguished samples collected in March, April, June, July and August mainly at
station S4, but also at station S2, from samples collected at all stations in
November-December. Taking into account that stations S2 and S4 have a clear
neritic character, whereas stations S3 and S5 are more influenced by the Aegean
Sea, and this influence affects all stations in November-December (Christianidis,
1991), one could assume that this axis is related to the influence of the open-sea
waters, namely the Aegean Sea waters.
CA was performed on the 2 year data set of the Saronikos Gulf proper in order
to obtain a general picture on the spatial heterogeneity of the area. In the plane
of the first two axes (Figure 8), there is a clear discrimination within the samples
collected between January and April, while samples of the June-December
period are projected very close. In this analysis also the first axis is related to sea
temperature (r = 0.893, P < 0.001). As for the second axis, samples collected in
(a)
M5
N2
M2
M3
F2
I*
J2
F3 J3
.
jS
J2
axis 1.
m5
F5
m3
aS
A3
o3
a2
t
A2
I
m2
axu 2.
856
Zooplankton assemblages and environmental parameters
(b)
frp
clp
pta
OXIS 1.
elf
dot
CtY
axis 2.
Fig. 8. Correspondence analysis ( 1 x 2 plane) of data collected in the main Saronikos Gulf in 1984
and 1985. (a) Ordination of samples. Small letters are for samples collected in 1984, e.g. j2 = January
1984 at station S2. Capital letters are for samples collected in 1985, e.g. J2 = January 1985 at station
S2. (b) Ordination of species and groups, eel = Cenlropages typicus, clf = Ctausocalanus furcatus, clp
= Clausocalanus pergens, ctv = Clenocalanus vanus, dol = doliolids, evn = Evadne nordmanni, evs =
Evadne spinifera, evt = Evadne lergestina, frp = Fritillaria pellucida, ois = Oilhona similis, pea = Penilia
aviroslris, tes = Temora stylifera.
March 1985 at S4 and S5 characterized by Fritillaria pellucida are opposed to
samples collected in March 1984 at S2 (characterized by E.nordmanni) and in
April of both years at stations S2, S3 and S4 (characterized by Centropages
typicus). This discrimination could be related to the trophic habits of the characteristic species: appendicularians (F.pellucida) feed on small particles (Fenaux,
1967), whereas copepods (C.typicus) and cladocerans (E.nordmanni) could feed
on diatoms which dominated in March 1984 at S2 and in April in the whole
Saronikos Gulf (Gotsis, 1986). Furthermore, it is known that F.pellucida presents
a clear seasonality in the Mediterranean Sea with maximum abundance in February and March (Fenaux, 1967).
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I-Siokou-frangon et al.
The 'horseshoe' positioning of samples and species is obvious in the 1 x 3 plane
of the same analysis (for the data set of both years) (Figure 9). Along the third
axis, the following samples are opposed: (i) samples collected in June-August at
S4, in June at S2 (characterized by the cladocerans P.avirostris, E.tergestina, the
appendicularian Fritillaria formica, the copepod Centropages ponticus), and
samples collected in March and April at stations S2 and S4 (characterized by the
species E.nordmanni, F.pellucida and C.typicus); (ii) samples collected in November-December at all stations (characterized by the copepods Nannocalanus
minor, Clausocalanus furcatus, Calocalanus pavoninus, Oithona plumifera). As
for the analyses of each year, we could assume that this axis is related to the influence of the Aegean Sea waters.
Hierarchical clustering based on the x2 distance distinguished mainly five
groups of-samples with the relative assemblages (Table I):
1. The first group includes samples collected at all stations in January and March
1984, at station S3 in April 1984, at all stations in February 1985, and at S2 and
(a)
axis 3.
858
Zooplankton assemblages and environmental parameters
(b)
axis 3.
Fig. 9. Correspondence analysis ( 1 x 3 plane) of data collected in the main Saronikos Gulf in 1984
and 1985. (a) Ordination of samples. Symbols are as indicated in Figure 8. Delimitation of groups
based on hierarchical clustering (x2 distance), (b) Ordination of species and groups, acl = Acania
clausi, one = Acartia negligens, cap = Calocalanus pavo, cav = Calocalanus pavoninus, cep =
Centropages ponticus, cet = Centropages typicus, cha = chaetognatru, che = Calanus helgolandicus, elf
= Clausocalanus furcatus, clj = Clausocalanus jobei, dp = Clausocalanus pergens, ctv = Ctenocalanus
vanus, dol = doliolids, evn = Evadne nordmanni, evs = Evadne spinifera, evt = Evadne tergestina, frf
= Fritillaria formica, frp = Fritillaria pellucida, leu = euphausid larvae, Iga = gastropod larvae, mte =
Mesocalanus tenuicornis, nmi = Nannocalanus minor, oil = Oikopleura longicauda, oip = Oithona
plumifera, ois = Oithona similis, onm = Oncaea media, ost = ostracods, pea = Penilia avirostris, pop =
Podon polyphemoides, ppa = Paracalanus parvus, pte = pteropods, sal = salps, sip = siphonophores,
les = Temora stylifera.
S3 in March 1985. This group is characterized by the presence of the coastal
winter assemblage. A small group, close to the first one, includes samples collected in March 1985 at stations S4 and S5, characterized by Epellucida (Figure
9b). We could therefore consider this species as belonging to the coastal winter
assemblage.
2. Samples collected at station S2 in March and April of both years, at S4 in April
859
LSiokou-Frangou et al.
and May, and at S3 in April 1985, formed the second group characterized by
the presence of the spring assemblage.
3. The third group comprises samples collected in June-August of both years at
stations S2 and S4, in August at S3, in September-October at S4 and in September at S5. This group is characterized by the presence of the coastal
thermophilic assemblage.
4. The fourth group comprised samples collected mainly at stations S3 and S5
from July to October, at S2 in September-October, and at all stations in
November 1984. The thermophilic assemblage influenced by the open sea
characterizes these samples.
5. The fifth group includes samples collected at all stations in December 1984, in
November and December 1985, at stations S2, S4 and S5 in January 1985, and
at station S5 in April 1984 and 1985. This group is characterized by the presence of the psychrophilic assemblage influenced by the open sea.
It is worth mentioning the existence of similarities in assemblages from different stations at different times of the year assuming a transport of assemblages
between neighbouring stations. Namely, the coastal thermophilic assemblage was
found at S2 in July 1984 and at the neighbouring S3 the following month. The
same assemblage was observed at S4 in August and at S5 in September of both
years. On the other hand, the thermophilic assemblage influenced by the open
sea was found at S5 in October 1984 and at S4 the following month, in August
1985 at S3 and the next month at S2.
Environmental factors affecting zooplankton
Multiple correspondence analysis was performed on zooplankton and the
environmental data set of each year, firstly for all stations and secondly for the
Saronikos Gulf proper (Elefsis Bay excluded).
All stations data. In the 1 X 2 plane of the analysis performed on the 1984 data
set of all stations (Figure 10), samples collected in Elefsis Bay are positioned
Table L Zooplankton assemblages in the Saronikos Gulf proper as derived by hierarchical clustering
using x2 distance
Assemblage
Species and groups
Coastal winter
Ctenocalanus vanus, Clausocalanus pergens, Oithona similis, Oncaea
media, Acartia clausi, Calanus helgolandicus, Mesocalanus tenuicornis,
siphonophores, Fritillaria pellucida
Oithona plumifera, Clausocalanus jobei, Nannocalanus minor,
Calocalanus pavo, Calocalanus pavoninus, chaetognaths, ostracods,
gastropod and euphausid larvae
Cenlropages typicus, Evadne nordmanni, salps
Penilia avirostris, Evadne tergestina, Temora stylifera, Paracalanus
parvus, Centropages ponticus, Evadne spinifera, Podon polyphemoides,
Oikopleura longicauda, Fritillaria formica, doliolids
Clausocalanus furcatus, Acartia negligens, pteropods
Psychrophilic influenced
by the open sea
Spring
Coastal thermophilic
Thermophilic influenced
by the open sea
860
Zooplankton assemblages and environmental parameters
separately from those of the Saronikos proper. High abundances of A.clausi and
Podon polyphemoides, high values of phosphates, silicates and chlorophyll a, and
low abundances of other species are projected close to the Elefsis Bay samples.
These samples and species are opposed along the first axis to the samples of
station S3 collected in the period June-September, of station S2 in June and
September, to the high abundances of Clausocalanus furcatus and T.stylifera, and
low values of phosphates, chlorophyll a and nitrates. Phosphates and chlorophyll
a values vary parallel to thefirstaxis, which therefore accounts for the difference
between the eutrophic conditions in Elefsis Bay and the oligotrophic conditions
in the western Saronikos Gulf (stations S2 and S3) during summer. Temperature
values vary parallel to the second axis, along which are discriminated: (i) samples
collected in summer in Elefsis Bay and at stations S2 and S4, and high abundances
of the species Penilia avirostris, E.tergestina and Podon polyphemoides; (ii)
samples collected in January, March and April, and high abundances of the
species Ctenocalanus vanus, Centropages typicus, Clausocalanus pergens and
E.nordmanni. Therefore, temperature should be the main factor for the samples
and species discrimination along the second axis.
The 1985 data set analysis revealed similar results, discriminating the Elefsis
Bay community from that of the main Saronikos Gulf; but in this case the first
axis is related to temperature and the second one to chlorophyll a.
Saronikos Gulf (Elefsis Bay excluded). In the plane of the first two axes of the
analysis of the Saronikos Gulf proper in 1984 (Figure 11), sample positioning is
similar to that obtained in the CA, i.e. in a 'horseshoe' along which temperature
and chlorophyll a values vary; these parameters contribute to the formation of
the first axis. Abundances of the species Penilia avirostris vary parallel to temperature, and those of Clausocalanus pergens, Ctenocalanus vanus, E.nordmanni and
F.pellucida inverse to temperature, assuming the significant influence of temperature on these species. Temperature also accounts for the second axis, along
which are opposed: (i) summer samples of stations S2, S3 and S4, high abundances of Eformica, high temperature and low chlorophyll a values; (ii) samples
collected in November-December at S3, S4 and S5, high abundances of Nannocalanus minor and Clausocalanus jobei, median temperature and chlorophyll a
values. A similar positioning of samples, species and environmental parameters
was obtained in the 1 x 2 plane of the 1985 data set analysis.
Discussion
Communities and assemblages
According to the present study, two distinct communities were present in the
Saronikos Gulf: one in Elefsis Bay and the other in the Saronikos Gulf proper.
All three multivariate analyses confirmed these results for both yearly data sets.
The Elefsis Bay community was characterized by the high dominance of a low
number of species (A.clausi, Penilia avirostris, E.tergestina, Podon polyphemoides), which were followed in a rank order by some rare neritic species.
Previous study in the area has revealed pronounced fluctuations in the total
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LSiokou-Frangou et al.
zooplankton abundance, low diversity values and linear curved rank-frequency
diagrams, suggesting a disturbed community (Siokou-Frangou et al., 1995).
Similar zooplankton communities have also been observed in the Gulf of Fos
(Patriti, 1984), in the port of Mahon (Jansa, 1986) and in the Bay of Thessaloniki
(Siokou-Frangou and Papathanassiou, 1991).
Taking into account the composition of zooplankton in Mediterranean coastal
areas given by Scotto di Carlo and Ianora (1983), Gaudy (1985) and MoraitouApostolopoulou (1985), we could assume that the zooplankton community of the
Saronikos Gulf proper is similar to the neritic communities of the Mediterranean
Sea in the species composition and their seasonal evolution. Some differences,
such as the dominance of Ctenocalanus vanus in winter, could be attributed to the
positioning of the gulf within the Eastern Mediterranean. This species is not
abundant in the Western Mediterranean Sea, but was found to be dominant in
Kastela Bay of the Middle Adriatic (Regner, 1985).
The high dominance of F.pellucida only in March 1985 at stations S4 and S5
could be due to the capacity of appendiculanans to develop large populations
very quickly under favourable conditions (Gorsky et al., 1991). The abundance of
F.pellucida during February-March is reported in the Mediterranean Sea
(a)
O1
JL1
S1 N1
01
AIM
S3 S2
SA
AU1
JN1
M1
J1
AU2
AU5
JN<
JN2 JL3
OA S3
* * JN3
N2
N3
02
OS
A1 MA1
0 5
MA*
A2
J2
J3
A
M5
43
J5
M2
hi*
AS
A3
axis 2.
862
QXIS 1.
Zooplankton assemblages and environmental parameters
(b)
NA1
p*'
\
SA1
NA3
•M
/
PP\
X
c<3
/
OXIS 1.
a c 1 [p
/p*2 >A2
PH2V
Op2
XL2|
511
tr>3 fp3
cp3
cv3
axil
2.
Fig. 10. Multiple correspondence analysis ( 1 x 2 plane) of data collected in 1984 at all stations, (a)
Ordination of samples. Symbols are as indicated in Figure S. (b) Ordination of environmental
parameters and species classes. TE1 = low temperature values, TE2 = median temperature values,
TE3 = high temperature values. NA = nitrates, SA = salinity, SI = silicates, PH = phosphates, XL =
chlorophyll a. Lines depict high, median and low values of parameters contributing to the formation
of the first axis (dotted) and the second axis (dash), ad = Acartia clausi high abundance values, ac2
= A.clausi median abundance values, ac\ = A.clausi low abundance values, ce = Centropages typicus,
cf= Clausocalanus furcatus, cp = Clausocalanus pergens, cv = Ctenocalanus vanus, en = Evadne nordmanni, el = Evadne lergestina, fp = Fritillaria pellucida, op = Oithona plumifera, pa = Paracalanus
parvus, pe = Penilia avirostris, pp = Podon polyphemoides, is = Temora stylifera.
(Fenaux, 1967; Scotto di Carlo and Ianora, 1983) and extremely high abundances
have been found in the neighbouring Evoikos Gulf (Yannopoulos and Yannopoulos, 1978; Siokou-Frangou etal, 1984). In the January-March period, Paracalanus
parvus, A.clausi, Clausocalanus paululus and Clausocalanus furcatus were among
the most dominant copepods in the Gulf of Naples (Mazzocchi and Ribera
d'Alcala, 1995), whereas in the coastal Lebanese waters P.parvus, Acartia
discaudata, Acartia longiremis, Clausocalanus furcatus and Clausocalanus
arcuicornis were abundant (Lakkis, 1990).
863
I-Siokou-Frangou el al.
During a longer period (December-April), the psychrophilic assemblage
influenced by the open sea was observed mainly at the deep stations S3 and S5,
characterized by the species O.plumifera and Clausocalanus jobei. In the Gulf of
Naples, O.plumifera is among the abundant species for the period
September-January (Mazzocchi and Ribera d'Alcala, 1995). According to Scotto
di Carlo et al. (1985), this copepod presents a mixed neritic-pelagic character with
a wide horizontal distribution in coastal (Gulf of Naples) and open-sea areas
(Tyrrhenian Sea). Clausocalanus jobei was among the dominant species in February-March in the Aegean Sea (Siokou-Frangou et al, 1994) which provides
source water to the Saronikos Gulf. The influence of the Aegean Sea is also
obvious from the presence during this period of some rare epipelagic or
mesopelagic copepods (Paracandacia bispinosa, Clausocalanus lividus,
Eucalanus monachus, Haloptilus longicornis, Heterorhabdus papilliger, Euchaeta
marina, Lucicutia flavicornis, Pleuromamma gracilis). A similar presence of
epipelagic or mesopelagic species (most of them found as juvenile stages) was
also observed in the winter period in the Gulf of Naples (Scotto di Carlo et al.,
1985) and in the Lebanese coastal waters (Lakkis, 1990).
The spring assemblage was delimited temporally and spatially since it predominated at shallow stations (S2 and S4). Therefore, species constituting this assemblage have a clear coastal character, reinforced by their negative contribution to
(a)
JN2
AU2
J3
JN<
S3
52
J2
AU3
JL2
JL3 JN3
AU4
AUS
M3
M2
MS
JS
•M* •
O5
JL<
55
N2
NS
02
OS
O<
AS
A3
03
A2
N<
N3
axis 2.
864
OXH 1.
Zooplankton assemblages and environmental parameters
(b)
Fig. 11. Multiple correspondence analysis ( 1 x 2 plane) of data collected in 1984 in the Saronikos
Gulf proper, (a) Ordination of samples. Symbols are as indicated in Figure 5. (b) Ordination of
environmental parameters and species classes. Symbols are as indicated in Figure 10 and cj =
Clausocalanus jobei,ff- Fnrillaria formica, run = Nannocalanus minor. Lines depict high, median and
low values of parameters and species contributing to the formation of the first axis (dotted) and the
second axis (dash). Species in ellipsis contribute in the formation of the first and second axes.
the axis of the CA which accounted for the open-sea influence. In the Gulf of
Naples, Acartia clausi and Centropages typicus were found to be dominant
between April and August (Mazzocchi and Ribera d'Alcala, 1995), while the
dominance of A.clausi and E.nordmanni is mentioned in the Gulf of Malaga in
spring (Rodriguez, 1983).
During the warm period (June-September), the coastal thermophilic assemblage was observed mainly in the shallow stations and occasionally in the deeper
ones. Its characteristic species (Penilia avirostris, E.tergestina, T.stylifera) were
also found to be dominant in the Spanish coastal waters during summer (Estrada
et al, 1984), whereas in the Gulf of Naples they were abundant in
August-September (Scotto di Carlo et al, 1985). This assemblage was also
observed in Thermaikos Gulf (Siokou-Frangou and Papathanassiou, 1991).
During this period at the deeper stations, and in October-November at almost
865
LSiokoa-Frangou et at.
all stations, another thermophilic assemblage was observed which is influenced
by the Aegean Sea water masses. The dominant species {Clausocalanus furcatus)
presents a wide horizontal distribution since it has also been found to be abundant in the offshore waters of the Mediterranean Sea (Gaudy, 1985; SiokouFrangou et al., 1997) and namely in the Aegean Sea (Moraitou-Apostolopoulou,
1972; Siokou-Frangou et al, 1990).
Influence of environmental factors
Among the environmental parameters measured, nutrients and chlorophyll a,
both indicative of eutrophic conditions, seem to play a major role in separating
the Elefsis Bay zooplanktonic community from that of the Saronikos Gulf
proper. This distinction was very clear in all analyses and the role of these factors
in the characterization of the community was evidenced by the projection of
their high values close to the Elefsis Bay samples. In conditions of increasing
eutrophication, the number of species gradually decreases and generally the
faunistic assemblage is simplified. The low species richness under these
conditions and the abundance of few species in a particular biotope result from
their tolerance of the environmental variability and their capability for optimum
exploitation of food resources. This variable tolerance results from special
physiological adaptations of the organisms (Gaudy, 1984). In Elefsis Bay, apart
from eutrophic conditions, high values of hydrocarbons and heavy metals have
been measured when compared to the Saronikos Gulf proper (Scoullos and
Oldfield, 1986; Mylona and Mimikos, 1991). Therefore, the observed community
reflects a polluted environment.
Temperature seems to be the main factor relating to the seasonal evolution of
zooplankton and the distinction of the relative assemblages. This influence was
also clear from the observation of a thermophilic assemblage in November 1984
when the mean seawater temperature was ~21°C; on the contrary, a psychrophilic
assemblage was found in November 1985 when the mean temperature was -18°C.
The influence of the seawater temperature was expected since the seasonal
succession is mainly dependent on temperature (Sullivan and McManus, 1986;
Villate, 1994). It was also revealed in the study of the annual cycle in each station
of the Saronikos Gulf (Siokou-Frangou et al., 1995; Siokou-Frangou, 1996). In
this coastal area, temperature was found to be the main factor regulating
zooplankton productivity (Christou, 1991) and metabolism (Christou and
Moraitou-Apostolopoulou, 1995). Furthermore, the reproductive potential of
cladocerans depends on temperature (Fonda-Umani, 1980) and appendicularians
are highly sensitive to it (Acuna and Anadon, 1992). On the contrary, Mazzocchi
and Ribera d'Alcala (1995) argued that temperature could not be the sole trigger
of the biological response of zooplankters in the Gulf of Naples.
Salinity was not a limiting factor for zooplankton composition or abundance in
the area, a fact that may be due to the narrow range of values measured (37.5-39).
Water circulation and hydrology seem to be important factors for both
zooplankton composition and distribution. Although they were not measured
directly, their influence was revealed in the analyses. The coastal-open-sea factor
866
Zooplankton assemblages and environmental parameters
was among the main factors explaining the distinction of subcommunities in the
Gulf of Finland (Viitasalo, 1992). The open-sea influence has also been detected
in the Gulf of Naples (Scotto di Carlo et al., 1985), in the eastern Adriatic
(Regner, 1985) and in the Lebanese coastal waters (Lakkis, 1990). Water circulation permits the influence of the open sea towards shallow and more coastal
stations and, inversely, the spreading of coastal assemblages towards deeper
stations. This was shown by the time lag in the appearance of an assemblage at
neighbouring stations. The circulation pattern prevailing at each time allows
communication among stations and population transportation from one basin to
the other through the passages G-B, S-A and M-P (Figure 2a). Namely, in
August-September at passage G-B, the prevailing water flow is southwards and
therefore the coastal thermophilic assemblage could spread from station S4
towards station S5. The opposite waterflowprevails between October and February, resulting in the Aegean Sea water influence in the inner Saronikos Gulf and
the transportation of the relative assemblage (thermophilic influenced by the
open sea). On the other hand, the water column mixing, occurring between
November and February, facilitates the communication among the basins, as well
as between the Aegean Sea and the Saronikos Gulf (Christianidis, 1991). As a
result, similarities among stations are stronger during the cold period (November-February) and less in the March-September period. In March, or even in
April, a hydrological differentiation among stations is evident due to the development of the thermocline. During this period, in the shallower stations S2 and S4,
large populations of cladocerans and appendicularians prevail due to the
favourable environmental conditions (water temperature, phytoplankton populations). The development of these populations differentiates the most coastal
stations S2 and S4 from the deeper stations S3 and S5. Therefore, the presence
or not of each assemblage in each area also depends on water mass movements
and hydrology. Relationships between water movements and the distribution of
communities have been noticed in the Adriatic Sea (Hure et al., 1980), while
Braarud and Nygaard (1980) suggested that water movement parallel to the coast
could transport planktonic communities for a long distance. This transport could
modify the zooplankton composition in gulfs and semi-enclosed areas (Lindahl
and Henroth, 1983; Aksnes et al, 1989).
On the other hand, the topography of the sampling site also seems to be important. Shallow stations (SI, S2 and S4) present some particular aspects: early
seasonal appearance of species, abrupt fluctuations of the annual cycle (SiokouFrangou, 1996), weak and delimited influence of the open sea. Deeper stations and
those closer to the Aegean Sea (S3 and S5) are largely influenced by its water
masses, enriching them with many epipelagic and mesopelagic species. This was
also obvious in the CA where deep station samples had higher positive scores than
the shallow ones on the axis accounting for the open-sea factor. Similarly, shallow
and coastal stations are more influenced by the neighbouring coasts, especially
those positioned closer to the cities (anthropogenic influence). This influence
becomes more acute due to the confinement of the area: the semi-enclosed Elefsis
Bay has a slower water renewal when compared to the main Saronikos Gulf proper
(Christianidis, 1991) and therefore pollutants are trapped in the area.
867
I-Siokoa-Frangou et al.
Conclusively, two distinct zooplankton communities have been observed in
Saronikos Gulf and this distinction is due to the strong differentiation of environmental conditions between the polluted Elefsis Bay and the non-polluted
Saronikos Gulf proper. The community of the latter area is constituted by five
assemblages influenced mainly by the seasonal variability in temperature and the
coastal-open-sea factor. All multivariate techniques revealed very coherent
results, suggesting the robustness of the results regarding the similarity among
stations, the composition of the zooplankton community and the influence of
environmental factors affecting it.
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Received on June 5,1997; accepted on December
870
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