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Evaluation of estuarine mesozooplankton
dynamics at a fine temporal scale: the
role of seasonal, lunar and diel cycles
SÓNIA COTRIM MARQUES1*, ULISSES MIRANDA AZEITEIRO1,2, FILIPE MARTINHO1, IVAN VIEGAS1
AND MIGUEL ÂNGELO PARDAL1
1
INSTITUTE OF MARINE RESEARCH (IMAR), C/O DEPARTMENT OF ZOOLOGY, UNIVERSITY OF COIMBRA,
SCIENCE AND TECHNOLOGY, UNIVERSIDADE ABERTA,
3004-517 COIMBRA, PORTUGAL AND 2DEPARTMENT OF
4200-055 PORTO, PORTUGAL
*CORRESPONDING AUTHOR: [email protected]
Received April 21, 2009; accepted in principle May 28, 2009; accepted for publication July 11, 2009; published online 1 August, 2009
Corresponding editor: Mark J. Gibbons
In order to study the influence of physical forcing at different temporal scales, zooplankton was
sampled at a fixed station located at the mouth of Mondego estuary (southern Europe). Samples
were collected during diel cycles, over neap and spring tides. Zooplankton abundance and diversity
were estimated for each sampling period. Holoplankton were dominated by three taxa: Copepoda,
with 48% of total zooplankton abundance, Cladocera (16%) and Medusae (12%).
Meroplankton occurred mainly as barnacle and decapod larvae. Copepoda were the most diverse
group, represented by 26 species followed by Decapoda larvae (21) and Medusae (16). In order
to assess significant differences between seasons, a univariate analysis was carried out. Higher
abundance and diversity were found in warm months, particularly at neap tides, when water temperature and salinity were higher. Multivariate analysis revealed significant seasonal differences in
species composition. The estuarine community was strongly dependent on allochthonous events,
such as tidal exchange and river inflow. The results of our study show that the period of higher
river flow, coincident with winter, resulted in changes in the zooplankton community. Short-term
temporal variations in the species composition and abundance were also attributed to tidal and diel
cycles. Zooplankton reached significantly higher densities at night (P , 0.05), suggesting the
occurrence of vertical migrations. By emphasizing the importance of different timescale changes in
the zooplankton community of the Mondego estuary, this study will be useful for the design of
more efficient sampling programs, aiming at documenting changes in the zooplankton at a broad
but also at a fine temporal scale.
I N T RO D U C T I O N
One of the major goals in marine ecological research is
to understand the response of planktonic communities
to physical forcing. In addition, trophic relationships
and environmental parameters (such as temperature,
salinity, turbidity and pollution) are known to influence
the structure of zooplankton communities (Roman et al.,
2001; Uriarte and Villate, 2005). In estuarine and
coastal areas, the environmental conditions fluctuate at
different time and space scales, subjecting organisms
that inhabit the pelagic realm to tidal, diurnal and
seasonal environmental changes. Knowledge of the
variability of zooplankton communities at different
spatial and temporal scales is therefore a prerequisite to
understanding their dynamics.
Physical processes such as tidal currents and estuarine
circulation associated with coastline configurations and
bottom topography are well-known phenomena that
contribute to horizontal patchiness of zooplankton
(Alldredge and Hamner, 1980; Jessopp et al., 2007). The
study of these rather complex hydrodynamic processes,
however, is often complicated because of their multiple
doi:10.1093/plankt/fbp068, available online at www.plankt.oxfordjournals.org
# The Author 2009. Published by Oxford University Press. All rights reserved. For permissions, please email: [email protected]
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interactions. Moreover, biological mechanisms may also
account for a significant part of the temporal variation
in zooplankton community structure. Among the biological mechanisms involved in temporal changes in
zooplankton distribution, active vertical migrations are
the most consistent (Rawlinson et al., 2004). Diel vertical
migrations (DVMs) occur in a wide range of both freshwater and marine zooplankton taxa, probably representing the largest synchronized animal migration in
terms of biomass on the planet, and is of a paramount
importance for ecosystem functioning and carbon
cycling (Hays, 2003). The majority of DVM studies have
been focused on freshwater Cladocera and Copepoda
(e.g. Dauvin et al., 1998; Armengol and Miracle, 2000;
Haupt et al., 2009) since these organisms are good
swimmers and show vertical movements of higher
amplitude. Despite the fact that in recent years there
has been an apparent growing interest in this research
topic in marine ecosystems (Hays, 2003), few studies
have been made in southern European coastal systems
(e.g. Queiroga et al., 1997; Rawlinson et al., 2004; David
et al., 2005; Morgado et al., 2006). These studies focused
mainly on macrozooplankton populations or on specific
species.
The mesozooplankton abundance and specific composition are well documented in the Mondego estuary
(Azeiteiro et al., 1999; Marques et al., 2006; Primo et al.,
2009), but the results obtained in previous studies were
based on monthly sampling and did not address shortterm variations. However, to examine stresses on a community, the composition, the structure and dynamics
should be reasonably understood. Up to this date, only
one study addressed the dynamics of decapod crustacean larval under different lunar phases and during
nyctemeral cycles in this estuary (Gonçalves et al., 2003).
Thus, the present study focuses on short-term temporal
and spatial variations in the mesozooplankton community of the Mondego estuary. This estuarine system
covers a marine, brackish and freshwater system, providing useful data for comparison with other estuaries. The
specific aims were (i) to describe the taxonomic composition and seasonal patterns of zooplankton at different
lunar phases and (ii) to determine the short-term
changes in the community in relation to the diel light/
dark cycle and the semidiurnal tidal cycles.
METHOD
Study site
The Mondego River estuary, located on the west coast
of Portugal (408 080 N, 88 500 W), has an area of 8.6 km2
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and a volume of 0.0075 km3 (Fig. 1). The hydrological
basin of the Mondego, with an area of 6 670 km2, provides an average freshwater flow rate of 8.5 109 m3
s21. This system is located in a warm temperate region
with a basic Mediterranean temperate climate. At about
5.5 km from the sea, the river branches into two arms
(north and south), which converge again near the
mouth. Tides in this system are semi-diurnal, and at the
inlet the tidal range is 0.35– 3.3 m, with an average residence time of 2 days for the north arm and 9 days for
the south arm.
Sampling and laboratory analysis
The zooplankton community was sampled at one fixed
station at the mouth of the estuary (Fig. 1), during 1
year: June, September, October, December 2005 and
March, April 2006, over neap and spring tides. In this
area, the influence of both the river flow and neritic
waters is strong. The sampling station was characterized
by depths of 6 – 13 m. Zooplankton samples were collected by horizontal tows, using a bongo net of 335 mm
mesh sized equipped with a hydro-bios flowmeter to
calculate the filtered volume (average 20 m3).
Considering copepods, the mesh size used certainly
under-estimates the early life stages and smaller organisms. Yet, only adult copepods were taken into account
in this study and smaller organisms are discussed with
some caution. Hourly samples were collected from subsurface and 1 m above the bottom, over diel cycles. The
samples were classified as day, from sunrise to sunset,
and night, periods. Net samples were immediately preserved in a 4% borax-buffered formalin seawater solution for further analysis. A total of 388 samples were
examined and sub-sampled using a Folsom-splitter, and
a minimum of 500 individuals (all categories) were
counted. The zooplankton analysis was carried out
under a stereoscopic microscope and identification was
made to species level whenever possible. Abundance
estimates were standardized as the number of individuals per m3 for each depth level.
In parallel with the zooplankton tows, water temperature (T), salinity (S), dissolved oxygen (DO) and pH
were recorded in situ with appropriate sensors (WTW)
at both depths; turbidity was measured using a Secchi
disk. Also, at each sampling event, a 500 – 1000 mL
water sample was filtered for determination of chlorophyll a (Chl a) and suspended particulate matter (SPM).
All data concerning precipitation and freshwater runoff
were acquired from the Portuguese Water Institute
(INAG, www.inag.pt) stations Soure 13/01G and Açude
Ponte de Coimbra 12G/01A (nearby city of Coimbra,
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Fig. 1. Map of the Mondego estuary and location of sampling site.
since no meteorological station was present in the study
area), respectively.
Statistical analysis
The zooplankton community structure was described
for each sampling occasion, over the temporal and
spatial scales, by determining their abundance
(ind.m23) and two diversity indices: Shannon diversity
index (H0 ) and species richness (defined as the number
of species). The comparison of these indices will indicate whether diversity variations are due to a change in
the number of species, or a modification in the relative
contribution of taxa.
The general linear model (GLM) procedure was used
for two analyses of variance (ANOVAs). The first analysis
considered spatial and temporal variations in zooplankton abundance and diversity at a longer timescale
(season, tide and depth). The second analysis considered
variation at shorter timescales (diel, tidal cycle and
depth) within seasons. When the differences were significant, Bonferroni adjusted pairwise comparisons amongst
groups were computed. Prior to statistical analyses, normality and homogeneity of variance were checked for all
data (Kolmogorov –Smirnov test and Levene’s test,
respectively). When necessary, log (x þ 1) or square-root
transformation was performed. Univariate data analysis
was performed in SPSS v16.0 software (SPSS).
Additionally, multivariate statistical analyses were performed to examine the variation in community composition through non-metric multidimensional scaling
(MDS) plots. These analyses were based on triangular
matrices of the Bray –Curtis similarities, by performing
a fourth-root transformation of the species abundance
data in order to down-weight the influence of highly
abundant species, using only those taxa that represent
.0.1% of the zooplankton community. One-way analysis of similarity (ANOSIM) was subsequently used to
test whether the community structure differed significantly between groups. The contribution of each
species to the average Bray – Curtis similarity within
each group was analyzed using the similarity percentage
procedure (SIMPER), and these results were used to
help interpret the faunal change responsible for the
pattern observed in the MDS ordination.
Finally, the relationships between the hydrological
variables were analyzed separately, using the BIOENV
procedure developed by Clarke and Ainsworth (Clarke
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and Ainsworth, 1993), to define the environmental variables that better explain the assemblages’ structure. The
BIOENV procedure (using Spearman’s rank correlation
method) was used on log-transformed environmental
data. All these analyses were carried out by means of
the PRIMER-6 software (Clarke and Gorley, 2006).
R E S U LT S
Hydrological conditions
The hydrological conditions recorded during the study
period are shown in Fig. 2. A clear seasonal pattern of
precipitation and runoff was observed, with the highest
values in the winter. However, in the hydrological year
of 2005/2006, high values were also observed in March
and April.
As in most river-influenced estuaries, salinity was
greatly driven by the seasonality of the Mondego river
freshwater discharge (Fig. 2). Mean salinity values were
generally higher in spring and summer months at both
depths (surface: 29.3 + 2.65, bottom: 32.37 + 4.09)
(Fig. 3). At the surface, a sharp decrease in salinity was
observed in autumn and winter (mean 11.6 + 7.24),
showing the occurrence of the intrusion of low saline
water. At the bottom, this turnover was more pronounced in the winter (average of 23.3 + 8.4). The
mean salinity gradient between the high water and low
water ranged up to 4.0 at both depths, being more pronounced in autumn/winter. The water temperature was
only slightly different between surface and bottom
(1.1 + 0.98C on average), suggesting thermal homogenization of water column (Fig. 3). The seasonal cycle was
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marked, with high water temperature values recorded
in spring and summer (mean 17.7 + 0.688C) and lower
in autumn and winter (mean 13.1 + 0.68C). Secchi disc
visibility decreased with increasing river discharge,
inversely with the load of SPM, which generally
increased. Fluctuations of SPM values over the tidal
cycle were more pronounced at surface depths than on
the bottom. In the winter, exceptionally high values of
SPM were measured for both depths (average.140 +
5.1 mg L21, Fig. 3). Chlorophyll a values generally
increased in spring and autumn being higher at the
bottom, independent of the tidal cycle.
Zooplankton abundance and diversity:
temporal and spatial distribution
Pooling all samples, a total of 112 species of zooplankton belonging to 18 taxonomic groups were identified
in this survey (Table I). Generally, holoplanktonic taxa
(80 + 20%) predominated over the meroplanktonic
organisms (20 + 3%). Concerning holoplanktonic
abundance, the highest values were attained by three
taxa: Copepoda, with 50 + 12% of total abundance,
Cladocera (13 + 12%) and Medusae (10 + 11%).
Meroplankton occurred mainly as barnacle and
decapod larvae (4 + 10 and 5 + 4%, respectively).
Copepoda were the most diverse group, represented by
26 species followed by Decapoda larvae (21) and
Medusae (16). Cumacea and Cladocera were composed
of nine and seven species, respectively.
At longer timescales, total zooplankton abundance
showed highly variability within the study period (Fig. 4),
ranging between 3 and 2548 ind. m23, with an average
of 272 + 406 ind. m23. Zooplankton abundance
Fig. 2. Monthly variation of precipitation (mm) and river runoff (dam3) from June 2005 to April 2006.
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Fig. 3. Environmental parameters recorded during each sampling period (mean + SD). T, temperature (8C); Chl a; chlorophyll a (mg m23);
SPM, suspended particulate matter (mg L21) (open circle, surface samples, closed triangle, bottom samples).
exhibited significant seasonal differences for all biological
descriptors (Table II), being generally higher in the
spring and summer. Only Mysidacea and Chaetognatha
exhibited higher abundance in colder seasons.
Regarding the Shannon diversity index and species richness, higher values were also significantly recorded in
warm months (Table I). Regarding the lunar phase, total
zooplankton abundance was generally higher at neap
tide (310 + 411 ind. m23; spring tide 251 + 405 ind.
m23), with the exception of the winter period, where
abundance was significantly higher at spring tide
(Table II). In addition, a significant interaction between
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Table I: Mean abundances (ind. m23) for the principal zooplankton taxonomical groups (%
contribution to the total zooplankton density, average+SD) and main taxa identified in Mondego
estuary for each season and lunar phase (neap and spring) and sampled depth [surface (S) and
bottom (B)]
Shaded boxes indicate significant differences in the three-way interaction between season, tide and depth (ANOVA, Bonferroni, P , 0.05). Bold
numbers indicate the significant higher depth. Values in boxes represent higher abundance tide.
Others include Amphipoda, Polychaeta larvae, Echinodermata larvae, Bivalvia and Gastropoda post-larvae, Cumacea and Isopoda groups. –, not
found.
lunar phase and depth (Bonferroni, Table II) indicates
high abundance near bottom. Although species richness
values were not significantly different between lunar
phases, higher values were recorded at neap tide in
warm months and at spring tide in colder months.
Shannon diversity index was significantly lower at neap
tide, driven by the dominance of a few species.
In the spring, the marine copepod Acartia clausi and barnacle larvae constituted the bulk of zooplankton abundance at neap tide, contributing 34 and 29%, respectively
(Table I). At spring tide, the estuarine copepod Acartia tonsa
showed the highest values (20%), followed by the appendicularian Oikopleura dioica (16%) and the hydrozoan
Muggiaea atlantica (14%), being more evenly distributed. In
summer, A. clausi composed more than 20% of total abundance. While at neap tide Penillia avirostris was also an
important contributor (20%), at spring tide Temora longicornis (17%) and O. dioica (18%) were the most abundant. In
autumn, unlike former seasons, the proportion of the
copepods increased and species composition was slightly
altered. At both tides, the freshwater copepod
Copidodiaptomus numidicus exhibited the highest abundance
(56 and 31% of total abundance, respectively). Up to this
point, a decrease in abundance was observed throughout
the seasons. However, the exception noted for winter, at
spring tide, was due to A. clausi (38%) and the marine cladoceran Evadne nordmanni (30%). At neap tide, the main
contributors were C. numidicus (18%), A. clausi (15%) and
Carcinus maenas larvae (14%).
Another strong response was observed for depth.
With few exceptions, higher abundance was found near
the bottom, with an average of 302 + 413 ind. m23,
when compared with the surface (258 + 403 ind. m23)
(Tables I and II).
Considering a short timescale, zooplankton community was strongly affected by the phases of the tidal and
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Fig. 4. Variation in total zooplankton abundance (ind. m23) at each season and lunar phase according to tidal cycle (LT, low tide; HT, high
tide) and diel phase at each sampled depth. Arrows delimit each lunar phase.
diel cycles. A detailed analysis of the zooplankton abundance and diversity highlighted the differences between
the daylight and dark periods (ANOVA, abundance:
F ¼ 45.872, P , 0.001; species richness: F ¼ 51.168,
P , 0.001; Shannon diversity index: F ¼ 11.880, P ¼
0.001) with significantly higher values at night,
suggesting the occurrence of vertical migration (Figs 5
and 6). Concerning the tidal cycle, an inconsistent
pattern was observed for zooplankton abundance and
diversity (Figs 4 and 5).
Community structure: seasonal patterns
The results of multivariate analyses demonstrated that
there were significant differences in the zooplankton
community structure, defining four major groups
(Fig. 6). A clear cycle of species abundance and composition is revealed by the MDS plot, in which the
samples are grouped by season. Group I represents the
spring samples, which occurred in warmer water.
Group II, which clustered closely to Group I, occurred
concomitantly in warm water and was associated with
higher salinities, representing summer samples. Group
III included only samples from autumn. Group IV was
associated with higher river flows and represented the
winter communities.
Despite moderate convergence of shared species
between the four groups obtained by the MDS (stress ¼
0.18, Table III), divergence was statistically significant at
all groups (ANOSIM global R ¼ 0.651, P , 0.001 for
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Table II: Results of factorial three-way ANOVA to evaluate significant differences in biologic descriptors
between season (S), tide (T) and depth (D) and their interactions
Season
Tide
Depth
Variables
F- value
F- value
F- value
Zooplankton
Species number
Shannon diversity
Holopankton
Meroplankton
Copepoda
Cladocera
Medusae
Cirripedia
Appendicularia
Decapoda
Mysidacea
Chaetognatha
14.65**
45.130**
37.818**
9.682**
138.139**
8.032**
54.045**
129.539**
230.091**
129.756**
28.991**
11.075**
80.939**
S SP W A
SP S A W
S SP A W
S SP W A
SP S W A
S W A SP
S SP W A
SP S W A
SP S W A
SP S W A
SP W S A
A W SP S
A S SP W
0.187
0.208
20.438**
0.473
5.314*
4.478*
26.749**
5.838*
43.776**
121.204**
9.936*
15.225**
0.014
NS
NS
SN
SN
NS
NS
SN
SN
NS
SN
NS
NS
NS
9.892*
15.054**
7.849*
10.336*
12.838**
9.373*
1.585
6.806
0.536
38.202**
17.228**
9.095*
9.546*
B
B
B
B
B
B
B
B
B
B
B
B
B
S
S
S
S
S
S
S
S
S
S
S
S
S
S3T
F- value
S3D
F- value
T3D
F- value
S3T3D
F- value
21.704**
17.345*
10.395**
24.212**
19.659**
21.329**
76.946**
42.841**
58.416**
5.099*
6.718**
3.776*
1.127
0.992
0.590
1.849
0.730
3.382*
0.864
0.427
1.991
0.087
0.961
1.007
1.423
5.647*
0.211
0.799
2.066
0.288
0.418
0.962
0.633
1.923
0.072
2.451
0.004
0.382
1.120
6.730
1.512
0.085
0.674
1.088
0.710
2.009
2.354*
0.487
6.949**
0.135
0.281
1.025
Pairwise comparisons are listed from highest mean (left) to lowest mean (right) (Bonferroni, P , 0.05). Interactions are highlighted in Table I.
Season: SP, spring; S, summer; A, autumn; W, winter.
Tide: N, neap; S, spring.
Depth: S, Surface; B, bottom.
P 0.05, *P 0.05, **P 0.001.
all paired comparisons tests). Since most of these species
occurred in all seasons, differences between groups
appeared to be mostly the result of the variations in its
relative abundance. Yet, markedly differences were
noted between spring/summer and autumn/winter
samples driven by a distinct zooplankton composition.
The BIOENV procedure showed that among all possible combinations of the eight environmental variables,
water temperature and salinity (that fluctuated with river
discharge) were the major variables influencing the
faunal pattern showed in the MDS ordination. Table IV
shows that SPM, in combination with the above parameters, was also closely correlated with the zooplankton community structure (third best result; rho ¼ 0.501).
Community structure: tidal and diel
fluctuations
As described earlier, zooplankton community was
affected by the phases of the tidal and diel cycles.
During the study period, the most abundant taxa
showed significant diel variations in surface waters.
Other taxa were not present in large enough numbers
over the study period for the analysis. Concerning tidal
cycle, differences in zooplankton community structure
were noted between different tidal cycle phases
(SIMPER). Such differences were greatest between high
water (+1 h) and low water (+1 h) than for other pairwise comparisons. Table V shows the species contributing most to the dissimilarity observed between high and
low tide.
A general pattern regarding the community structure
was observed throughout the sampling period.
Although differing somewhat in abundance, the zooplankton composition in spring and particularly in
summer were quite similar. Marine species which made
up the bulk of the zooplankton community were
responsible for the differences observed between the
two tidal phases, with higher abundance at high water.
Particularly in spring, the estuarine species A. tonsa was
observed with high abundance at low water, when the
extrusion of estuarine waters is at its maximum.
Conversely, the zooplankton community differed considerably in species composition in the autumn and
winter, showing a more pronounced effect of the tidal
cycle during periods of high river flow. While there was
a trend towards a freshwater community during low
tide (e.g. copepods Copidodiaptomus numidicus, A. robustus,
Daphnia longispina and Ceriodaphnia sp.), a large number
of species with marine affinities were found at high tide.
Considerably high numbers of the decapod Carcinus
maenas larvae (Zoea 1), during ebb and low tide at neap
tide were also found during the winter period.
DISCUSSION
Analysis of the zooplankton community indicated a seasonal pattern of high abundance and species richness in
warm months, common to most European estuaries
(Dauvin et al., 1998; Rawlinson et al., 2005). A seasonal
succession of numerically dominant taxa was evident
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Fig. 5. Species number and Shannon diversity index at each season and lunar phase according to tidal cycle (LT, low tide; F, flood; HT, high
tide; E, ebb) and diel phase (D, day; N, night) at each sampled depth. Shaded box represents night period.
over the study period, due to pulses of abundance variation in several holoplanktonic and meroplanktonic taxa.
As expected, the most abundant and diverse holoplanktonic taxa were the calanoid copepods. This taxonomic
group comprised 34 to 72% of total zooplankton, a usual
contribution for marine coastal areas all over the world,
especially for marine and brackish part of estuaries
(Humes, 1994; Kibirige and Perissinotto, 2003; David
et al., 2005; Leandro et al., 2007), as already stated for this
estuarine system (Azeiteiro et al., 1999; Marques et al.,
2006, Primo et al., 2009). Considering meroplankton, the
decapod larvae were the most important contributors.
This is not surprising, since the local benthic community
is composed of important decapod populations (Baeta
et al., 2005; Viegas et al., 2007), which in turn have life histories that include a planktonic larval phase. The
Mondego estuary food chain supports an important fish
community (Martinho et al., 2007). Studies performed by
Martinho et al. (Martinho et al., 2008) and Dolbeth et al.
(Dolbeth et al., 2008), who analyzed the feeding ecology
of the main fish species of the Mondego estuary, concluded that copepods were an important component of
fish diet, mainly for the juveniles of the European sea
bass Dicentrarchus labrax. Consequently, high zooplankton
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Fig. 6. Multidimensional scaling (MDS) plot for zooplankton assemblages sampled in the Mondego estuary. Dashed line shows the division
between the four main groups. circle: ebb tides, triangle: neap tides.
Table III: SIMPER analysis (cut-off 50%)
for zooplankton densities per group/season
(average group similarity) determined with the
MDS
Group and characteristic species
Group I. Spring (53.59)
Acartia clausi
Oikopleura doica
Muggiaea atlantica
Diphyes sp.
Nauplii cirripedia
Evadne nordmanni
Lizzia blondina
Group II. Summer (60.47)
Acartia clausi
Temora longicornis
Oikopleura doica
Penilia avirostris
Muggiaea atlantica
Sagitta friderici
Podon polyphemoides
Group III. Autumn (52.45)
Copidodiaptomus numidicus
Temora longicornis
Sagitta friderici
Acanthocyclops robustus
Acartia clausi
Group VI. Winter (43.87)
Acartia clausi
Carcinus maenas Zoea 1
Copidodiaptomus numidicus
Temora longicornis
Clausocalanus arcuicornis
%, percentage explained.
%
Faunal group
Table IV: Results of the BIOENV analysis of
the influence of the eight environmental
parameters on zooplankton community in
Mondego estuary
Best singles
9.6
9.4
8.1
7.9
7.4
7.0
6.8
Copepod
Appendicularian
Siphonophore
Siphonophore
Cirriped
Cladoceran
Hydromedusa
10.7
10.3
8.4
7.8
6.0
5.7
5.5
Copepod
Copepod
Appendicularian
Cladoceran
Siphonophore
Chaetognatha
Cladoceran
15.1
10.9
9.4
8.5
6.7
Copepod
Copepod
Chaetognatha
Copepod
Copepod
18.6
12.7
10.4
7.4
5.5
Copepod
Decapod
Copepod
Copepod
Copepod
Best set
Variable name
Rho
Variable name
Rho
Temp
Sal
SPM
pH
Chl a
0.513
0.304
0.265
0.216
0.079
Sal, temp
SPM, temp
SPM, temp, sal
DO, sal
SPM, Temp
0.513
0.513
0.501
0.497
0.491
The six single variables most highly correlated with the biota (best single)
and the six sets of variables which give the highest correlation (best set)
and the Spearman’s correlation coefficient (rho) are reported.
densities may lead to important trophodynamic effect on
the fish community. Furthermore, pelagic filter feeders,
such as gelatinous zooplankton and larger zooplankters,
play an important role in this estuarine ecosystem. The
gelatinous planktonic species also showed abundance
peaks during summer months, which have been reported
to have a significant impact on the zooplankton community (Azeiteiro et al., 1999). When jellyfish occur in high
numbers, their collective prey-consumption rate can be
so high that this predation directly or indirectly controls
the population size of other zooplankton organisms, such
as fish larvae (Hansson et al., 2005). This may lead to a
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Table V: SIMPER analyses for zooplankton assemblages considering tidal cycle: average Bray– Curtis
percentage dissimilarities and ANOSIM results among high tide (HT) and low tide (LT) for each
sampling occasion
Mean abundance
LT
HT
Spring neap 49.87 (ANOSIM, R ¼ 0.396, P ¼ 0.05)
Nauplii cirripedia
425
34
Acartia tonsa
45
0
Acartia clausi
44
439
Oikopleura doica
31
28
Pachygrapsus marmoratus
3
63
Summer neap 43.44 (ANOSIM, R ¼ 0.427, P ¼ 0.03)
Diphyes sp.
2
51
Muggiaea atlantica
3
56
Penilia avirostris
25
182
Oithona plumifera
8
97
Lizzia blondina
1
5
Autumn neap 48.89 (ANOSIM, R ¼ 0.344, P ¼ 0.05)
Copidodiaptomus numidicus
119
29
Ceriodaphnia sp.
5
0
Temora longicornis
2
15
Schistomysis spiritus
0
6
0
1
Evadne nordmanni
Winter neap 57.59 (ANOSIM, R ¼ 0.563, P ¼ 0.03)
Copidodiaptomus numidicus
52
0
Acartia tonsa
3
0
Carcinus maenas
26
305
Calanus helgolandicus
3
8
Daphnia longispina
1
0
Mean abundance
%
LT
HT
Spring spring 48.46 (ANOSIM, R ¼ 0.875, P ¼ 0.03)
Diphyes sp.
3
69.0
Acartia clausi
2
78
Muggiaea atlantica
5
89
Acartia tonsa
16
0
Liriope tetraphylla
1
27
Summer spring 44.59 (ANOSIM, R ¼ 0.552, P ¼ 0.05)
Penilia avirostris
2
31
Evadne nordmanni
1
39
Podon leuckarti
0
5
Podon polyphemoides
2
31
Acartia clausi
14
60
Autumn spring 56.81 (ANOSIM, R ¼ 0.979, P ¼ 0.03)
Copidodiaptomus numidicus
46
1
Daphnia longispina
5
0
Acanthocyclops robustus
7
0
Penilia avirostris
0
3
Muggiaea atlantica
0
2
Winter spring 58.64 (ANOSIM, R ¼ 0.688, P ¼ 0.03)
Muggiaea atlantica
0
18
Copidodiaptomus numidicus
65
0
Diphyes sp.
0
13
Acartia clausi
72
149
Acanthocyclops robustus
5
0
8.2
7.7
5.3
3.1
3.0
6.2
5.9
5.6
5.5
4.3
7.2
6.4
5.0
4.3
4.2
12.2
6.7
5.3
5.2
5.0
%
6.4
5.9
5.7
5.4
5.1
4.3
4.3
3.9
3.4
3.3
9.9
6.1
5.8
4.6
4.2
6.6
6.6
6.3
5.6
5.4
Mean abundance and percentage explained by the five taxa contributing most to dissimilarity.
shift in the trophic structure of the pelagic community as
a result of a trophic cascade effect.
The temporal turnover in species composition,
measured by the average similarities between seasons,
had a consistent relationship with environmental predictors. Temperature was found to be the most important
environmental factor, enough to determine species’ seasonal distribution. This fact agrees with other studies,
which demonstrated that metabolic processes in zooplankton are related to temperature (Hirst and Kiørboe,
2002; Leandro et al., 2006). Nevertheless, it is well known
that the factors that determine species distribution interact in complex ways. Temperature itself is not necessarily
the proximal factor of zooplankton distribution patterns.
In fact, a number of studies carried out in the Mondego
estuary have emphasized the significant influence that salinity has on zooplankton abundance and composition
(Azeiteiro et al., 1999; Marques et al., 2006, 2007; Primo
et al., 2009) this environmental parameter being an indicator of different water masses. Hence, the speciesspecific relationship with salinity can indicate that the
zooplankton distribution is related to different water
masses. Previous studies have shown that winter climate,
which favors high river discharge, can affect the mesozooplankton community, especially A. tonsa abundance,
an important resident estuarine species in the Mondego
estuary (Marques et al., 2007; Primo et al., 2009). It is well
known that the diffusive and advective properties of freshwater discharge play a critical role in population distribution patterns and richness, as well as in their temporal
variability (Kimmel et al., 2006). While the upper estuary
was dominated by a freshwater community at periods of
highest flow, a different scenario was observed for dry
years, the zooplankton community being dominated by
A. tonsa (Marques et al., 2007). It was suggested that the
brackish population of this species may have been drifted
away during higher freshwater flow. Moreover, during
dry years, the decreasing trend of river flow was associated with variations of hydrological parameters such as
an increase in salinity which contributed to high abundance of A. tonsa, namely in the upstream areas. While
this work has emphasized the effects of physical forcing at
short-term and vertical scales, as well as at horizontal
spatial scales resulting from the movement of water
passing through the fixed station, the brackish waters and
associated species were not represented. To take into
account spatial variability in population dynamics, at
least a second sampling location would be useful. Indeed,
this study showed that A. tonsa was not well represented
(numerically) in the zooplankton community. Besides,
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high densities were found mostly in bottom waters.
Salinity can be an important factor, limiting the occurrence of A. tonsa population (Marques et al., 2008) and
may lead to high mortality outside the optimal salinity
range. Our findings suggested that A. tonsa might have a
retention mechanism to maintain its population within a
range of brackish salinities, acting through the combined
effect of the swimming behavior that allows regulation of
vertical distribution (Kouassi et al., 2001) probably synchronized with tidal cycle, the production of diapause
eggs (Castro-Longoria, 2001) and life history traits such
as short generation times and high reproductive potential.
Further sampling and experiments are required to fully
understand these mechanisms.
In dry months, low river flow makes tidal exchange
the main process of water movement, which explains
the higher importance of marine neritic species in the
estuary. Such a composition is similar to what has been
reported in other temperate estuaries (e.g. Dauvin et al.,
1998). The present results showed that the period of
higher river flow, coincidently with autumn and winter,
resulted in changes in the zooplankton community. We
suggest that this water mass is characterized by its own
zooplankton community that is drifted away through
upstream estuarine areas. In addition, a replacement in
the community composition and abundance was
observed, and the taxa responsible for the differences in
assemblage structure were identified. Moreover, at times
of low freshwater discharge, high species richness was
observed. Exchange of water with the adjacent coastal
area broadened the salinity gradient, providing a wider
variety of marine and brackish habitats. Increasing the
likely range of habitats increases the diversity of zooplankton species that will be accommodated, which will
also result in a more even species distribution.
Conversely, previous studies, conducted in this estuarine system by Marques et al. (Marques et al., 2006),
found a lack of seasonality in zooplankton abundance.
Besides the fact that fluctuations in abundance may be
the result of specific and population patterns, the
sampling design conducted in this study did not take
into account the lunar cycle (spring and neap tides),
which was probably a source of bias in the zooplankton
abundance comparisons. As reported by Kennish
(Kennish, 1990), the structure of the zooplankton community along an estuary depends not only on the ebbflood cycle, but also on the neap-spring tidal cycle, as
has been concluded in the presently study. Indeed,
regarding lunar phase, neap tide samples had generally
greater total zooplankton abundance, with the exception of winter, where abundance was significantly
higher at spring tide. At Lough Hyne (Ireland), a
coastal marine system connected to the Atlantic Ocean,
31
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a similar pattern in mesozooplankton abundance was
observed by Rawlinson et al. (Rawlinson et al., 2005),
but much debate has focused on the underlying reason
for such observed pattern. On the Portuguese coast,
neap high tides occur early in the evening, and many of
the benthic species release their larvae during crepuscular neap high tides (Paula, 1989). These findings
suggested that rhythmic cycles of larval export are best
explained by the timing of the change in light intensity
rather than tidal amplitude and is the main factor promoting synchrony with lunar cycle. Yet, studies concerning the effect of the lunar cycle on the zooplankton
community led to the conclusion that minimum amplitude tides may be easier to swim against, and also that
nights become progressively darker between the thirdquarter and new moon, potentially reducing losses to
predation (Sponaugle and Cowen, 1997). In the present
work, spring tide samples were carried out at full moon,
when nights were more illuminated, possibly reflecting
the mechanisms described above.
According to McLusky and Elliot (McLusky and
Elliot, 2004), two features potentially limit zooplankton
abundance in estuaries: turbidity and, often more
important, tidal currents. On one hand, turbidity can
limit phytoplankton production and thus the food available for the zooplankton. In the Gironde estuary
(France), the high SPM values, and consequently, turbidity were found to affect copepod selective feeding, given
that it was responsible for a very reduced primary production, which indirectly controlled the temporal variability of copepods Acartia spp. and mysids (David et al.,
2005). In the Mondego estuary, SPM, in combination
with other parameters, was also closely correlated to the
community structure of zooplankton. However, SPM
concentration is very low comparatively with the
Gironde estuary (1 g L21 and up to 10 g L21 in the
bottom against 0.1 g L21 in Mondego estuary). In
Chesapeake Bay, Roman et al. (Roman et al., 2001) found
that some copepod species had the ability to ingest suspended sediments and detritus with their associated
microfauna, allowing species to prosper on the high particulate concentration. In the Mondego estuary a question arises: is the correlation between SMP and
zooplankton a consequence of nutritionally favorable or
unfavorable environment? To answer to this question
more sampling and experiments are undoubtedly
needed. Additionally, currents can also transport zooplankton out of the estuary. McLusky and Elliot
(McLusky and Elliot, 2004) stated that for overcoming
such stressors and maintaining themselves inside the
estuary, zooplankton species stay near the bottom and
utilize as far as possible the inflowing marine currents.
In our study, we found evidence of such mechanism,
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ZOOPLANKTON DYNAMICS AT A FINE TEMPORAL SCALE
since a clear higher abundance was observed near the
bottom. Nevertheless, currents are tidally intermittent,
and the best a species may achieve is to be carried to
and fro about one location. Yet, in the Seine estuary, a
high-frequency sampling concluded that vertical variability of zooplankton in the estuary should be considered
more like a trade-off between flushing avoidance and
predation (Devreker et al., 2008). Vertical migrations of
estuarine zooplankton may serve as a way to control
their horizontal transport when combined with tidal
streams (Hill, 1991). Such behavioral mechanisms imply
a process of tidally timed vertical migration synchrony,
which has been suggested for copepods (Dauvin et al.,
1998; Devreker et al., 2008), for meroplankton (Queiroga
et al., 1997; Pereira et al., 2000) and for mysids (Hough
and Naylor, 1992). In our study, we have evidence to
suggest tidally oriented motion. Nonetheless, these
results must be interpreted with some caution. Rapid
variations in estuarine environmental and biological parameters require a sampling frequency high enough to
capture consistent patterns of variation within the tidal
scale (Devreker et al., 2008). However, it has been shown
that decapod larval stages undergo vertical migrations.
The most common situation in first stage zoea of
Carcinus maenas is an upward migration at receding tide,
in order to maximize seaward transportation (Queiroga
et al., 1997). This pattern of migration was also observed
for the Carcinus maenas zoea in this study. Macho et al.
(Macho et al., 2005) noted that on the NW Iberian
Peninsula, barnacle larvae were released during high
tide. Here, we found high abundances of barnacle
larvae around low tide. We can speculate that this drift
could be related to the location of hard substrates along
the shore. The distribution pattern could represent tidal
flow of larvae, being displaced downstream by a combination of ebb tides and surface currents. However,
except in the case of some vertical movements that are
coupled with tidal flow in coastal regions, horizontal
movements are probably just a consequence of DVM
(Hays, 2003). Nocturnal vertical movements in the water
column have been commonly reported for different
taxa, including copepods (Rawlinson et al., 2005), and
may have different causes. Synergistic benefits might
have shaped the evolution of this complex behavior.
However, predation and physical stress are believed to
be the major selective pressure for the development of
vertical migrations (for a detailed review, see Hays,
2003). Yet, there are associated consequences for higher
trophic levels of this behavior. For example, Hays (Hays,
2003) noted that some predators at higher trophic levels
modify their behavior to exploit the vertical movement
of the food source, while at the same time possibly minimizing their own risk of predation.
In conclusion, our data demonstrate that besides tidal
changes, short-term variations in the zooplankton community may also result from diurnal cycles.
Zooplankton abundance attained significantly higher
densities at night than during the day, independent of
tidal current, following the most common pattern of
vertical migration: nocturnal migration, characterized
by an evening ascent and a morning descent. The
amplitude and pattern of migration may differ greatly
between species and between ontogenetic stages of the
same species (Rawlinson et al., 2004). The pattern
recorded in this study may also reflect the use of zooplankton net with the 335 mm mesh size. This coarse
mesh net may have under estimated the early developmental stages and smaller specimens, which may have
masked some seasonal trends corresponding to the
reproductive activities of the invertebrates within the
estuary. A more suitable spatial and temporal survey of
zooplankton has recently started with 64 and 200
micron mesh size net in Mondego estuary, in which it
will be possible to evaluate the extent of this underestimation and its biological implications. The present
study, by emphasizing the importance of different timescale changes in the zooplankton structure, will be
useful for the design of more efficient sampling programs and to document changes in zooplankton abundance at a broad but also at a fine temporal scale.
AC K N OW L E D G E M E N T S
A special thanks to all colleagues that helped during
this fieldwork. The authors wish to thank Juan Ignacio
González-Gordillo for help in the identification of
decapod larvae. Statistical advices of the colleague
Susana Mendes were very helpful for the final version
of the present manuscript.
FUNDING
The present work was supported by I.I.I. (Instituto de
Investigação Interdisciplinar of the University of
Coimbra) through a PhD grant awarded to S.C.M.
(III/AMB/28/2005).
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