Journal of Plankton Research Vol.20 no.ll pp.2109-2127, 1998
Nutrient and plankton dynamics in a Mediterranean salt marsh
dominated by incidents offlooding.Part 2: Response of the
zooplankton community to disturbances
Xavier D.Quintana1-3, Francisco A.Comfn2 and Ramon Moreno-Amich1
institute of Aquatic Ecology and Department of Environmental Sciences,
University ofGirona, Facultat de Ciencies, Campus de Montilivi, 17071 Girona,
2
Department of Ecology, University of Barcelona, Av. Diagonal, 645, 08028
Barcelona and 3Mosquito Control Service ofBadia de Roses i Baix Ter, PI. Bruel
s.n. Sector Carlit, Empuriabrava, 17486 Girona, Spain
Abstract. The composition of the zooplankton community which colonizes some temporary basins
in the salt marshes of the Aiguamolls de l'Emporda (NE Spain) was studied. The structure of the
zooplankton community depends mainly on natural and anthropogenic disturbances, which are
irregular and highly variable both in their nature and intensity. Six environmental situations with a
regular community structure have been identified by means of correspondence analysis (CA) (each
dominated by a characteristic species or taxon). The temporal pattern is described by the temporal
positioning sequence of each basin in the C A and is modelled as displacements between the six aforementioned situations. The first three CA axes relate to, respectively, the intensity of inundation (i.e.
the entry of external energy), the complexity of the zooplankton community, and special conditions
of water confinement. As the natural hydric dynamics lead the system towards desiccation (situation
of minimum external energy), the CA community representation tends to converge towards the origin
of the coordinates. On the other hand, disturbances can be considered as supplies of external energy.
By their effect on the zooplankton community structure, disturbances produce three main divergent
displacements in the CA factor space depending on the nature and intensity of the disturbance (pulse,
press or desiccation).
Introduction
The salt marshes of the Emporda wetlands (NE Iberian peninsula) show the
characteristics of a fluctuant Mediterranean system. In these wetlands, the
temporal pattern is determined by the occurrence of floods (by subterranean or
surface inputs) due to meteorological disturbances (sea storms, rainfall, etc.) and
the natural process of desiccation. These events are unpredictable and do not
follow strict seasonal patterns, although storms are usually more frequent in
spring and autumn, and most lagoons dry out in the summer. Flux regulation has
been the major factor of disturbance since January 1990, drastically changing the
flooding conditions in the whole system due to a greater input of fresh water.
Owing to the hydric dynamics, the physical and chemical characteristics of the
water depend on the flooding-related nutrient input and on the confinement
causing water masses to reach a relative oligotrophy. This impoverishment of
soluble nutrients is due to the accumulation of phosphorus in basins and nitrogen loss to the atmosphere or the aquifer, indicating a differential confinement
of nutrients (Quintana et ai, 1998, accompanying paper). Moreover, the system
dynamics is directly related to the entry of nitrogen and the entry of external
energy that removes phosphorus from sediment. Both entries are associated with
flooding events.
© Oxford University PTess
2109
X.D.Quintana, F.A.Comin and R.Moreno-Amich
It seems realistic to expect a dependence of the zooplankton community structure on the entry of external energy associated with disturbances, explaining the
high variability in the composition of the community. There are few studies
regarding the planktonic community in intermittent or fluctuant coastal Mediterranean environments (Bigot and Marazanof, 1965; L6pez et al., 1991; Toja et al.,
1991; Galindo et al., 1994). Existing studies of this type of system typically deal
with physical and chemical questions (Golterman, 1984; De Groot and Van
Wijck, 1993; Soria and Alfonso, 1993; Serrano, 1994) or the vegetation (Mesleard
etal., 1991; Pozo and Colino, 1992). Zooplankton communities have mainly been
studied in permanent lagoons (Aguesse and Marazanof, 1965; Carrillo etal., 1987;
Miracle et al., 1987; Lasserre, 1989; Heurteaux, 1992).
Changes in water characteristics occur in a temporal sequence with different
delays after flooding (Quintana et al., 1998, accompanying paper), depending
heavily on the initial state of the system and other factors affecting the system's
kinetics. Parameters related to the activity of organisms (i.e. [soluble reactive
phosphate (SRP)], [chlorophyll] and alkalinity) are the last to change, so in the
Emporda wetlands we can expect changes in the zooplankton community to
occur with stochastic delay. This makes it difficult to correlate these changes with
the intensity of flooding or the entry of nutrients. Nevertheless, it is realistic to
relate the occurrence of a disturbance with the posterior changes observed in the
structure of the community.
The aims of the present study are to obtain a functional classification of the
disturbances in a fluctuant Mediterranean salt marsh by means of their effect on
the structure of the zooplankton community and, secondly, to model the dynamics of the community, identifying the different structures of the community
related to the corresponding environmental situations.
Study area
The samples were collected from April 1989 to March 1991 in a group of temporary basins situated in the salt marsh along the coast of the Aiguamolls de 1'Emporda Natural Park. The salt marshes of the Emporda wetlands are made up by
a group of coastal lagoons and salt marshes that are not under tidal influence. The
hydrology of the area is dominated by sudden marine intrusions during sea storms
which are highly irregular, although relatively frequent. A sluice gate was
installed in this drainage channel at the beginning of 1990, during our study
period, in order to obtain a greater level of inundation in the system of lagoons.
Flux regulation due to the installation of the sluice gate has considerably altered
the hydrologic regime of the area and increased the frequency and permanence
of inundation (Quintana, 1995; Quintana et al., 1998, accompanying paper).
Four basins running in a perpendicular line to the coast were chosen. They are
small depressions of the salt marsh situated between the old sandbars where
floodwater is accumulated. Their beds are bare and are isolated from the group
of permanent lagoons. The average level of water is between 30 and 60 cm, with
the highest values (1.2 m) rarely recorded during storms. In the summer, all basins
dry out and occasionally remain dry for periods in the winter. Further details of
2110
Nutrient and plankton dynamics in a salt marsh. Part 2
the characteristics of the basins can be found elsewhere (Quintana, 1995; Quintana et al., 1998, accompanying paper). These studies show that basins 1 and 2 are
more eutrophic (mean [SRP] = 10.45 and 5.26 uM, respectively; mean [chlorophyll a] = 21.62 and 35.57 ug H, respectively) than basins 3 and 4 (mean [SRP] =
1.64 and 0.82 uM, respectively; mean [chlorophyll a] = 8.24 and 13.34 ug I"1,
respectively).
Method
A pump was used to collect water samples. Samples were taken at a depth of
10-15 cm at positions close to the central area with a frequency varying from a
week to a month during inundation periods. Each zooplankton sample was taken
from 5 1 of filtered (50 urn) water, and was preserved in 4% formalin. For the
study of phytoplankton, a further water sample was collected and, without filtering, preserved with Lugol. The physical and chemical characteristics of the water
have also been analysed in these basins (discussed in Quintana et al., 1998,
accompanying paper).
For most species, estimates of biomass were obtained from the allometric
relationship between the weight and the length of the body (Smock, 1980;
McCauley, 1984; Lawrence et al, 1987; Malley et al., 1989; Meyer, 1989). For
phytoplankton, rotifers, medusae and polychaetes, biomass was calculated by
converting volume into dry weight (Ruttner-Kolisko, 1977; McCauley, 1984;
Reynolds, 1984; Malley et al., 1989; Schonborn, 1992). Volume was estimated
from the measurements of the principal diameters of the organisms. The development stages of taxonomic groups with greatly differing sizes were grouped by size
in order to obtain greater precision in the estimation of the biomass (Table I).
The smaller forms of larvae were classified at the lowest taxonomic level possible, which is higher than species.
The variability of zooplankton (>50 um) was analysed through CA using the
VAX version of the BMDP statistical program (Dixon, 1988). This type of analysis is adequate when species abundance is used and when a unimodal relationship of the correlated variables is to be expected (Digby and Kempton, 1987;
Jongman et al., 1987). We have not taken into consideration those species of
zooplankton which only appear in one sample nor those in which there were <25
individuals (~5 ind. I"1). The regression parameters of the biomass size spectra
were calculated following the methodology given in Rodriguez (1994).
Results
Specific composition and seasonal patterns of the zooplankton
The specific composition of the zooplankton community was dominated by copepods and rotifers (Table I). Amongst the copepods, the calanoids Eurytemora
velox and Calanipeda aquae-dulcis, as well as the cyclopoids, Diacyclops bicuspidatus odessanus and Diacyclops bisetosus, were the most abundant during the
flooded period. The rotifers, Brachionus plicatilis, Synchaeta spp. and Hexarthra
fennica, present abundance peaks of >1000 ind. I"1. Considering the biomass
2111
X-D.Quintana, F-AXomin and R-Moreno-Amich
(Table I, Figure 1), the amphipod, Gammarus aequicauda, and the medusa,
Odessia maeotica, presented higher concentrations than copepods and rotifers.
Fish were almost entirely absent due to the dry periods of the basins. The virtual
absence of cladocera (only some specimens of Daphnia g. pulex occasionally
appeared) is also notable.
Table L Species composition of the zooplankton community. The codes are the same as those used in
the figures. Species with significant size differences during their development have been size grouped.
If applied, the size group is indicated after the name of the organism by roman numerals. N, nauplius
stage; Cpd, copepodite stage. Data refer to the whole study
Code
ciM
odmal
odma2
odma3
odma4
brpli
Rotifera
nosqu
nostr
coadr
synsp
tepat
tecly
hefen
Nematoda
nemat
polyd
Annelida
polk:
Cladocera
dapul
calnl
Copepoda
caln2
caln3
calcl
calc2
calc3
caad
euve
cycnl
cycn2
cycn3
cyccl
cycc2
disc
diod
aero
harnl
ham2
harn3
hard
harc2
meli
hali
Oslracoda
ostra
Amphipoda gaael
gaae2
gaae3
gaae4
Diptera
aedel
aede2
aede3
aede4
aecal
Cilia ta
Cnidaria
2112
Species
Size range
(jim)
length (width)
Abundance
(ind. I"1)
mean (max.)
Biomass
(Mgl-1)
mean (max.)
Euplotes sp.
Odessia maeotica I
O.maeotica II
O.maeotica III
O.maeotica IV
Brachionus plicatilis
Nolholca squamula
N.slriata
Colurella adriatica
Synchaeta spp.
Testudinclla patina
T.clypaeata
Hcxanhra fennica
indet. nematodes
Polydora sp.
indet. polychaetous larvae
Daphnia g. pulex
Calanoida NI
Calanoida Nil
Calanoida NIII
Calanoida Cpd I
Calanoida CpdII
Calanoida CpdIII (E.velox)
Calanipeda aquae-dulcis
Eurytemora velox
Cyclopoida NI
Cyclopoida Nil
Cyclopoida NIII
Cyclopoida Cpdl
Cyclopoida CpdII
Diacyclops bisetosus
D.bicuspidatus odeaanus
Acanthocyclops robustus
Harpacticoida NI
Harpacticoida Nil
Harpacticoida NIII
Harpacticoida Cpdl
Harpacticoida CpdII
Mesochra lilljeborgi
Harpacticus littoratis
indet. ostracods
Gammarus aequicauda I
Caeauicauda 11
C.aequicauda HI
G.aequicauda IV
Aedes detritus I
A.detritus II
A.detritus HI
A.detritus IV
A.caspius I
100-170 (60-80)
210-800
900-1500
1600-3000
3000-«000
100-*60 (50-330)
140-250(70-130)
140-250(70-130)
100-130 (50-80)
70-250 (50-160)
160-190(140-170)
130-180(90-120)
120-360(90-240)
150-1400(10-50)
80-1900(40-200)
400-450(250)
550-2080
120-200
200-300
300-450
280-660
650-980
1000-1290
800-1855
1190-2395
60-120
120-190
200-300
230-500
500-1000
900-1465
930-1335
800-1495
60-110
110-160
160-260
180-400
410-680
600-750
600-1045
300-1300
1000-2000
2100-4800
4700-7500
7600-18 000
1100-2800
2900-4400
4500-6400
6500-8500
1100-1900
0.02 (1.56)
0.15 (11.00)
0.03 (2.40)
0.04(1.60)
0.02 (0.89)
451.41(16 537.60)
7.93 (833.25)
7.32 (833.25)
2.49 (131.00)
45.45 (1376.89)
0.01 (1.60)
0.92 (22.40)
42.54 (241333)
0.06 (6.40)
3.69 (189.60)
0.02 (2.00)
0.04 (5.33)
46.58 (909.18)
22.75 (414.67)
9.39(145.33)
6.88 (223.56)
7.49(241.33)
2.32 (37.56)
4.40(361.56)
3.42 (160.67)
44.91 (557.56)
77.62 (1282.22)
26.40(366.22)
13.12(624.00)
5.08 (97.78)
0.06 (5.33)
0.27(12.44)
0.01 (0.44)
7.05 (170.22)
4.75(153.60)
0.80(70.40)
0.25 (13.10)
0.42(31.06)
<0.01 (0.25)
0.20 (13.40)
0.01 (1.00)
0.02 (1.56)
0.03 (1.78)
0.04 (2.22)
0.03 (1.00)
<0.01 (0.22)
0.01 (0.50)
0.01 (0.67)
<0.01 (0.22)
0.01 (0.80)
<0.01 (0.05)
0.33 (19.87)
1.04 (66.43)
19.17(1863.68)
28.78 (2106.88)
36.85 (2298.48)
0.16(14.96)
0.16(14.96)
0.04 (2.07)
2.26 (70.86)
<0.01 (0.06)
0.02 (0.46)
10.33 (641.57)
<0.01 (0.04)
0.51 (29.36)
0.02 (1.82)
0.12(12.13)
2.62 (52.86)
2.74 (47.74)
2.71 (41.24)
5.35 (178.08)
15.33(551.33)
9.34 (154.32)
17.54(1402.15)
23.58 (980.33)
0.83 (10.74)
2.85 (57.07)
2.48(41.06)
3.42 (138.08)
4.20 (94.52)
0.14(12.51)
0.61 (29.62)
0.02(1.24)
0.10 (235)
0.14 (3.68)
0.04 (3.29)
0.05 (2.80)
0.21 (16.54)
<0.01 (0.26)
0.17 (10.32)
0.02(2.17)
0.18(16.79)
5.89 (338.53)
26.77(1131.27)
93.00(4719.81)
0.01 (0.89)
0.45 (27.64)
0.92(113.28)
0.42 (63.73)
0.01 (1.45)
c
3'
a.
•o
s
I
1
Biomass
ACARI
ANELLIOA
CNIDARIA
S
.
I
I
.
S
I
S
z
B'
e
X-D.Qaintana, F.A.Comin and RJHoreno-Amich
Brachionus plicatilis formed extremely dense populations as summer
approached in those basins which were more eutrophic and with a higher level of
alkalinity (Figure 2). We found densities of >16 000 ind. H, favoured by the
tendency towards the concentration of organisms when level diminution was
drastic and presumably the incidents of hypertrophy were frequent (Quintana,
1995). We also found B.plicatilis in winter, although in much lower densities and
always related to an increase in eutrophy. At least three species olSynchaeta have
been found in the basins: S.kitina and two species of marine origin which we have
not been able to determine at species level in the absence of live specimens. No
clear pattern was observed to explain the distribution of these three species in the
basins and mixtures were often present. The populations of Synchaeta spp. developed immediately after major level increases (Figure 2), caused by sea storms or
rainfall, but later decreased as populations of copepods increased. Their abundance diminished considerably after the flux regulation, although the changes
provoked by the introduction of flux regulation caused an increase in their populations at first. Among other rotifers, only Notholca squamula, Notholca striata,
Colurella adriatica and Hexarthra fennica gave >25 ind. I"1 (Table I). All these
species increased their densities after flux regulation (Figure 2). Hexarthra
fennica appeared principally in the less eutrophic basins, coinciding with
moments of maximum hydric stability, whilst the others appeared principally in
the more eutrophic basins.
The calanoids were the dominant organisms in the zooplankton community
(Figure 3), especially in winter and in relatively stable conditions (stable levels in
periods without rainfall): E.velox often appeared as the only species in zooplankton samples. Another calanoid, C.aquae-dulcis, substituted E.velox as the
summer approached and the level of eutrophy increased. The cyclopoids
increased considerably in number after flux regulation (Figure 3), especially
D.bicuspidatus odessanus, which was present throughout the year, with the
highest densities in autumn and winter. Diacyclops bisetosus appeared immediately after the entry of significant quantities of water, always where there were
not very high levels of eutrophy and salinity. These populations later decreased
rapidly.
Of the harpacticoids, only Harpacticus littoralis showed relatively stable populations in 1989 before flux regulation. The abundance of H.littoralis decreased
considerably after this event. During the second year, the presence of adult
harpacticoids was slight, although there were abundant populations of larvae.
The few adult specimens that were captured during the second period were
Nitocra spinipes and Mesochra lilljeborgi.
The amphipod G.aequicauda (Figure 3) was especially abundant in the spring
in all basins (except basin 3 during spring 1989), although densities of
Fig. 2. Temporal patterns of the most abundant rotifers at each basin. Abundance refers to ind. I"1.
The arrows indicate the main disturbances that occurred during the study period: T, intense sea storm
(>1 day with waves >3 m); t, low-intensity sea storm (<1 day with waves >3 m); P, intense rainfall that
produces an increase of water volume of >50%; p, intense rainfall that produces an increase of water
volume of <50%; R, beginning of the flux regulation. Black points correspond to more eutrophic
basins and white points correspond to less eutrophic basins.
2114
Nutrient and plankton dynamics in a salt marsh. Part 2
T
T
E
8
-
6
-
p
t
p
JLJL
VV
10
R
_y_
Brachionus plicatilis
•— Basin 1
J
— •Basin 2
— - oBasin 3
— «• - - Basin 4
4 —
2
-
I
Synchaeta spp.
T
10
Nothoica spp.
0)
o
c
8
-
CO
6
-
3
4
-
2
-
T3
0
10
Colurella
8
-
6
-
4
-
2
-
0
adriatica
-i
-i—| "*!>»*< y y
1 r—P-xp
10
8
-
6
-
Hexarthra
fennica
? ft
'9 • » "
4 —
2
0
6.
-
rwTfjiAisioirTT5iT3v
1989
^T
"ST
1 991
2115
X.D.Qiiintana, EA.Comin and R-Moreno-Amich
G.aequicauda also increased in later winter in conditions of high confinement. In
the summer, when the basins dried out, there was significant accumulation of this
species on the beds of the basins.
Dense populations of the medusa, O.maeotica, appear in a very specific fashion,
mainly in the spring and in basin 3 (Figure 3), which has high values of salinity
and a low nitrogen/phosphorus ratio. It was always absent in conditions of high
eutrophy. The predatory effect of O.maeotica drastically reduces the density of
copepods, its principal food source (Picard, 1951; Morri, 1981). The appearance
of polychaete larvae {Polydora sp.) was characteristic, coinciding with the occurrence of O.maeotica. We did not, however, capture more advanced development
stages of this organism.
The temporal pattern of variation by means of correspondence analysis
We have considered the first three principal axes of the CA, which explain 40.6%
of the variance (Figure 4). Spearman correlation coefficients between these three
axes and those variables related to the environmental characteristics and those
related to the community structure are shown in Table II.
Starting from the representation of samples and species in the factor space of
the three first axes, we identify six environmental situations with a regular
community structure (Figure 4).
Table II. Spearman correlations between the first three axes of the correspondence analysis and
diverse variables. Only significant correlations (P < 0.001) are presented
Variable
Axis 1
Axis 2
Axis 3
Level
Conductivity
Temperature
[NO2-]
[SRP]
[DIN]/[SRP]
(NH,* + NO2-)/[DIN]
[Chlorophyll a]/phytoplankton biovolume
Phytoplankton/zooplankton ratio (dry weight)
Zooplankton biomass (dry weight)
N (number of zooplankton individuals)
S (number of zooplankton size classes)
r (correlation coefficient of BSS)
B (slope of BSS)
Eigenvalue
% of explained variance
Accumulated %
0.3856
-0.5500
_
-0.3567
0.3779
-0.5385
-0.3566
0.9508
14.2
14.2
—
0.3935
0.5760
0.4374
0.4617
-0.4147
-0.5150
-0.5981
0.9148
13.6
27.8
—
0.5074
0.5894
0.4290
0.3527
-0.4173
-0.3824
-0.4525
-0.4247
0.8579
12.8
40.6
SRP, soluble reactive phosphate; DIN, dissolved inorganic nitrogen (NH4* + NO2" + NO3"); BSS,
biomass size spectrum.
Fig. 3. Temporal patterns of calanoid, cyclopoid and harpacticoid copepods, the amphipod
G.aequicauda and the medusa O.maeotica at each basin. Legend as in Figure 2.
2116
Nutrient and plankton dynamics in a salt marsh. Part 2
8
08
T3
C
3
X)
<
2.5
-
Gammarus
aequicauda
2 -.
1-5 H
1
0.5
r
-_
SA
0
3
Odessla
2.5 -_
• — Basin 1
2 ^
1.5 ^
1 -_
— •— o-
Basin 2
Basin 3
— o- - - Basin 4
»
0.5 -!
0
maeotlca
y j A
1989
O
Jrj
1990
1 991
2117
XJJ.Qnintana, F.A.Comfn and RJHoreno-Amich
Synchaeta situation
CM
Brachionus situation
jn
3
0
0.5
1
1.9
2
2.5
1.2
1.4
axis 1
Odessia situation
°
Gammanis situation
CM
J2
X
Cydopoids situation
i
/
•/-fcT* ^ \
0dma2
/
odma;
.
.
.
i
. Odessia situation °
a
co
•
basin 1
•
o
basin 2
basins
o
basin 4
'• { y7 .
~~S" Gammanis situation
o \
u
»•
-1
-0.5
0
0.9
I
axis 1
2118
CM a OB anSSt"
19
Nutrient and plankton dynamics in a salt marsh. Part 2
Situation 1. Situation dominated by calanoids (henceforth 'calanoids situation').
It is a relatively oligotrophic situation corresponding to periods of hydric stability
without entries of nutrients occurring during periods of meteorological stability.
Samples from these periods are characterized by the abundance of the calanoid
species.
Situation 2. Situation dominated by cyclopoids (henceforth 'cyclopoids situation')
corresponding to periods of hydric stability with a low rate of nutrient entry.
These samples have positive coordinates for axis 1 and the most negative ones
for axis 2. The continuous inflow of fresh water after the flux regulation shows a
similar and more persistent effect. Samples from these periods are characterized
by cyclopoid dominance (especially D.bicuspidatus odessanus), with the presence
of other species such as calanoids and most rotifers, especially H.fennica,
N.striata, N.squamula and Cadriatica.
Situation 3. Situation dominated by Synchaeta spp. (henceforth 'Synchaeta situation') corresponding to sudden and massive inundations with entry of nutrients.
These samples have the most positive coordinates for axes 1 and 2. Any important flood due to storms, important precipitations, or the beginning of flux regulation, causes a major disturbance to the zooplankton community. Samples taken
after these events are almost entirely made up of Synchaeta spp.
Situation 4. Situation dominated by G.aequicauda (henceforth 'Gammarus situation') corresponding to periods of confinement in which the decrease in water
level favours the development of benthic species, especially G.aequicauda and
some harpacticoids. This situation is frequent during the spring and at the beginning of the summer. These samples have coordinates close to zero for both axes
1 and 2. The presence of calanoids accompanying G.aequicauda and harpacticoids
is also characteristic.
Situation 5. Situation dominated by O.maeotica (henceforth 'Odessia situation')
corresponding to periods of confinement in oligotrophic conditions. The samples
from these periods are especially discriminated by axis 3. These periods appear
only in the less eutrophic waters (basins 3 and 4) where confinement leads to high
salinity, high temperatures and lack of inorganic nitrogen. The characteristic
species are O.maeotica and Polydora sp.
Situation 6. Situation dominated by B.plicatilis (henceforth 'Brachionus situation') corresponding to periods of high concentration in eutrophic basins during
which incidents of hypertrophy are presumably frequent (Quintana, 1995). These
Fig. 4. Bidimensional representation of samples and species in the CA factor space of the three first
axes: top graph, in the factor space (1, 2); bottom graph, in the factor space (1, 3); middle graph,
amplification of the highlighted area of the top graph. Circles indicate the samples corresponding to
the situations explained in the text. Codes identify the species according to Table I. Black points correspond to more eutrophic basins and white points correspond to less eutrophic basins.
2119
X-D.Quintana, EA.Comin and ILMoreno-Amich
periods always result from intense evaporation, at the end of spring and at the
beginning of summer, when the basins are nearly dry, and only in the more
eutrophic basins (basins 1 and 2). Samples from these periods are characterized
by the abundance of B.plicatilis.
The order of the aforementioned situations by their axis 1 coordinates is, from
positive to negative value: Synchaeta, cyclopoids, calanoids, Gammarus, Odessia
and Brachionus. Positive coordinates correspond to situations of flooding events,
while negative ones correspond to periods of desiccation. Given this, the first axis
can be interpreted as an 'inundation-desiccation' gradient related to disturbances
and environmental fluctuations. The correlation (Table II) between axis 1 and
water level is in agreement with this interpretation. Since inundation supplies
nutrients which support the growth of phytoplankton, significant positive correlation of axis 1 with phytoplankton/zooplankton ratio, and negative correlation
with zooplankton biomass and the slope of the biomass size spectrum (B), also
support this interpretation. Axis 1 also presents a negative correlation with the
concentration of chlorophyll per unit of phytoplankton biovolume which may be
due to the dominance of mixotrophic species, such as dinoflagellates and chrysophytes (Quintana, 1995), at the beginning of the inundation. The effect of concentration depends on the quantity of material that entered during prior inundations
which has accumulated in the basins. Thus, the more negative coordinate in axis
1 (maximum concentration) is only attained in the more eutrophic basins (Figure
4)—those which have received greater contributions and in which hypertrophic
events are probably frequent.
The order of the situations for the second axis is, from positive to negative
coordinate value: Synchaeta (the situation mainly discriminated by this axis),
Brachionus, Odessia, Gammarus, calanoids and cyclopoids. The 'Synchaeta situation' is dominated by opportunistic species which form a community of low
complexity. At the other extreme, other situations follow a gradient of complexity where the 'cyclopoids situation' is the most complex situation with a greater
number of species. Thus, the second axis can be interpreted as a complexity gradient of the zooplankton community, related to the differential effect of disturbances on the complexity of the community. The significant correlation (Table II)
of axis 2 with the number of size classes (5) and the correlation coefficient (r) of
the biomass size spectrum—r has been related to the structure of the community
(Gaedke, 1992; Rodriguez, 1994)—support this interpretation.
The third axis discriminates the 'Odessia situation' (with positive coordinates)
from the rest (all of them with coordinates of about zero). The hypothesis that
the 'Odessia situation' corresponds to a situation of confinement in moderately
eutrophic basins (basins 3 and 4) with conditions of elevated salinity, high temperatures and lack of inorganic nitrogen, is supported by several significant correlations which have been found (Table II). Moderate eutrophy would permit the
effective oxygenation of the whole mass of water, whilst confinement would
favour the exhaustion of nitrogen and the diminution of the N/P ratio (Quintana
et al., 1998, accompanying paper).
The temporal pattern for each basin can be described by the temporal positioning sequence of each basin in the factor space of the first three axes and it can be
2120
Nutrient and plankton dynamics in a salt marsh. Part 2
modelled as displacements between the six situations that we have described
(Figure 5). Thus, the natural dynamics of inundation -» desiccation is modelled
by 'calanoids situation' -» {'Gammarus situation' displacements, eventually
'calanoids situation' —* 'Brachionus situation1 if the concentration of organic
matter is very high, or 'calanoids situation' -» 'Odessia situation' in more oligotrophic conditions. Sudden disturbances due to sudden and massive inundation
with nutrient entries are modelled by 'calanoids situation' -> 'Synchaeta situation'
displacement. Finally, slow continued fertilization (low-intensity disturbances or
continuous inflow of fresh water after flux regulation) is modelled by the
'calanoids situation' —»'cyclopoids situation' displacement.
Discussion
The structure of the zooplankton community
The composition of the zooplankton community in the basins studied is characteristic of Mediterranean coastal lagoons with medium to high mineralization
(Aguesse and Marazanof, 1965; Margalef, 1969). The absence of Cladocera, in
particular, distinguishes the situation from that of fresher coastal waters (Bigot
and Marazanof, 1965; Lopez et al., 1991; Galindo et al., 1994), Species composition in Mediterranean salt marshes is clearly conditioned by the salinity, as is
typical in coastal and estuarine environments (Ambrogi et al., 1989; Bamber et
al., 1992; Oltra and Miracle, 1992). However, in the salt marshes of the Emporda
wetlands, species composition depends much more on the tolerance of species to
variation in salinity. Fluctuations in the salinity are frequent events (Quintana et
al., 1998, accompanying paper), which occur in a much shorter time period than
that needed for most species of zooplankton which colonize the basins to develop.
Synchaeta
situation/^7\
'-
I1
• Brachionus situation
:(^,
O
A J-|
Odessia situation
'ka&nokls situation
ZAP*—-^
Gammarus situation
^
)
Cyclopoids situation
' i
•
•
i
I
i
i
i
.
I
•
i
•
i
I
•
i
•
•
I
.
•
.
,
I
.
.
,
.
i
.
.
•
•
1
O.S
axis 1
Fig. 5. General dynamics in the CA factor space (1,2) of the zooplankton community, related to the
action of different types of disturbances. Disturbances are indicated by: P, high-intensity pulse disturbance; F, low-intensity press disturbance; H, incidents of hypertrophy.
2121
X.D.Quintana, EA.Comin and R.Moreno-Amich
Species which do not support sharp changes in salinity are not, therefore, to be
found.
In the Emporda wetlands, the temporal pattern is determined by the occurrence of floods due to meteorological disturbances and the natural process of
desiccation, and since 1990, also to flux regulation. An extended low-intensity
disturbance (included in the 'cyclopoids situation') is the continuous inflow of
fresh water during periods of flux regulation which produces a slow continued
fertilization.
The 'calanoids situation' appears in relation to oligotrophic conditions derived
from confinement. In this competitive situation, the most efficient species (the
calanoids E.velox and Caquae-dulcis) are at an advantage and simpler communities are made up principally by different size groups of them. The trophic strategy of the calanoids based on the filtration of small particles from a wide range
of sizes seems to be more efficient than the more selective capture of larger
particles which is typical of the cyclopoids.
Desiccation drastically reduces planktonic production and the community
becomes dominated by species which feed on benthos. In moderately eutrophic
conditions, the most usual situation, the community is dominated by the amphipod, G.aequicauda, and some harpacticoids ('Gammarus situation'). It is
common to observe a high concentration of dead G.aequicauda in the deepest
points of the basins after desiccation.
In more oligotrophic conditions with high salinity, high temperature and a lack
of inorganic nitrogen, the medusa, O.maeotica, and larvae of the polychaete Polydora sp. ('Odessia situation') are the dominant species. At the beginning of the
desiccation process, O.maeotica takes advantage of the zooplankton concentration, its polyp growing on the colonies of Ficopomatus enigmaticus (Picard,
1951; Morn, 1981) which were frequent in our area of study, especially in basin
3. The capacity of O.maeotica to control the copepod populations was extraordinary, an abiiity which is not common in the majority of lagoon medusae (Daan,
1986; Purcell, 1992; Purcell and Nemazie, 1992). In just a few days, the populations of copepods were reduced to only some isolated harpacticoid larvae and
a few adult harpacticoid specimens (generally H.littoralis).
In the most eutrophic conditions, confinement also causes the concentration of
organic matter that can be consumed by detritivorous zooplankton ('Brachionus
situation'). The excess of concentration probably causes hypertrophic events with
crisis of anoxia. The regular exhaustion of oxygen during the night is a frequent
event in other hypertrophic environments and limits the plankton community to
a few species which are able to tolerate periods without oxygen. The abundance
of B.plicatilis in these conditions and the ecological characteristics of this species,
adapted to prolonged periods without oxygen (Walker, 1981; Miracle et al., 1987,
1988; Esparcia et al., 1989), are in agreement with this interpretation. This species
filters the great quantity of particles of organic matter which are accumulated by
the concentration in a not very selective way (Walker, 1981). The presence of this
species is almost exclusive in this situation.
Any flood with entry of nutrients dilutes the populations of zooplankton,
expands the habitat area, and increases resources due to the phytoplankton
2122
Nutrient and plankton dynamics in a salt marsh. Part 2
bloom. This gives extra space to be occupied by zooplankton and extra resources
to feed. Nevertheless, major changes are due more to nutrient entry with flooding than to the increase in habitat area, and the consequent population dilution,
or to changes in salinity. A counterexample supports this hypothesis: during an
intense spring sea storm, there was an entry of marine water that increased the
volume of water in basin 1 significantly, without any important entry of nutrients
being detected. After this event, the zooplankton community did not present
changes in the species composition, but dominance changed from adults of the
calanoid E.velox to larvae of the same species.
However, the way the system responds depends much more on the rate of entry
of water and nutrients than on the quantity of these entries. A high turnover rate
is associated with a sudden, massive and brief flood. A sudden availability of
nutrients leads to a rapid increase in numbers of small species such as Synchaeta
spp. which have a high rate of population growth, and a drastic change in the
community composition is observed ('Synchaeta situation'). Synchaeta spp. have
a specialized diet adapted to the capture of relatively large prey (Gilbert and
Bogdan, 1984) which allows them to take advantage of the bloom of phytoplankton caused by the intense disturbances before the appearance of copepods.
A low turnover rate is associated with a slow, continuous and longer flood. The
consequent high and long production permits the maintenance of a greater
number of species ('cyclopoids situation'). The community is relatively complex
and structured (the corresponding samples contain the majority of the detected
species) and is dominated by the cyclopoids, principally D.bicuspidatus
odessanus, accompanied by calanoids and the rotifers H.fennica, N.squamula,
N.striata and Cadriatica.
Stability, disturbances and ecological meaning of the main CA axes
As has been stated before, we have found that the main CA axes are related to
disturbances or environmental fluctuations in the salt marshes of the Emporda
wetlands. Similar results are given by ordination from physical and chemical variables (Quintana et al., 1998, accompanying paper). This seems to differ from the
characteristic patterns of other lakes and lagoons in which zooplankton composition is related to variation in temperature, salinity and nutrient concentration
(Miracle, 1974; Gulati et al., 1992; Van Tongeren et al., 1992). Many analogies can
be found, however, if we compare the functioning of different aquatic systems in
terms of input of external (auxiliary) energy. In fact, temperature, salinity and
nutrient concentration vary on a seasonal basis related to the warming cycle and
the hydrological processes (stratification and mixture, horizontal currents or flow
variation), and we can even go so far as to say that the warming cycle and hydrological processes are the expression of the entry of external energy in lakes and
lagoons. Salinity may also be an expression of the external flux of energy circulating through some coastal lagoons (Comm and Valiela, 1993; Herrera-Silveira,
1993). Analogously, hydrological fluctuations and disturbances are the principal
form of entry of external energy in fluctuating systems like the salt marshes of the
Emporda wetlands.
2123
X-D.Quintana, F.A.Comin and R.Moreno-Amich
Thus, the first axis which is related to the inundation can also be defined as an
axis expressing the input rate of external energy. External energy moves water
which transports or mobilizes nutrients and fertilizes the system. The most positive coordinate in this respect ('Synchaeta situation') would correspond to a high
rate of external energy entry which rapidly increases primary production. At the
other extreme, the 'Brachionus situation' would correspond to a situation with a
'negative rate' due to water escapes by evaporation and infiltration. Desiccation
reduces the water volume of the basin and so concentrates the organic matter. In
this situation, the system dissipates the energy contained in the accumulated
organic matter, instead of fixing energy through primary production. The excess
of organic matter favours the domination of the community by heterotrophic
species corresponding to the detritic pathway. It is clear that the accumulated
organic matter comes from a previous situation of eutrophy (the 'Brachionus situation' only occurs in the more eutrophic basins). In this situation, the autotrophic
pathway is unable to carry all thefluxof energy and a large portion of the primary
production bypasses it to be directly accumulated as dead organic matter.
The major difference between the salt marshes of the Emporda wetlands and
other aquatic systems is the frequency and unpredictability of its environmental
variations. Bender et al. (1984) makes a distinction between two different types
of disturbance, 'pulse' and 'press' types, depending on the treatment they receive
on being studied. Other authors have used similar distinctions in order to create
models for disturbed systems, such as 'initial conditions' or 'persistent conditions'
by Vincent (1987). In the 'pulse' type, the disturbing factor acts intensively and
briefly, causing sudden and drastic changes in the aquatic system, after which the
community restores itself to the previous or similar situation. Our 'Synchaeta situation' coincides with this type. In the 'press' type, the disturbing factor acts more
progressively and for a longer period. Changes in the community are gradual, and
if the disturbance lasts long enough, the community achieves a new structure
which remains while these conditions continue. In our study, the 'cyclopoids situation' would be an example of this type (Figure 5).
From the point of view of the zooplankton community, the natural tendency to
oligotrophy of the limnetic systems (Margalef, 1983) leads the community to the
'calanoids situation' when the cause of disturbance disappears. Therefore, it can
be considered to be the most stable situation during periods of inundation.
Dominance in this situation corresponds to efficient species (calanoids) with a
lower individual and population growth rate. Although the 'calanoids situation'
is the most stable situation, if the conditions brought by a disturbance of the
'press' type last enough time, the community will achieve a temporary stable
structure in accordance with these new conditions ('cyclopoids situation'). Nevertheless, the maintenance of this structure requires a continuous external energy
entry (such as in flow cultures).
The natural hydric dynamics leads to desiccation, and consequently the
community tends towards the 'Gammarus situation'. Desiccation represents a
situation of minimum flux of external energy and hence the inexorable convergence of the system. In this sense, the 'Gammarus situation' acts as an attractor
to its central position in the CA factor space (1, 2, 3).
2124
Nutrient and plankton dynamics in a salt marsh. Part 2
Intense energy inputs increase primary production, but they also destabilize the
connections along the food chains and in some other relationships, decreasing the
diversity (Margalef, 1997), as has been observed in the 'Synchaeta situation'. The
high coordinate in axis 2 is related to little complexity in the zooplankton
community: little diversity, a small number of species and size classes, and
destructuring (low r value for the linear adjustment of the biomass spectrum). In
relation to this, axis 2 may be useful to quantify the importance of a disturbance
by a destructuring effect on the zooplankton community, independently of the
origin, type and intensity of the disturbing factor. The utilization of such 'internal'
measurements to evaluate the intensity of the disturbance has, however, the risk
of confusing the effect with the cause (Sommer et al., 1993), and will only be useful
if the disturbance has had an effect upon the community under consideration.
Acknowledgement
This work was supported by a grant from the Comision de Investigaci6n Cientifica y T6cnica (CICYT), Programs de Recursos Hidricos (ref. HID96-0916).
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Received on July 22, 1997; accepted on June 22, 1998
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