Hydrobiologia 522: 165177, 2004.

2004 Kluwer Academic Publishers. Printed in the Netherlands.

165

Resilience of a zooplankton community subjected to marine intrusion in a

tropical coastal lagoon
Betina Kozlowsky-Suzuki & Reinaldo Luiz Bozelli
Laboratorio de Ecologia do Plncton, Universidade Federal do Rio de Janeiro, Departamento de Ecologia, CCS,
CEP 21941-590, Rio de Janeiro, RJ, Brazil
Present address: Marine Biology, Lund University, Campus Helsingborg, Box 882, 25108, Helsingborg, Sweden
E-mail address: betina.kozlowsky-suzuki@ekol.lu.se
Received 2 October 2002; in revised form 8 October 2003; accepted 2 December 2003

Key words: zooplankton, tropical coastal lagoon, sand bar opening, persistence, resilience

Abstract
One of the main disturbances on Imboassica Lagoon is the occasional artificial opening of its sand bar. Following
two such events, two environmental gradients were observed. One was directly related to entry of marine water
(salinity gradient); and the other to a decrease in dilution of the nutrient load, because of water level reduction
(trophic status gradient). Two stations were sampled. At Station 1, located near the sand bar, salinity increase
caused a decrease in the total zooplankton density and a shift in community composition due to a loss of relatively
small individuals (i.e. rotifers) and the subsequent entrance of larger ones (i.e. copepods). High diversity was related
to salinity increases. At Station 2, located near the mouth of a sewage canal, the total zooplankton abundance and
dominance were related to the salinity increase, while the highest richness and the lowest dominance were obtained
at a high trophic state. The zooplankton community showed high persistence and resilience, which together with
other ecological features in the system, returned to the pre-disturbance state 2 months after the sand bar was closed.
Canonical correspondence analysis was a useful tool to assess system resilience.

Introduction
One of the central issues in ecology concerns the existence and strength of relationships between ecosystem
biodiversity and functioning. In this perspective, disturbances (anthropogenic or otherwise) may induce
responses of biodiversity and ecosystem functioning
(Loreau et al. 2001) through qualitative and quantitative changes in natural populations and communities (Connell & Sousa, 1983). Persistence is merely
expressed by qualitative changes and indicates that
populations and species either did not become extinct
during a given period of time and in a given area or if
extinction occurred that they managed to re-establish
within a time span required for one turnover of all
the individuals in the population (Connell & Sousa,
1983). Stability refers to the capacity of the system to
either resist or to return to pre-disturbance state after
significant changes (Connell & Sousa, 1983).

Coastal lagoons are inland water bodies occupying 13% of coastal areas worldwide, which are either
isolated from the sea by a barrier, or connected to
the ocean by one or more restricted inlets (Kjerfve,
1994). Located between land and sea, such systems
act as filters, retaining inorganic and organic nutrients
and material, which in combination with their relatively shallow depth, high penetration of solar radiation
and frequent water column mixing, usually result in
high biomass production (Kjerfve, 1994; Castel et al.,
1996). Because of these characteristics such systems
tend to be highly impacted by anthropogenic activities.
Anthropogenic impacts on coastal lagoons include the
acceleration of the eutrophication process and in many
cases the artificial opening of a channel in the sand
bar that isolates some coastal lagoons from the ocean.
Such interventions are made to improve and renew fish
stocks, export inorganic and organic material to the

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sea, and to increase seawater inflow and water renewal
(Sei et al., 1996; Suzuki et al., 1998).
The opening of the sand bar provides a unique
opportunity to test the effect of an intermittent disturbance on the structure and resilience of aquatic
communities and ecosystem biodiversity and functioning. Recent studies have been conducted in Imbossica
Lagoon (northern Rio de Janeiro State, Brazil) in order
to understand the influence of such events on different
aquatic communities (Albertoni et al., 1998; Frota &
Caramaschi, 1998; Palma-Silva et al., 2000; Albertoni
et al., 2001; Palma-Silva et al., 2002) and processes
(Faria et al., 1998; Panosso & Esteves, 2000). The
aim of the present study was to investigate the effect
of this disturbance (sand bar opening) on the structure, persistence and resilience of the zooplankton
community. The relationships of the zooplankton to
other biotic and abiotic variables and system resilience
were assessed by means of canonical correspondence
analysis.

Materials and methods

Study area
Imbossica Lagoon is located in the city of Maca
(22 24 S, 41 42 W) in northern Rio de Janeiro State,
Brazil (Fig. 1). It has an area of 3.26 km2 , a maximum depth of 2.0 m and a highly colonized littoral
zone dominated by Typha domingensis and Eleocharis
mutata. The lagoon has been subjected to a series
of anthropogenic impacts, namely sewage disposal,
opening of the sand bar separating the lagoon from the
sea, and reduction of its area by landfills.
Sampling and laboratory analysis
Sampling was carried out from November 7 1996
to May 17 1997 at two sites (Fig. 1), a period encompassing two openings (November 16, 1996 and
January 6, 1997) of the sand bar. At Station 1, near
the sand bar, weekly sampling began 2 weeks before the first opening. While the sand bar remained
open, sampling was conducted, at first, daily and later
weekly. After reconsolidation of the sand bar from
wave action and shore deposition, samples were taken
daily to fortnightly. At Station 2, close to the mouth
of a sewage canal, sampling only began after the first
opening and continued as long as there was water in
that part of the lagoon. Water level fluctuated tidally

while the sand bar was open and with rainfall intensity
when it was consolidated.
In the field, 20 l water samples were obtained
through the entire water column with a diaphragm
electric pump (36900100 ITT Jabsco). The internal
diameter of the hose coupled to the pump was 1.5 cm
and the pumping rate was approximately 10 l per
min. Samples were filtered through a 68-m plankton net and preserved with a 4% buffered sucrose
formaldehyde solution. Sampling with the pump had
previously been compared with vertical net hauls and
a SchindlerPatalas sampler and shown to be the most
efficient for all zooplankton taxa (Kozlowsky-Suzuki
& Bozelli, 1998).
In the laboratory, five 1 ml sub samples of smallbodied zooplanktonic organisms (protozoans, rotifers,
copepod nauplii, and larvae of some meroplanktonic
organisms) were counted in Sedgewick-Rafter cells.
For larger organisms (cladocerans, juvenile and adult
copepods) sub samples of varying volumes, depending on the density of the organisms, were enumerated
in open chambers. In some cases entire samples were
counted.
Temperature was measured at the surface and the
bottom, and water transparency was estimated by
Secchi disc. Vertically integrated samples were obtained from the surface to the bottom of the water
column to estimate bacterial density, chlorophyll-a
content, physico-chemical variables and nutrient concentrations. Bacterial density was estimated using a
flow cytometer (FAC Sort, Becton Dickison) according to the protocol described by del Giorgio et al.
(1996) from samples preserved with 2% buffered and
filtered formaldehyde. Chlorophyll-a content, corrected for phaeophytin, was determined spectrophotometrically after filtration onto GF/C glass filters and
extraction with 80 C ethanol according to Nusch
& Palme (1975). Immediately after collection; pH
and conductivity were measured with a potentiometer,
total alkalinity was determined by sulphuric acid titration (Gran, 1952), salinity was measured with a
salinometer-refractometer and dissolved oxygen (O2 )
was estimated according to the Winkler method modified by Golterman et al. (1978).
In the laboratory, water samples from the entire water column were analyzed for total (TkN) and
dissolved Kjeldahl nitrogen (DkN) by titration after
digestion (Mackereth et al., 1978), nitrate plus nitrite

(NO
3 + NO2 ) by flow injection using the cadmium
reduction method described in Zagatto et al. (1981),
ammonium (NH+
4 ) according to the indophenol color-

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Figure 1. Location of Imboassica Lagoon and sampling Stations 1 and 2, chosen to follow sand bar openings from November 7 1996 to May
17 1997.

imetric method (Koroleff, 1976), total (TP) and total

dissolved phosphorus (TDP) by the molybdenum blue
reaction after acid persulphate oxidation (Golterman
et al.,1978), orthophosphate (PO3
4 ) by the molybdenum blue reaction, and soluble reactive silica (Si)
by the molybdate method (Golterman et al., 1978).
Dissolved organic carbon (DOC) was measured using
a Total Organic Carbon Analyzer (Shimadzu TOC5000).
Data analysis
The number of taxa per sample was defined as the
taxonomic richness, community diversity was measured using Hills index N1 (Ludwig & Reynolds,
1988), and dominance was calculated using index
d of Berger-Parker according to Magurran (1988).
Community persistence was determined by comparing the taxonomic composition (presence or absence)

during the period before the openings occurred and

after each intervention. To measure community resilience, the Spearman rank correlation was used to
compare changes of the abundance of each taxa from
the initial zooplankton community, which existed before the sand bar was open, with the two communities
which were present after each reconsolidation (Ross
et al., 1985). Both community persistence and resilience were measured only at Station 1 where sampling
started before sand bar openings.
Canonical Correspondence Analysis (CCA) was
applied to the all log(x + 1) transformed data to
relate biotic and environmental variables to the zooplankton taxa abundance (Ter Braak, 1986). Nine
variables (pH; salinity, SAL; dissolved oxygen, O2;
dissolved organic carbon, DOC; ammonium, NH4;
soluble reactive silica, Si; total phosphorus, TP; bacterial density, BAC and chlorophyll-a, CHL) and the

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densities of the 42 most common zooplankton taxa
from both sampling stations were used in the analysis.
To assess the significance of the ordination axes, 9999
unrestricted permutations were conducted using the
Monte Carlo test.

Results
Zooplankton composition and diversity
The zooplankton community was composed of 46 taxa
at Station 1 and 33 taxa at Station 2 (Tables 1 and 2).
The rotifers Brachionus rotundiformis and Hexarthra
brandorffi, calanoid and cyclopoid copepod nauplii,
calanoid copepodites, Polychaeta larvae, and Gastropoda veligers were the only taxa occurring at all
salinity values. Total zooplankton density ranged from
3150 to 4830 103 ind. m3 . At Station 1, zooplankton abundance had a negative relation with salinity
(r = 0.71, p < 0.001), whereas a positive relation
(r = 0.73, p < 0.01) was observed at Station 2.
At Station 1, before the sand bar openings, the zooplankton was numerically dominated by the rotifers
Brachionus rotundiformis and Hexarthra brandorffi.
In contrast, Copepoda was the most abundant zooplankton group while Imboassica Lagoon was connected to the sea. As soon as the lagoon was isolated
larvae of meroplanktonic organisms, mostly Gastropoda veligers, became the dominant taxa. At Station
2, Brachionus rotundiformis, Keratella cochlearis and
calanoid nauplii were the most abundant taxa when
the sand bar was open, whereas during closed periods
density maxima of Gastropoda and Bivalvia veligers
and Polychaeta larvae were observed.
Taxonomic richness ranged from 6 to 25 taxa,
while diversity varied from 1.44 to 12.24 taxa and
dominance from 0.23 to 0.93. At Station 1, salinity had
a positive relation with diversity (r = 0.42, p < 0.05),
but no significant relationship with richness (r = 0.16,
p > 0.05) and dominance (r = 0.15, p > 0.05).
Nevertheless, due to high richness and abundance of
copepods, not only the highest diversity (12.24 taxa)
but also highest richness (25 taxa) were recorded when
the lagoon was connected to the sea. At Station 2, the
highest diversity (7.08 taxa) and the lowest dominance
(0.29) were recorded when the sand bar was open.
However, salinity increase was only related with an
increase in the dominance (r = 0.55, p < 0.05), but
no relationship with richness (r = 0.38, p > 0.05)
and diversity (r = 0.43, p > 0.05) was seen. As a

function of very high numbers of Gastropoda veligers,

the lowest diversity and the highest dominance were
obtained soon after the consolidation of the sand bar.
This was observed at both sites.

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Figure 2 CCA ordination diagram with zooplankton taxa (points) and variables (arrows) on the first two axes. Abbreviations of the variables are
given in the text and zooplankton taxa introduced were: Eup=Euplotes sp.; Fav=Favella cf. campanula; Bde=Bdelloidea; Bro=Brachionus rotundiformis; Fte=Filinia terminalis; Hbr=Hexarthra brandorffi; Kco=Keratella cochlearis; Lbu=Lecane bulla; Lgr=L.grandis; Sbi=Synchaeta
bicornis; Ssp=Synchaeta sp.; Tbi=Trichocerca bicristata; Amo=Alona cf. monacantha; Can=calanoid nauplii; Cyn=cyclopoid nauplii;
Han=harpacticoid nauplii; Cac=calanoid copepodites; Cyc=cyclopoid copepodites; Hac=harpacticoid copepodites; Pac=parasitic copepodites;
Ali=Acartia lilljeborgi; Ato=A.tonsa; Pcr=Paracalanus crassirostris; Psp=Paracalanus sp.; Apr=Apocyclops procerus; Mme=Metacyclops
mendocinus; Ohe=Oithona hebes; Oos=O.oswaldocruzi; Cgi=Corycaeus giesbrechti; Ocu=Oncaea cf. curta; Eac=Euterpina acutifrons;
Hal=Halicyclops sp.; Pco=parasitic copepods; Cir=Cirripedia cypris; Cin=Cirripedia nauplii; Biv=Bivalvia veligers; Gav=Gastropoda veligers;
Pol=Polychaeta larvae; Chl=Chaoboridae larvae; Ecl=Echinoderma larvae; Nem=Nematoda; Dec=Decapoda zoea.

Bacterioplankton, chlorophyll-a and abiotic variables

Minimum and maximum values of the abiotic variables, bacterioplankton density and chlorophyll-a content are shown in Table 3. At Station 1, bacterioplankton density and chlorophyll-a content tended to decrease with the entry of marine water, but only the
relationship of salinity and the number of bacteria was
significant (r = 0.57, p < 0.01). At Station 2, no
relationship between those variables and salinity was
detected. While higher chlorophyll-a values were observed in Station 2 than at Station 1 (MannWhitney
test, p < 0.05), no difference in the bacterial numbers
was verified between these sites (MannWhitney test,
p > 0.05).
At Station 1, the increase in salinity was positively
correlated with increase in total alkalinity (r = 0.80,
p < 0.001), electrical conductivity (r = 0.87, p <
0.001), nitrate plus nitrite (r = 0.75, p < 0.001),
dissolved phosphorus (r = 0.42, p < 0.05) and total
phosphorus (r = 0.56, p < 0.01). Soluble reactive
silica (r = 0.59, p < 0.001), dissolved Kjeldahl
nitrogen (r = 0.77, p < 0.001) and dissolved or-

ganic carbon (r = 0.58, p < 0.01) were negatively

correlated with the influx of salt water.
At Station 2, on November 27, the only sampling
accomplished when the sand bar was still open, the
highest ammonium (238.04 M) and total phosphorus
(9.19 M) concentrations were observed. Concomitantly, the lowest pH (6.87) and dissolved oxygen
(2.54 mg l1 ) values were obtained. Lower pH, water transparency and N:P ratio values, and higher
orthophosphate and total phosphorus concentrations
were measured at Station 2 than at Station 1 (Mann
Whitney test, p < 0.05) after the first consolidation.
After the second consolidation of the sand bar, besides lower pH and transparency, in addition to higher
total phosphorus concentrations, higher ammonium
and total Kjeldahl nitrogen concentrations at Station
2 (MannWhitney test, p < 0.05) were seen.
CCA ordination: relation between zooplankton and
other variables
The results of the CCA ordination are summarized in
Figure 2 where the zooplankton taxa are represented

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Figure 3 CCA ordination diagram with samples (1 to 28) obtained at Station 1, as a function of the same variables and taxa mentioned in Fig. 2,
in the first two axes. The arrows represent the temporal sequence observed at this site. Numbers 1 and 2: samples collected before the sand bar
openings; 3 to 10: first open bar period; 11 to 17: first closed bar period; 18 and 19: second open bar period; and 20 to 28: second closed bar
period. C indicates sand bar closed periods; O sand bar open periods.

by points and the variables by arrows. The first two

axes accounted together for 50.7% of the total variance. The first canonical axis and the overall test were
highly significant (Monte Carlo test, p < 0.01). The
first axis of the CCA diagram represents a salinity
gradient, while the second axis is associated with variables indicating the trophic status of the environment.
The first axis was mostly related to Station 1, which
had oligohaline to marine conditions, whereas trophic
status variation was mostly evident at Station 2.
The positive side of the first axis indicates high
salinity conditions, low bacterial numbers and low
dissolved organic carbon, soluble reactive silica, and
chlorophyll-a values. This describes the situation at
Station 1 when the sand bar was open. The zooplankton taxa related to this situation were marine copepod
species, Echinoderma larvae and the rotifer Synchaeta
bicornis. On the other side of the diagram are situations in which the sand bar was closed. Low salinity
values, high bacterial densities, and high dissolved organic carbon, soluble reactive silica and chlorophyll-a
were then verified. The rotifers Hexarthra brandorffi
and Brachionus rotundiformis and the copepod Acartia tonsa (the 3 most frequent and abundant species)
occurred predominantly during these oligohaline conditions. At intermediate salinity levels meroplanktonic
larvae, some copepod species (Apocyclops procerus

and Oithona hebes), and nauplii and copepodites of

calanoid and cyclopoid copepods dominated the community.
The upper part of the diagram (positive side of axis
2) indicates situations of high trophic status (high total
phosphorus, ammonium, and soluble reactive silica
concentrations, and low dissolved oxygen and pH values), while the negative side of axis 2 shows opposite
situations (Fig. 2). Naupliar forms of harpacticoid
copepods, the cyclopoid Metacyclops mendocinus,
and the rotifer Lecane bulla were the species mainly
associated with the low pH and dissolved oxygen values and high nutrient concentrations, which occurred
when the sand bar was open.
Zooplankton persistence and resilience
Eighty-six percent of the taxa present in the predisturbance community was recorded again after the
consolidation of the sand bar; only 2 out of 14 taxa,
accounting for less than 1% of the total zooplankton density, were not observed when the sand bar
reformed. In addition, pre-disturbance species densities were similar on the basis of rank correlation to the
densities observed after the occurrence of the disturbance: before sand bar openings and after the first sand
bar closure, r = 0.55, p < 0.001, before and after
the second sand bar closure, r = 0.66, p < 0.001,

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and after the first and second closures, r = 0.74,
p < 0.001.
CCA ordination: system resilience
The capacity of other environmental variables to return to pre-disturbance conditions is seen in Figure 3,
which shows the distribution of all samples obtained at
Station 1 (as a function of the same taxa and variables
introduced into the CCA) and indicates the resilience
of the system. The arrows in this figure represent the
temporal sequence since before the first sand bar opening until the period following the consolidation of the
sand bar after the second opening. The amount of
time following the closure of the sand bar determined the extent of recovery. After the first opening
(samples 11 to 17 in Fig. 3) the sand bar remained
closed for 30 days. After the second intervention
(samples 20 to 28) sampling was carried out until approximately 4 months after the closure and the most
similar samples to those obtained before the openings
(samples 1 and 2) were those collected from 59 days
after reconsolidation of the sand bar.

Discussion
Zooplankton community structure
One of the main consequences of the sand bar opening is a direct influence from the adjacent marine
environment, contributing to more variability in the
system. During such periods the lagoon presents estuarine characteristics and is subjected to daily physicochemical fluctuations that impose physiological and
behavioral adaptations by aquatic organisms. Salinity
was the main factor related to the structure of thezooplankton community (Fig. 2), a fact that has also been
observed for other coastal systems (Attayde & Bozelli,
1998; Schallenberg & Burns, 2003).
In our study, salinity increase was related to both
an increase (Station 2) and decrease (Station 1) in the
total zooplankton abundance. At Station 2, salinity
increase promoted a bloom of Gastropoda veligers,
while in Station 1 the lagoon fauna was replaced by
a marine one with loss of relatively small individuals
(i.e. rotifers) and entry of large organisms, although
at lower densities (i.e. copepods). Diversity patterns
also differed between sites; there was a tendency
to increase diversity with salinity increase at Station
1, while diversity seemed unaffected and community
dominance prevailed in Station 2. Changes in salinity

have a significant influence on zooplankton diversity

(Attayde & Bozelli, 1998; Schallenberg et al., 2003),
the direction of response depending on the salinity
range the community is exposed to. In the present
study, before the sand bar was open the salinity varied
from 5 to 7 psu and at Station 1 reached 37 psu, while
the maximum value at Station 2 was 19 psu. The contribution of a rich-marine fauna was considerable at
the first site, while restricted at Station 2.
At Station 1, species found during saline intrusion, such as Synchaeta bicornis, have occasionally
been observed in nearby coastal lagoons when subjected to marine influence (Attayde & Bozelli, 1998;
Kozlowsky-Suzuki et al., 1998; Branco et al., 2000),
while Corycaeus giesbrechti, Euterpina acutifrons,
Paracalanus crassirostris, Acartia lilljeborgi, Pseudodiaptomus richardi, Oithona oswaldocruzi are frequent in estuarine systems and/or along the Rio de
Janeiro coastline (Mont & Gloeden, 1986; Lansac
Tha & Lima, 1993; Bonecker, 1995; Dias, 1995).
Although the contribution of meroplanktonic larvae was important soon after the lagoon was isolated
from the sea, in general, Brachionus rotundiformis,
Hexarthra brandorffi and Acartia tonsa were the dominant species when the sand bar reformed. These taxa
tended to dominate in situations with high concentrations of bacterioplankton and phytoplankton (Fig. 2).
We have previously observed, during an enrichment
mesocosm experiment in Imboassica Lagoon, that
both rotifers (B. rotundiformis and H. brandorffi) exerted grazing pressure on both bacterioplankton and
phytoplankton (Kozlowsky-Suzuki & Bozelli, 2002).
Both species belong to genera found worldwide in
coastal lagoons with varying salinity regimes (Dolan
& Gallegos, 1992; Greenwald & Hurlbert, 1993; LamHoai et al., 1997; Attayde & Bozelli, 1998; Branco
et al., 2000). The availability (swimming activity) of
B. rotundiformis may decrease when subjected to abrupt salinity changes, however it increases with time
indicating that, at least part of the population is able to
acclimate (Fielder et al., 2000). Cervetto et al. (1999)
reported minimum (less than 1
) and the maximum
(72
) salinities for which A. tonsa could survive and
demonstrated that this species is able to withstand, for
several days, higher salinities (3538
) than those
found in its natural environment provided the salinity
increase is gradual to allow animals to acclimate.
Changes in the lagoon trophic state represented
the second most important environmental gradient observed in our study (Fig. 2). Metacyclops mendocinus
and the highest rotifer species richness were observed

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in a situation, which suggests an intense mineralization process. This copepod species has been observed
in polluted sites (J. Reid, pers. commun.) and was
the only copepod found in the hypereutrophic Jacarepagu Lagoon in Rio de Janeiro (Ferro-Filho, 1998).
In general, rotifers (as a part of the microzooplankton)
tend to increase in importance in terms of abundance
and/or biomass in high trophic status conditions (Bays
& Crisman, 1983; Beaver & Crisman, 1990).
Bacterioplankton, chlorophyll-a and abiotic variables
The decrease in bacterial numbers and chlorophyll-a
values might have resulted from drainage of lagoon
water exporting particulate and dissolved matter with
later incursion of nutrient-poor marine water (Knoppers & Moreira, 1988; Suzuki et al., 1998). Bacterioplankton reduction may also be related to the
decrease of dissolved organic carbon availability as
seawater entered the lagoon. Whereas, the increase
in nitrate plus nitrite and phosphorus concentrations
during the period of higher marine influence could be
related to sediment resuspension, the advective transport of interstitial water with entry of higher density
marine water or the reintroduction of previously exported lagoon water (Niencheski et al., 1988; Abreu
et al., 1995; Suzuki et al., 1998).
Although chlorophyll-a values tended to be higher
at Station 2 than at Station 1, recorded values were not
as high as expected for a system, which receives continuous nutrient input. Competition from macrophytes
and macroalgae (Charophyte), which densely colonize
this region of Imboassica Lagoon, may have restricted phytoplankton development. Recent observations
indicate that the fast recolonization of a community
of Charophyte following periods of sand bar opening
may not only prevent the development of phytoplankton by decreasing the availability of nutrients in the
water column but also provide substrate and shelter for
the establishment of a diverse community of grazers
(Albertoni et al., 2001; Palma-Silva et al., 2002).
Lower pH, water transparency, and N:P ratio values and higher chlorophyll-a, orthophosphate, total
phosphorus, ammonium, and total nitrogen at Station
2 than at Station 1 suggest a higher trophic status
in that part of Imboassica Lagoon. This condition is
enhanced while the sand bar is open as water level reduction exposes macrophytes and benthic macroalgae
leading to their death (Palma-Silva et al., 2002) and
decomposition. A similar situation was also observed

by Faria et al. (1998) in Imboassica Lagoon during a

period following a sand bar opening.
Zooplankton and system resilience
The species composition of the post-disturbance community was almost identical to that recorded before the
sand bar was open, thus the zooplankton community
was considered persistent. In addition, species densities of the post-disturbance community were highly
correlated to those observed before the occurrence of
the disturbance indicating high community resilience.
Other ecological features of the lagoon (abiotic
and other biotic variables) also returned to the predisturbance state, the amount of time following the
consolidation of the sand bar determining the extent of
recovery. The most similar samples to those obtained
before the openings were those collected from approximately 2 months after the closure. This was also
confirmed by the rank correlation analysis: a higher
correlation was obtained between the pre-disturbance
community and that observed after the second sand bar
closure than the correlation obtained between the predisturbance community and that established after the
first closure. Furthermore, the highest correlation observed between both periods in which the sand bar was
closed, indicates that the community follows the same
trajectory when released from marine influence. Assessing the effect of acidification on several attributes
of zooplankton food webs in Canadian lakes, Locke &
Sprules (1994) observed that planktonic communities
eventually recover to resemble their pre-acidification
condition, given sufficient time without acidic inputs.
Extending the general view of the successional
process and trends observed in ecosystem development (Odum, 1969, 1985) to planktonic communities,
it can be expected that if the disturbance is sufficiently
frequent the community may become dominated by
species capable of surviving after the disturbance, or
by those species, which reach reproductive maturity
quickly (Reynolds, 1993). This principle may apply
to the pre-disturbance community in our study. The
zooplankton community was then mainly constituted
of oligohaline/mesohaline taxa, which tolerated the
changes in salinity, and although such changes may
affect their metabolism (Gaudy et al., 2000), motility
(Fielder et al., 2000) and fecundity (Castro-Longoria,
2003), they were able to survive or there was fast
population re-establishment after the disturbance.
The time required for the zooplankton community
to return to the pre-disturbance condition will depend

175
on the community composition when opening of the
sand bar occurs. Therefore, the zooplankton composition at a particular time is a result of the time interval
during which the lagoon remains closed in conjunction
with climatic conditions, mainly precipitation. The
amount of time the sand bar remains open seems to be
less important for the resilience of the system, since
after the closure marine species are gradually, but relatively soon excluded from the community. When
the lagoon is connected to the sea, marine organisms
will dominate the zooplankton in both diversity and
abundance. In intermediate periods, those in which the
sand bar has been recently closed, or without some
minimum time interval to develop a freshwater community, the zooplankton comprises a reduced number
of taxa, which are able to tolerate abrupt changes in
salinity. In periods when the sand bar remains closed
for a longer period of time, freshwater organisms
comprise the community, which then tends to include
high number of species or taxa. A spatial distribution
study carried out during 2 different periods in Imboassica Lagoon, showed that at low salinity conditions
(0.16 to 1.97 psu) a diverse zooplankton community is
dominated both in richness and abundance by cladocerans, mainly Moina minuta and at higher salinities
(11.67 to 18.25 psu) low diversity is found and the
community characterized by the dominance of copepods and meroplanktonic larvae, reduced number of
rotifers and absence of cladocerans (Branco, unpubl.
data). The first situation was observed when the lagoon
was isolated for approximately one year, whereas the
second scenario was seen 25 days after the consolidation of the sand bar. In our study, the pre-disturbance
community was isolated from the sea for 7 months. We
would, then expect that the time required for the reestablishment of the freshwater community to be much
longer than that required for the transient community
analyzed in the present study.

Conclusions
The opening of the sand bar provided a unique opportunity to assess the effect of a disturbance on
the structure and resilience of the zooplankton community. Salinity was the main factor structuring the
zooplankton community, to which composition and diversity were significantly related. Community persistence and resilience were guaranteed by the prevalence
of species with relatively short life cycles and broad
salinity tolerances. However, the effects of salinity on

behavior, secondary productivity and recruitment of

key taxa in tropical coastal systems are poorly understood and remain to be further investigated. Canonical
correspondence analysis showed to be a useful tool
not only to assess indicator properties of species assemblages along environmental gradients (Attayde &
Bozelli, 1998), but also to evaluate system resilience.
Besides causing physiological responses on aquatic
organisms, salinity changes may also alter their competitive abilities (Sarma et al., 2002), and through
shifts in community composition, the structure (Burns
& Schallenberg, 2001) and functioning (Sterner et al.,
1992) of aquatic food webs. Further studies are thus
needed to assess whether the effects of shifts in community composition in tropical communities resemble
observed trends in temperate systems usually dominated by larger organisms such as Daphnia.

Acknowledgements
We would like to thank S. Melo particularly for
his assistance in fieldwork, S. Jos de Paggi, G-O.
Brandorff, S. Bonecker, C. Dias, J. Reid and F. Joppert for identification and/or confirmation of some
zooplankton species, W. Granli for the use of the flow
cytometer and other facilities of the Limnology Department of Lund University, Sweden, R. Panosso, G.
Fistarol, M. Schallenberg and an anonymous referee
for valuable comments on the manuscript and J. Reid
for correcting the language. Grants were received from
CNPq, Petrobras, and Pronex.

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