ZOOPLANKTON COMMUNITY OF THE VITÓRIA BAY ESTUARINE SYSTEM ( SOUTHEASTERN BRAZIL ) . CHARACTERIZATION DURING A THREE-YEAR STUDY

In order to characterize the zooplankton community at the Vitória Bay estuarine system (Southeastern Brazil), samples were collected in 10 sampling stations during a three-year study (1998-2000), every three months. A total of 64 taxa were identified. Copepoda contributed with the highest species number (49) in the community, especially with Acartia lilljeborgi, Acartia tonsa, Paracalanus parvus, P. quasimodo, Parvocalanus crassirostris, Temora turbinata, Oithona hebes, Oithona oculata and Euterpina acutifrons. Highest abundances occurred in the summer of 2000. Diversity indexes were higher at the estuary mouth. Zooplankton composition was characterized by coastal and estuarine species, their distribution being influenced mainly by the salinity variation in this estuarine system.


INTRODUCTION
Estuaries are characterized as one of the most dynamic ecosystems, presenting diel and seasonal variations of tides, salinities, temperatures, dissolved oxygen, currents and nutrients (Summerhayes & Thorpe, 1998) which influence species density and diversity (Kramer et al., 1994).Estuarine plankton is required to respond to changes in the physical and chemical characteristics of the environment that impose diel and seasonal patterns, influencing population dynamics.High primary production levels make estuarine zooplankton very abundant, however some other biological factors, as well as environmental parameters, may restrict the variety of the zooplankton species when compared to that of the marine areas (Kennish, 1990).
Estuarine zooplankton is dominated by Copepoda and other less abundant groups such as Chaetognatha, Appendicularia and meroplanktonic larvae (Tundisi, 1970).Many zooplankton species may occur, but generally few dominate the population.These species may vary seasonally and spatially along the estuary, being influenced by freshwater and coastal inputs (Lansac-Tôha & Lima, 1993;Lopes, 1994).
Zooplankton communities have been studied in the Espírito Santo State coastal region and in the Espírito Santo Bay (Bonecker et al., 1987;Bonecker et al., 1991;Dias, 1994), focusing on composition, abundance and distribution, as well as their relation with environmental parameters such as temperature and salinity.The Vitória Bay estuarine system, an adjacent area to the Espírito Santo Bay, has undergone many changes due to anthropogenic actions along the years.It receives daily a great amount of domestic and industrial effluents from the neighboring cities that surround the estuary and also from a port system.Studies on zooplankton ecology in the Vitória Bay estuarine system are scarce, being the work by Loureiro Fernandes et al. (1998), who studied the morphological alterations in the copepod Acartia lilljeborgi, the only known paper.The main purpose of this study is to report zooplankton species composition and abundance in the Vitória Bay.

Study Site
The Vitória Bay estuarine system (around 20º23'S and 40º22'W) is located in the Vitória metropolitan area, Espírito Santo State, Brazil.With a mangrove of 2051 hectares, extending along approximately 25 km, this horseshoe-shaped system has two coastal water entrances, one in the Vitória Bay and the other in the Passage Channel.Local depth varies from 1.5 to 10 m outside the main port channel.Tidal currents enter the estuary by the Vitória Bay as well as by the Passage Channel (Fig. 1).

Sampling
Four sampling stations were selected in the Vitória Bay, determined mainly by their proximity to freshwater inputs, and six stations were selected at the Passage Channel following a salinity gradient that occurs from the mouth of the channel towards the Santa Maria River (Fig. 1).Sampling of the biological material and physical-chemical parameters were made every three months in ten stations from February 1998 to November 2000.
Single zooplankton hauls were taken using a conical-cylindrical plankton net with a 30-cm mouth opening and a 200µm mesh size, fitted with a mechanical flow meter to estimate the amount of water filtered (Omori & Ikeda, 1992).Sub-surface tows were obtained with the boat at approximately 1 knot during a five-minute period.Samples were preserved in aqueous solution of formaldehyde 5%, buffered with sodium tetra-borate.Along with the biological parameters, environmental parameters such as salinity, temperature and dissolved oxygen were measured "in situ" in each sampling station throughout the water column using a portable multi-sound (YSI 85).
For the zooplankton community diversity study, Shannon-Wiener diversity indexes were calculated (Henderson & Seaby, 1997) only for Copepoda because they represent the bulk of the population.
Analysis of variance (ANOVA) was applied to the chemical-physical parameters (temperature, salinity and dissolved oxygen) and to the abundance of the dominant species, in order to test differences among samples (temporal patterns) and sampling stations (spatial patterns).Towards equalizing the variance and normalizing distribution, all data used in the ANOVA were log transformed [log 10 (x+1)].When significant differences were detected by the ANOVA, Tukey´s Honestly Significantly Different (DHS) test was applied to identify sources of variation.
To obtain possible distributional patterns and their relation with the physical-chemical parameters, a Principal Component Analysis (PCA) was performed with data of three year sampling after they were log transformed.Matrices were composed only by species and groups with relative abundance higher than 5%.Analyses were performed using the STATISTICA 6.0 software package.

Environmental Variables
Significant seasonal differences occurred for dissolved oxygen, where winter values were higher than in spring (ANOVA F= 3,65 and p= 0,01).Regarding sampling locations, differences were also observed (ANOVA F= 9,90 and p= 0,00).Highest dissolved oxygen values occurred at the stations near the entrance of the Vitória Bay and Passage Channel, whereas the lowest values occurred in the inner estuary region (Fig. 2).
Salinity values were significantly higher during fall and winter in relation to spring (ANOVA F= 7.68 and p= 0.00).A spatial distribution pattern for salinity was observed in all stations (Fig. 3).The highest values were registered at the stations located in the entrance of the Vitória Bay and Passage Channel, being these significantly higher than the ones located in the inner estuary (ANOVA F= 21.7 and p= 0.00).
Fall temperatures were significantly higher than the ones registered for summer and winter (ANOVA F=9.37 and p= 0.00).Temperature had an inverse pattern in relation to salinity, with values in the inner part of the estuary higher than in the outer region (ANOVA F=2.01 and p= 0.04), although these differences were not significant (Fig. 4).

Zooplankton
During the three-year study a total of 64 taxa was observed, with forty-nine species of Copepoda identified (Table 1).
Average total zooplankton abundances during summer and fall were significantly greater than during winter and spring (ANOVA F=4,83 and p= 0,00).Along the sampling stations, no significant differences were observed (ANOVA F=0,39 and p= 0,93).Figure 5 shows the average, standard deviation and standard error of species and group abundances.
Acartia lilljeborgi was the most abundant species.No significant differences were observed between sampling stations (Table 2).Acartia tonsa was significantly more abundant at station 4, the upper portion of the estuary (Table 2).The same was observed for copepodites of the Pseudodiaptomus genus, occurring mainly at stations in the inner part of the estuary (Table 2).
Appendicularia, Temora turbinata, Euterpina acutifrons, Paracalanus parvus, Paracalanus quasimodo and Parvocalanus crassirostris were significantly more abundant at the lower portion of the estuary.Decapod larvae were significantly more abundant at station 2 (outer region) and station 6 (inner region).The other species and groups did not show significant difference among stations (Table 2).Principal Component Analysis (PCA) allowed the corroboration of the above observed patterns, where copepodites of the Pseudodiaptomus genus were related with temperature, which, despite not being significant, had its greatest values in the inner estuary region.Appendicularia, Temora turbinata, Euterpina acutifrons and Paracalanus parvus were associated with salinity and dissolved oxygen, which had high values in the outer portion of the estuary.A. lilljeborgi revealed no significant correlation with the environmental variables, showing only a positive tendency with the dissolved oxygen and salinity values (Fig. 6).
Zooplankton diversity showed different seasonal and spatial patterns (Fig. 7).The highest values were observed for summer and spring (ANOVA F=3,55 and p= 0,01) at stations located at the Vitória Bay mouth (ANOVA F=4,26 and p= 0,00).The Vitória Bay Estuarine System can be divided into two portions: a lower part characterized by a water mass with high salinity and dissolved oxygen values, influenced mainly by coastal waters; and an upper portion characterized by a water mass with high temperatures, low salinity and dissolved oxygen, influenced by the input of continental waters.
According to Chapman (1992), low dissolved oxygen values in the upper estuary might be related to organic matter decomposition processes, due to the great input of rivers and sewages in the area, as observed by Barroso et al. (1997).Highest salinity values registered in the lower estuarine region evidence a strong influence of the coastal water input at both Vitória Bay and Passage Channel.The upper estuarine region, where freshwater runoff from sewage systems (Barroso et al., 1997) and rivers is evidenced, showed the lowest values as a consequence of the seawater dilution, characterizing a spatial variation.
Winter presented the highest concentrations, typical for the dry period in the region (Bonecker et al., 1991).Although not significant, highest temperature values in the upper estuarine regions occurred because these areas are shallower and more confined, being subjected to greater influence of the air-water interactions in the heating processes and also due to warmer continental water contribution.Lopes et al. (1998) observed a similar pattern at the Paranaguá estuarine complex (Paraná State), presenting higher temperature values and salinity decrease in the upper region of the estuary.

Zooplankton Composition
Zooplankton community was characterized by the presence of freshwater, estuarine, coastal and oceanic species.Acartia lilljeborgi, Acartia tonsa, Oithona hebes, Oithona oculata and Temora turbinata are species commonly found in estuarine and coastal waters (Lopes et al., 1998).The coastal region is highly influenced by the continent, being inhabited by species that are well adapted to great salinity variations, freshwater and runoff (Bradford-Grieve et al., 1999).The presence of oceanic species was well characterized by the occurrence of Calocalanus pavoninus, Clausocalanus furcatus, Subeucalanus subtenuis and Corycaeus giesbrechti as well as by chaetognaths such as Sagitta enflata.Typical freshwater species such as Thermocyclops minutus, Paracyclops fimbriatus, Halocyclops sp, Microcyclops anceps and Cletocamptus deitersi were also observed in the inner portion of the estuary.
The genus Bestiolina has been recorded in the Pacific by Lenz et al. (2000) at the Kaneohe Bay, Oahu, Hawaii; by McKinnon & Duggan (2001) at the Exmouth Gulf, Australia; and by Lo et al. (2004) at Tapong Bay, Taiwan.The presence of Bestiolina sp in the Vitória Bay estuary is the first record for Brazilian waters.
Zooplankton composition in the Vitória Bay/Passage Channel estuarine system is similar to that of other Brazilian estuaries, where holoplanktonic organisms dominate.However, copepods showed higher species richness, with the occurrence of 49 species along the three-year study, higher than the numbers found in other estuaries (Paranaguá & Nascimento-Vieira, 1984;Lira et al., 1996;Bonecker et al., 1991).The only work that found numbers similar to those of this study was performed in the Una do Prelado river estuary in the São Paulo State (Lansac Tôha & Lima, 1993) with a total of 48 species of Copepoda.Nevertheless, a large part of these species was of benthic freshwater copepods associated with the marginal vegetation of the rivers that carried water to the estuary during the rainy period.Also, the authors used a net of smaller mesh size for their sampling.In estuaries of other countries, such as in the Caribbean region, Youngbluth (1976) found 31 species.

Space-time Distribution
Acartia lilljeborgi can be considered as a marine-estuarine species since it was found along the entire estuary, not presenting a significant correlation with salinity.Acartia lilljeborgi is usually the dominant species in most Brazilian estuaries (Lopes et al., 1986;Lopes, 1994;Lira et al., 1996;Bonecker et al., 1991), mainly in intermediate and lower regions.Acartia tonsa is also another species developing well in intermediate (Lopes et al., 1998) and high salinities (Montú, 1980), being also dominant in estuaries, particularly in the Chesapeake Bay (Kennish, 1994).The concurrently occurrence of both Acartia species is an interesting fact.Although they compete for the same food resource (Kennish, 1986), they seem to coexist in the environment, with Acartia tonsa being more abundant in the upper portion of the estuary.The relative confinement of Acartia tonsa in the upper region may not only reflect preference for some hydrographical conditions, but also interspecific competition among the two species (Kennish, 1986).
Temora turbinata, Paracalanus parvus, P. quasimodo, Parvocalanus crassirostris, as well as Appendicularia, have a marine-euryhaline behavior because they occur preferably in areas with elevated salinities (Lopes et al., 1998).The positive correlation with salinity indicates that these organisms are dependent on the recruitment from the adjacent coastal region.
Zooplankton of the Vitória Bay system was composed mainly by holoplanktonic organisms, with Copepoda as the most abundant group, and a high number of species.Among them, the most abundant were: A. lilljeborgi, A. tonsa, P. parvus, P quasimodo, P. crassirostris, T. turbinata, O. hebes, O. oculata and E. acutifrons.Zooplankton community showed seasonal variations, in general with greater abundances occurring during summer, the greatest diversity values being observed at stations with higher salinity.Since the majority of the species are from coastal areas, spatial distribution of the abundance is controlled by the salinity gradient as observed by Lopes (1996) and Villate et al. (1993).However, other factors must be considered to a better evaluation of the distribution and abundance of zooplankton.To obtain a better answer, future studies should take into consideration nutrient concentrations and chlorophylla, since the environment receives influence from anthropogenic sources along its extension.

Fig. 2 .
Fig. 2. Average, standard error and standard deviation (n=120) of the dissolved oxygen values for the different seasons and sampling stations.

Fig. 3 .
Fig. 3. Average, standard error and standard deviation (n=120) of the salinity values for the different seasons and sampling stations.

Fig. 4 .
Fig. 4. Average, standard error and standard deviation (n=120) of the temperature values for the different seasons and sampling stations.

Fig. 5 .
Fig. 5. Average, standard error and standard deviation (n=120) of the total zooplankton abundance values for the different seasons and sampling stations.Mean ±SE ±SD Summer Fall Winter Spring

Table 1 .
Inventory of the zooplankton in the Vitória Bay/Passage Channel estuarine system (Southeastern Brazil).

Table 2 .
Analysis of Variance (ANOVA) of the most abundant species and groups along the sampling stations (n=120).