Spatial and temporal distribution of fish eggs and larvae in a subtropical coastal lagoon , Santa Catarina State , Brazil

This study investigated the variation in abundance, distribution and composition of ichthyoplankton in a lagoon in southern Brazil through the year and at different stations within the lagoon. Ibiraquera Lagoon is a shallow coastal lagoon connected to the sea by a semi-permanent sandbar. Ichthyoplankton samples were collected monthly from December 2003 to December 2004, with a 200 μm mesh net using horizontal surface hauls. A colder, drier period was detected, contrasting with warm months during which salinity varied depending on rainfall and whether the sandbar was open or closed. The mean abundance of ichthyoplankton over the study period was 459.6 ± 76.2 (SE) eggs · 100 m-3 and 63.6 ± 7.9 (SE) larvae · 100 m-3, and they were present during all months. Significantly higher abundances of eggs and larvae were observed during warm months. The community was dominated by the family Engraulidae followed by Clupeidae, Gobiidae and Mugilidae. Engraulidae and Clupeidae were present throughout the year, with greater abundances in months with higher temperatures. Some coastal fish species spawn in Ibiraquera Lagoon, mainly near to the sandbar, demonstrating that the lagoon is a spawning area for coastal stock. We recommend the establishment of environmental procedures to promote the conservation of Ibiraquera Lagoon and its ichthyoplankton community.


Introduction
Temporal and spatial variations of fish abundances in estuaries can be the result of changes in physical conditions that influence species' seasonal movements (Vieira, 1991;Barletta et al., 2003;Spach et al., 2003).Indeed, studies of ichthyoplankton carried out in Brazil have shown that fish larvae abundance, distribution and composition may have temporal and spatial patterns that are caused by physical factors such as rainfall and salinity (Barletta-Bergan et al., 2002a, 2002b) and temperature (Muelbert & Weiss, 1991;Castro et al., 2005).
Life cycles of many commercial species are related to estuaries (Castro & Bonecker, 1996;Esper et al., 2001;Franco & Muelbert, 2003;Freitas & Muelbert, 2004).The southern Brazilian continental shelf is one of the most productive fishing areas of Brazil's 8,500 km coast.In Santa Catarina State, artisanal mullet fishing is an important economic and cultural activity among local communities of fishermen living in estuarine areas (Peterson et al., 2008).In the same way, mullet, pink shrimp and blue crab are the most important artisanal fishery resource in Ibiraquera Lagoon (Seixas & Berkes, 2003;Bonetti et al., 2005).Despite its natural characteristics and tourist importance, Ibiraquera Lagoon has been poorly studied, therefore there are no specific biological data to subsidize management plans for the area (Bonetti et al., 2005).
This aim of this study is to test the hypothesis that the variability in abundance and composition of fish eggs and larvae is homogeneous throughout the year and in a spatial gradient in the lagoon.Our findings were also reported at the Local Agenda 21 Forum to help improve the management initiatives in the area.

Study area
The Ibiraquera Lagoon is located on the southern Brazilian coast between 28°06'1' ' and 28°10'1'' S and between 48°37'44'' and 48°41'53'' W (Fig. 1).It is about 9 km long with a total area of 8,700 km 2 , and the local depth ranges from 0.2 m to 2.0 m with a sandy bottom (Seixas & Berkes, 2003).According to Kjerfve (1994) it is a "shallow shocked" lagoon, with a high surface/volume ratio and restricted water exchange with the adjacent ocean.It is geomorphologically segmented into four sectors known locally as lagoa de Cima, lagoa do Meio, lagoa de Baixo and Lagoa do Saco (Bonetti et al., 2005).These four sectors are interconnected by small channels and the largest of them (Cima) has an area of 4,000 km 2 .Baixo and Saco are the sectors closest to the adjacent coastal region, and they are separated from the sea by a semi-permanent sandbar that is 150 m wide.
When the sandbar is closed long enough to rise the water level due to freshwater inputs and rainfall events, water pressure opens the sandbar naturally (Seixas & Berkes, 2003).Nowadays, the sandbar is also opened artificially twice a year and the time of opening is dependent on the influence of local political groups.This opening causes significant changes in all areas of the Ibiraquera Lagoon, with increased salinity, even in the innermost sector (Bonetti et al., 2005).In this study, the four sectors of Ibiraquera Lagoon will be referred to as Cima, Meio, Baixo and Saco, or simply as the stations.
Freshwater input is restricted to small streams at Baixo and Saco, and conditioned mainly by rainfall.The input of salty water and the reduction of the water level during the opening of the sandbar, associated with the local wind, improve the water mixture and therefore the nutrients and oxygen distribution in the Lagoon (Bonetti et al., 2005).The area is under the intermediary subtropical zone (humid mesothermic group).

Sampling methods
Monthly ichthyoplankton samples were collected from December 2003 to December 2004, except for May and September 2004.The sandbar was opened from December 2003 to February 2004 and from June to August 2004.Three replicates were taken at each station (Cima, Meio, Baixo and Saco), with the exception of the January and February 2004 samples at Saco, and the June and July 2004 samples at Cima, due to shallow depth, comprising a total of 124 samples.Samples were collected with a 200 µm mesh net equipped with a General Oceanics flowmeter, during surface horizontal hauls lasting 5 minutes each.
Water temperature was measured using a thermometer (precise to 0.5 ºC) and salinity (in 0.5 increments) was measured with a refractometer at the surface, at the same time as the plankton was sampled.For months without ichthyoplankton samples, temperature and salinity were obtained from the team conducting the main project in the area.Data on local rainfall were obtained from EPAGRI (Empresa de Pesquisa Agropecuária e Extensão Rural de Santa Catarina S.A) station, located in Urussanga (28º31'S 49º19'W), Santa Catarina State.

Data analysis
Dominance and frequency of occurrence were determined in order to identify the most important fish larvae families in the Ibiraquera Lagoon.Dominance was calculated for each family using the mean abundance of the family in relation to the total mean larvae abundance.The frequency of occurrence was calculated from the number of samples in which each family was caught as a proportion of the total number of samples.
Two-way ANOVA was used to determine whether there were any significant differences in temperature, salinity or ichthyoplankton density for different months and stations.Missing data were estimated from the mean of other replicates.Ichthyoplankton data were log(x+1) transformed.The Bartlett test was applied in order to verify the homogeneity of variances before each analysis and Tukey's multiple comparison test was used whenever significant differences were detected (Zar, 1996).The tests were performed on Statistica © 5.0 (Statsoft Inc., 1984-1995).Graphs were plotted to illustrate the ANOVA interactions for families with high dominance and/or with commercial value.
Cluster analysis was conducted to evaluate similarities between samples in terms of the distribution of families.Samples were clustered using the ranked Bray Curtis index according to mean fish larvae densities at each station (n = 42).Hierarchical group-average linking was carried out using PRIMER © 5.1 routines (PRIMER-E).All data were log (x+1) transformed.

Hydrographic conditions
The water temperature characterized two periods during the year (Fig. 2a): warm months, with mean temperatures greater than 25 °C (January, February, March, November, and December 2004), and cold months with mean temperatures below 20 °C (June and July 2004).The interaction between months and stations can be explained by the significantly higher (p < 0.01) mean temperature at Saco in October, November and December 2004, and at Cima in June and July 2004.
When the sandbar was opened in December 2003, the salinity increased at all stations until March (Fig. 2b).After September 2004, when the bar was closed, the salinity decreased as the months passed.The results observed between April and August 2004 can be explained with reference to the ANOVA interactions.In April, July and August 2004 the salinity was significantly higher (p < 0.01) at Baixo, while in May and June the salinity was significantly higher at Saco.
The variation of rainfall, during the study period, characterized months with rainfall above 200 mm (December 2003, May and September 2004), and months with rainfall less than 100 mm (February, June, July, August, and October 2004) (Fig. 2c).
Analysis of the hydrographic conditions characterized a cold and dry period (June to August 2004), with high salinity at stations near the sandbar.During the warm months, salinity varied depending on rainfall and whether the sandbar was open or closed.

Ichthyoplankton distribution
During the entire study a total of 3,741 fish larvae were identified, while 25,702 eggs were sorted from the samples.Mean ichthyoplankton abundances in the Ibiraquera Lagoon were 459.6 ± 76.2 (SE) eggs • 100 m -3 and 63.6 ± 7.9 (SE) larvae • 100 m -3 .The highest mean egg abundance (5,784.1 eggs • 100 m -3 ) was obtained in January and the highest mean larval abundance (512.9 larvae • 100 m -3 ), in November 2004 (Fig. 3).These values were obtained respectively at Cima and Meio Lagoon.High mean abundances of fish eggs were observed during all months, especially December 2003 and January 2004.The lowest mean abundance of eggs was during June 2004.Fish larvae were also observed every month, with lower mean abundance between June and August 2004 (Fig. 3).
The ANOVA showed the interaction between months and stations in relation to the distribution of eggs (Table 1).The mean abundance of eggs in Meio, Baixo and Saco followed the general pattern seen in Fig. 3.The ANOVA's interaction was explained by the reverse pattern of Cima, with significantly lower (p < 0.01) mean abundances in April, July, November and December 2004.

Composition of fish larvae
Engraulid larvae had the highest mean abundance, dominance and frequency of occurrence (Table 2 and Fig. 4).The second most abundant family was Clupeidae followed by Gobiidae, Mugilidae and Sciaenidae.Other families, such as Syngnathidae, Atherinopsidae and Achiridae had frequencies of occurrence greater than 10%, although with low abundance and dominance.Only engraulid, clupeid and syngnathid larvae were found in samples taken during all months of the year.
The dominance of the main families in the ichthyoplankton community changed over different months (Fig. 5).The Engraulidae family was dominant in December 2003 and August 2004 and shared dominance with Gobiidae in January 2004 and with Clupeidae in June 2004.Clupeid larvae were   Clupeid larvae were present every month and at significantly higher abundances in December 2004 and at Baixo.The abundance of blenniid larvae was also significantly higher (p < 0.01) in December 2004, while syngnathid larvae had a significantly higher (p < 0.05) abundance at Saco (Table 2).
The ANOVA results demonstrated a significantly higher (p < 0.01) abundance of engraulid larvae at Saco from December 2003 to February 2004, and at Meio during the cold and dry period.There was also a significantly higher abundance at Baixo during March and April 2004 (Fig. 6a).There were significantly higher abundances of mugilid larvae during October and November 2004 at Saco, and in December 2003 and March 2004 at Meio (Fig. 6b).In December 2003, gobiid larvae were significantly more abundant distributed at Saco and Meio, while their abundance was significantly higher at Baixo and Cima during March 2004.In February 2004, sciaenid and achirid larvae were significantly more abundant at Meio.Moreover, in March 2004 haemulid larvae had significantly higher (p < 0.01) abundance at Baixo.
The cluster analysis identified two groups (Fig. 7) distinguished by hydrographic conditions and seasonal +  abundance of fish larvae.In both groups, engraulid and clupeid larvae were the most abundant.Group A was characterized by the cold and dry season, with low larvae abundance (mean of 8.21 larvae • 100 m -3 ), and syngnathid, atherinopsid, sciaenid, gobiid and blenniid larvae were also registered.The warm months were clustered in group B, where high larvae abundances were obtained (mean of 71.44 larvae • 100 m -3 ), with gobiid and mugilid larvae also being abundant.

Discussion
Salinity is strongly influenced by rainfall and dynamics of the sand bar, and characterizes Ibiraquera Laggon as a mixohaline laggon (Bonetti et al., 2005).Temperature variation follows the pattern found in subtropical latitudes (Muelbert & Weiss, 1991;Lüchmann et al., 2008), and the rainfall pattern is similar to that recorded at Conceição Lagoon (Lüchmann et al., 2008).Freshwater input was mainly influenced by rainfall, since Ibiraquera Lagoon has few small freshwater sources (Bonetti et al., 2005).
Mean eggs abundance ranges in Ibiraquera Lagoon were comparable with coastal areas from Bahia to Santa Catarina State (Franco & Muelbert, 2003;Freitas & Muelbert, 2004;Mafalda Jr. et al., 2004) and the rio de la Plata estuary (Berasategui et al., 2004).The mean abundance of fish larvae was higher than along the adjacent coast (Franco & Muelbert, 2003;Freitas & Muelbert, 2004) and than in the rio de la Plata estuary (Berasategui et al., 2004), but was lower than the channel area of laguna dos Patos (Muelbert & Weiss, 1991).Due to the small dimensions of Ibiraquera lagoon in relation to the systems cited above and its abundance of ichthyoplankton, we can consider it a spawning and nursery area.
Like in other estuarine systems (Muelbert & Weiss, 1991;Sánchez-Velasco et al., 1996;Tovar-Faro & Bonecker, 2000;Barletta-Bergan et al., 2002a;Joyeux et al., 2004;Castro et al., 2005) the community was dominated by engraulids and clupeids.Gobiid larvae, the third most abundant family in Ibiraquera Lagoon, were also important in the ichthyoplankton community in the southern Gulf of Mexico (Sánchez-Velasco et al., 1996) and in Vitória Bay (Joyeux et al., 2004).In the channel area of laguna dos Patos, Caeté estuary and Guanabara Bay, ichthyoplankton communities were also dominated by Sciaenidae (Muelbert & Weiss, 1991;Barletta-Bergan et al., 2002a;Barletta-Bergan et al., 2002b;Castro et al., 2005), which was the fifth most abundant family in the present study.All those examples corroborated the fact that these families use inner coastal systems during their life cycle, despite of its dimension and water exchange mechanism with the sea.
In coastal areas, down to 100 m depth, engraulid and clupeid larvae make up 60% of the total catch (Katsuragawa et al., 2006).These families are known to be estuarine residents, estuarine dependents or marine visitors (Garcia & Vieira, 2001) and can be found in the lagoon due to the dynamics of the sandbar.Engraulidae and Clupeidae exhibited higher abundance in the months when the sandbar was closed.Since their life cycle is short, up to 45 days for Sardinella brasiliensis reared in the laboratory (Silva et al., 2003;Katsuragawa et al., 2006), they could be breeding and spawning in the lagoon.
In the present study, Mugilidae abundance was higher than in the channel area of laguna dos Patos, Vitória Bay and Guanabara Bay (Muelbert & Weiss, 1991;Joyeux et al., 2004;Castro et al., 2005).Mugilids occur along the whole south Brazilian coast, Mugil curema and Mugil platanus being dominant in the southern lagoons (Figueiredo & Menezes, 1985;Garcia & Vieira, 2001;Ferreira & Freire, pers. comm.).Spawning migrations of mugilids usually refer to the movement of ripe fish from their feeding areas (generally estuaries) to the open sea (Ibáñez & Benítez, 2004).Nevertheless, mugilid larvae enter the estuary to complete their development and they are considered estuarine dependent (Figueiredo & Menezes, 1985;Garcia & Vieira, 2001).Early mugilid larvae, produced from recent spawn in the coast, could enter the lagoon during the months when the sandbar is open.On the other hand, larval mugilid stages reared in the laboratory completed their development between 29 and 89 days, depending on species (Kuo et al., 1973;Boglione et al., 1992;Yoshimatsu et al., 1992;Ismail et al., 1998;Monteiro-Ribas & Bonecker, 2001).Therefore, abundance of early mugilid larvae in the lagoon after 3 and 4 months without the bar being open, could only be explained by spawning inside the lagoon.
In Ibiraquera Lagoon, warm months had higher egg abundances, in common with the northeast coast of Brazil (Mafalda et al., 2004).The highest egg abundances were found at the stations with the highest abundance of brachyuran zoeae (Freire, pers.comm.).According to Freitas & Muelbert (2004) a partial overlap between zooplankton and fish egg distribution suggests a synchrony between spawning and the availability of food for the future larvae.
Abundance and richness of fish larvae were also higher in warm months in Ibiraquera lagoon, which is comparable with the channel area of laguna dos Patos (Muelbert & Weiss, 1991), Guanabara Bay (Tovar-Faro & Bonecker, 2000;Castro et al., 2005), the Magdalena-Almejas Bay lagoon system (Avendaño- Ibarra et al., 2004) and Lima estuary (Ramos et al., 2006).In those estuaries, temperature increases are a controlling factor for spawning and recruitment periods (Phonlor, 1984), determining temporal patterns of ichthyoplankton composition, distribution and abundance.In contrast with this pattern, in estuaries located in lower latitudes (Sánchez-Velasco et al., 1996;Barletta-Bergan et al., 2002a, 2002b), it is salinity and freshwater inputs that induce increases in fish larvae abundance (Barletta-Bergan et al., 2002b).Fluvial discharges related to the rainfall increase, nutrient concentration and plankton biomass increase, results in the spawning of many fishes during this period (Sánchez-Velasco et al., 1996).
The most dominant families, Engraulidae and Clupeidae, were present throughout the year (Muelbert & Weiss, 1991), mainly in the warm months (Fig. 5).Clupeids can spawn all year round, mostly in the late spring and summer, as recorded for Sardinella brasiliensis which mainly spawn in December 2003 and January 2004 along the south-eastern coast (Magro et al., 2000;Katsuragawa et al., 2006).In Guanabara Bay, Clupeidae dominance was also associated with the warm and rainy months, while Engraulidae were present during the greater part of the sampling period (Tovar-Faro & Bonecker, 2000).Gobiidae larvae were also present in Ibiraquera Lagoon most of the year, and peaked during months when rainfall increased.The same pattern was detected in the southern Gulf of Mexico (Sánchez-Velasco et al., 1996), where gobiid species spawn in the rainy period, and the opposite was observed in the channel area of laguna dos Patos (Muelbert & Weiss, 1991), where gobiid larvae were only present during early spring and late summer.
The spatial distribution of fish larvae demonstrates that they were well distributed across all stations.In Patos Lagoon, the densities of larvae from the Engraulidae, Clupeidae, Sciaenidae, Gobiidae and other families found in the Ibiraquera Lagoon were uniformly distributed throughout the channel area (Muelbert & Weiss, 1991).Similarly, in Vitória Bay, spatial variation in ichthyoplankton assemblage was not very pronounced, because some species occupy all places at all times (Chagas et al., 2006).However, Saco and Baixo exhibited a high abundance of some important fisheries and ecological groups.Generally, an area has been called a nursery if a juvenile fish or invertebrate species occurs at higher abundances, avoids predation more successfully, or grows faster there than in a different habitat (Beck et al., 2001).Since Saco and Baixo are the closest stations to the sea and have the highest salinity, the larvae of coastal and estuarine dependent fish could be arriving from the sea while the sandbar is open.
Ichthyoplankton distribution and composition were strongly influenced by environmental conditions, mainly the temperature pattern, which is to be expected at subtropical latitudes (Muelbert & Weiss, 1991;Barletta-Bergan et al., 2002b).Some families, such as Engraulidae, occurred throughout the year with variations in abundance.However, important fish such as mugilids peaked in October 2004, due to their reproductive period (Esper et al., 2001).The fact that economically and ecologically important families like Engraulidae, Clupeidae and Mugilidae spawn in the lagoon emphasizes the importance of the Ibiraquera Lagoon as a nursery area for coastal fish.The depletion of coastal stocks is not only being caused by over fishing, but also by destruction of nurseries areas (Palumbi, 2001;Watson & Pauly, 2001;Myers & Worm, 2003;Palumbi, 2003).High numbers of ichthyoplankton were registered during months of increased tourist activity (late spring and summer) in Ibiraquera Lagoon.Therefore, we strongly recommend environmental procedures, as preservation of the lagoon vegetation and maintenance of the water quality, during these periods, especially in the area near the sandbar.Further studies should be conducted to understand the circulation of water throughout the lagoon and to investigate the ichthyoplankton community in the adjacent coastal area.

Fig. 1 .
Fig. 1.The location of Ibiraquera Lagoon on the southern Brazilian coast with its four stations in detail (Saco, Baixo, Meio and Cima).

Table 1 .
Results and significance level (** p < 0.01) for twoway ANOVA performed to test the hypotheses that fish egg abundances differed significantly in response to month and station.d.f.: degrees of freedom.Residual d.f.89.November and December 2004, while the larvae of Gobiidae dominated in March and July 2004.In February 2004, Sciaenidae was the dominant family, while in October 2004 Mugilidae was dominant.

Fig. 7 .
Fig. 7. Cluster dendrogram based on similarities of the samples collected in Ibiraquera Lagoon from December 2003 to December 2004.Samples were clustered by Bray Curtis similarity based on log (x+1) transformed abundances of 12 families.

Table 2 .
Mean abundances of fish larvae (larvae • 100 m -3 ), results and significance level (* p < 0.05, ** p < 0.01) for two-way ANOVA performed to test whether mean abundances of fish larvae differed significantly between different months and stations.For families where ANOVA detected no significant (ns) interaction the Tukey results are given.Letters indicate significantly different means from Tukey test.d.f.: degrees of freedom.Residual d.f.89.