Introduction

Predictable seasonal variation in densities of symbiotic dinoflagellates residing in scleractinian corals appears to be a characteristic of reef corals worldwide (Stimson 1997; Brown et al. 1999; Fagoonee et al. 1999; Fitt et al. 2000). Available light and temperature are thought to have a major influence on this variation (Brown et al. 2000; Warner et al. 2002), although the availability of dissolved nutrients in ocean waters may also play a role (Stimson 1997; Fagoonee et al. 1999).

Despite their importance to the economy and health of reef ecosystems (Muller-Parker et al. 1988), few studies have focused on the association between symbiotic dinoflagellates and corals in Brazil, where almost half of the scleractinian species are endemic. Brazilian studies have reported on the utility of zooxanthellae for aiding coral taxonomy (Costa and Amaral 2002) and their possible role in coral bleaching (Costa et al. 2001). Nevertheless, the data obtained in Brazil are still insufficient to allow conclusions to be made on possible seasonal variations in the abundance of zooxanthellae and their photosynthetic pigment concentrations in the tissues of particular coral species.

In this paper, we address this lack of data by documenting seasonal variation in the densities of zooxanthellae and their photosynthetic pigments from three species of corals endemic to Brazil: Mussismilia hartti, M. hispida, and Siderastrea stellata. Of these species, Mussismilia plays an important role in the construction of Brazilian reefs and in some areas, such as in Abrolhos region (Bahia State), it is the main constituent of reef foundations (Leão et al. 1988). Siderastrea is represented in Brazil solely by S. stellata and while it is one of the most conspicuous species, it is not prominent in the formation of Brazilian reefs.

Methods

Using a chisel and a hammer, three replicate fragments (approx. 10 cm in diameter) of Mussismilia hartti, M. hispida, and Siderastrea stellata were removed monthly from the substrate of the coastal reef of Picãozinho (06°42′05′′/7°07′30′′S and 34°48′37′′/34°50′00′′W), Paraíba State, Northeast Brazil, between September 1999 and 2000. The samples were collected from 3 m, transferred to clear plastic bags filled with seawater and transported to the lab in hermetic conditions.

Coral tissue was removed (1 cm2 surface area) using high-pressure filtered seawater (Water Pik and transferred to a clean plastic bag (following Dustan 1979). The extracted tissue was then recorded and mechanically homogenized. For each species, the density of zooxanthellae was determined from four randomly-selected replicates by counting the homogenate in a Fuchs-Rosenthal chamber, using a Zeiss standard microscope. Known volumes of the extract were decanted by centrifugation and the concentrate was used for the photosynthetic pigment measurements after extractions with 90% acetone. Spectrophotometer equations of Parsons and Strickland (1963) were used for the chlorophyll-a and chlorophyll-c analyses. The surface temperature (±0.1°C) and salinity (American Optical refractometer, model 10419) were also recorded monthly in the studied region. Rainfall data for the study period were obtained from local meteorological records.

Data for the density of symbionts and chlorophyll during each month for each species were tested for normality and homogeneity of variances using Levene’s Test, transformed if necessary, and then analyzed using one-factor analyses of variance (ANOVA). Significant differences among mean monthly recordings were separated using Scheffe post hoc tests (P< 0.05). Multiple correlation analyses (Pearson’s Correlation) examined associations between physical data and variation in zooxanthellae.

Results and discussion

Water temperature ranged from 26°C in May, June, and July (rainy months, winter season) to 30°C in January and February 2000 (dry months, summer season). Salinities between 32 ppt in September/2000 and 37 ppt in January and February/2000. The greatest rainfall was recorded between April and June with a maximum value around 500 mm (Fig. 1).

Fig. 1
figure 1

Seasonal variation of rainfall regime (total monthly), water surface temperature, and salinity in the Picãozinho Reefs, João Pessoa (Paraíba State), Brazil.

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Mussismilia hispida had the greatest pigment content and the largest average densities of zooxanthellae, while S. stellata, contained the smallest (Fig. 2).

Fig. 2
figure 2

Mean density (±SD) of symbionts of coral species collected between September 1999 and 2000 from the Picãozinho Reefs, João Pessoa (Paraíba State), Brazil.

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The vertical distribution of S. stellata was comparatively larger than the other species in the studied region. It occurred both in the intertidal zone and in deeper areas; however, colonies were always relatively small. The lower amount of zooxanthellae and photosynthetic pigments in S. stellata would probably limit its development in the area.

All coral species demonstrated distinct monthly patterns in the zooxanthellae parameters. For cell number, Fig. 2 shows no clear trend for S. stellata, and more variable results for the other species. Monthly differences in cell numbers were significant only for M. hispida (P< 0.05). For both chlorophylls (Figs. 3, 4), there appeared to be a peak during the Dec-April dry season, but this is only clear for M. hispida. All species showed significant monthly differences in chlorophyll-a data, but only M. hispida and S. stellata had significant differences for chlorophyll-c (P< 0.05).

Fig. 3
figure 3

Mean monthly concentrations (±SD) of chlorophyll-a (μg cm−2) of the zooxanthellae of coral species collected between September 1999 and 2000 from the Picãozinho Reefs, João Pessoa (Paraíba State), Brazil.

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Fig. 4
figure 4

Mean monthly concentrations (±SD) of chlorophyll-c (μg cm−2) of the zooxanthellae of coral species collected between September 1999 and 2000 from the Picãozinho Reefs, João Pessoa (Paraíba State), Brazil. The data is expressed as monthly means.

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A clear displacement in the times of maximum values was observed when chlorophyll data and cell counts are compared, especially in Mussismilia species. Such asynchrony seems to be uncommon in zooxanthellae data, since previous studies have observed a direct relationship between pigments and cell densities (Stimson 1997; Fitt et al. 2000).

Stronger, and occasionally significant, correlations between various biological measurements and either temperature or salinity were found, but only for M. hispida (Table 1). Similar data from near-equatorial Thailand have previously been published by Brown et al. (1999); the zooxanthellae data corresponding to data from the Pacific published by Stimson (1997) and Fagoonee et al. (1999). Caribbean correlates include Fitt et al. (2000) relating zooxanthellae density changes to changes in host tissue biomass.

Table 1 Multiple correlation analysis of environmental parameters and zooxanthellae data (Cell×106 cm−2 ; μm Chl-a cm−2; μm Chl-c cm−2) of the coral species collected in Picãozinho Reefs, João Pessoa (Paraíba State), Brazil, from September 1999 to September 2000
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