Natural variations in the zooxanthellae of temperate symbiotic Anthozoa
Few previous studies of zooxanthellae have considered temperate Anthozoan symbioses. The present study investigates how the characteristics of zooxanthellae symbiotic with temperate Anthozoa vary in response to natural variations in environmental parameters. Variations in the number (density), division rate, size and ultrastructure of zooxanthellae from the temperate anemones Anemonia viridis (Forskal) and Anthopleura ballii (Cocks) were examined in response to season, water depth and artificial irradiance (A. viridis in aquaria). In addition, variations in chlorophyll concentrations were considered in intertidal and laboratorymaintained A. viridis. Zooxanthellae from both intertidal and shallow subtidal A. viridis showed variations which correlated with seasonal variations in environmental parameters. Zooxanthella density in intertidal A. viridis showed an inverse relationship with temperature, daylength and sunshine. Higher zooxanthella density was observed in A. viridis from a shallow, subtidal habitat during February 1998 (2.06 ± 0.11 x 108 cells g"' wet weight) than during July 1998 (1.01 ± 0.09 x 108 cells g'' wet weight; T= 7.67, p< 0.001). Stereological analysis of transmission electron micrographs showed that zooxanthellae in intertidal A. viridis had significantly higher chloroplast volume fraction during February (32.1 ± 1.5 %) than July (21.8 ± 2.1 %; T= 4.07, p<0.05). The proportion of chlorophyll a per zooxanthella was significantly higher in December than all other months except January (ANOVA, F= 5.62 p<0.05). The zooxanthellae of A. viridis may thus photoadapt to low winter irradiances by increasing zooxanthellae density, chloroplast volume and the proportion of chlorophyll a per cell. By contrast, zooxanthellae from A. viridis maintained in artificial irradiances in the laboratory of 4 µmol m=2 s' and 20 pmol m2 s' showed no variation in density or ultrastructure, due either to the low irradiances used or a lack of variation in other physical parameters compared to the field. A. ballii zooxanthella density responded to both depth and season and was lower at 6m during summer than at 6m during winter and at 18 m during both summer and winter. Chloroplast volume fractions in A. ballii was not affected by depth during winter, nor by season at 18 in. Starch and lipid stores in zooxanthellae from both A. viridis and A. ballii responded to seasonal fluctuations. Lipid was present in zooxanthellae during summer (intertidal A. viridis, volume fraction 19.8 ± 3.4 %) and absent during winter, and starch volume was significantly higher from zooxanthellae in A. ballii at 6 in in winter (14.3 ± 4.2 %) than 18 min winter (4.7 ± 1.6 %) or summer (4.7 ± 1.1 %; ANOVA, F= 6.04 p< 0.05). It is concluded that the zooxanthellae of the temperate anemones A. viridis and A. ballfi show variations in zooxanthellae characteristics which correspond to variations in dayto-day weather, season and water depth.