Prolonged exposure to elevated CO(2) promotes growth of the algal symbiont Symbiodinium muscatinei in the intertidal sea anemone Anthopleura elegantissima

Abstract

Some photosynthetic organisms benefit from elevated levels of carbon dioxide, but studies on the effects of elevated PCO(2) on the algal symbionts of animals are very few. This study investigated the impact of hypercapnia on a photosynthetic symbiosis between the anemone Anthopleura elegantissima and its zooxanthella Symbiodinium muscatinei. Anemones were maintained in the laboratory for 1 week at 37 Pa PCO(2) and pH 8.1. Clonal pairs were then divided into two groups and maintained for 6 weeks under conditions naturally experienced in their intertidal environment, 45 Pa PCO(2), pH 8.1 and 231 Pa PCO(2), pH 7.3. Respiration and photosynthesis were measured after the 1-week acclimation period and after 6 weeks in experimental conditions. Density of zooxanthellal cells, zooxanthellal cell size, mitotic index and chlorophyll content were compared between non-clonemate anemones after the 1-week acclimation period and clonal anemones at the end of the experiment. Anemones thrived in hypercapnia. After 6 weeks, A. elegantissima exhibited higher rates of photosynthesis at 45 Pa (4.2 µmol O(2) g(-1) h(-1)) and 231 Pa (3.30 µmol O(2) g(-1) h(-1)) than at the initial 37 Pa (1.53 µmol O(2) g(-1) h(-1)). Likewise, anemones at 231 Pa received more of their respiratory carbon from zooxanthellae (CZAR = 78.2%) than those at 37 Pa (CZAR = 66.6%) but less than anemones at 45 Pa (CZAR = 137.3%). The mitotic index of zooxanthellae was significantly greater in the hypercapnic anemones than in anemones at lower PCO(2). Excess zooxanthellae were expelled by their hosts, and cell densities, cell diameters and chlorophyll contents were not significantly different between the groups. The response of A. elegantissima to hypercapnic acidification reveals the potential adaptation of an intertidal, photosynthetic symbiosis for high PCO(2).

Keywords: Anthopleura elegantissima; CZAR; Carbon dioxide; Intertidal; Metabolic rate; Ocean acidification; Photosynthesis; Zooxanthellae.

Fig. 1.. Mean mass-specific rates of gross photosynthesis (A), respiration (B) and net photosynthesis (C) in Anthopleura elegantissima following incubations of one week at PCO₂ of 37 Pa and six weeks at PCO₂ of 45 and 231 Pa.

Net photosynthesis was calculated on a 14:24 light:dark basis. Bars of the same color represent the same individuals, while different colors represent genetically identical clones. Error bars represent one standard error; n = 11 for all experiments. Letters designate statistically significant differences between individuals at two different PCO₂ (a = p<0.001, b = p<0.01, c = p<0.05) using paired t-tests, while asterisks represents significant differences (* = p<0.05; ** = p<0.01) between clonemates at two different PCO₂.

Fig. 2.. Ratios of photosynthesis to respiration (A) and potential contributions of carbon by zooxanthellae to the animal's respiratory carbon requirements (CZAR) (B) in Anthopleura elegantissima following incubations of one week at PCO₂ of 37 Pa and six weeks at PCO₂of 45 and 231 Pa.

Bars of the same color represent the same individuals, while different colors represent genetically identical clones. Error bars represent ± one standard error; n = 11 for all experiments. Letters designate statistically significant differences between individuals at two different PCO₂ (a = p<0.001) using paired t-tests, while asterisks represent significant differences (** = p<0.01) between clonemates at two different PCO₂.

Fig. 3.. Characteristics of the zooxanthella, Symbiodinium muscatinei, in Anthopleura elegantissima following incubations of one week at PCO₂ of 37 Pa and six weeks at PCO₂ of 45 and 231 Pa.

(A) Cell diameter. (B) Cell density. (C) Mitotic index. (D) Chlorophyll a concentration. Bars of the same color represent zooxanthellae from the same individuals, while different color bars represent those from genetically identical clones. Grey bars represent those from different individuals collected at the same time from the same population of anemones. Error bars represent ± one standard error; n = 11 for all measurements. Letters designate statistically significant differences using ANOVA of arcsine-transformed data (not shown) followed by Fisher's LSD post-hoc analyses between individuals (a = p<0.001, b and c = p<0.05).