Distribution patterns and nutritional contributions of algal symbionts in the sea anemone Anthopleura xanthogrammica

Abstract

The Pacific intertidal sea anemone Anthopleura xanthogrammica hosts 2 algal symbionts, zoochlorellae Elliptochloris marina and zooxanthellae Symbiodinium muscatinei, either alone or co-occurring. Previous studies have suggested that zoochlorellae and zooxanthellae represent 'cool' and 'warm' symbionts with respect to their field distributions, and that these symbionts may differ in their nutritional contributions to their host. We examined the seasonal distribution, density, and growth of these symbionts in A. xanthogrammica tentacles from tidepools and surge channels on the Olympic peninsula in Washington State, USA, measured temperature variation between these microhabitats, and estimated the contributions of zoochlorellae to A. xanthogrammica diet. Tentacles containing dense concentrations of zoochlorellae were found in both tidepools and surge channels at the lower intertidal limit of anemone occurrence. At the upper intertidal limit, tentacles containing primarily zoochlorellae were found in tidepools, and tentacles containing primarily zooxanthellae were found in surge channels. More extreme high tem peratures in the upper surge channel may limit the distribution of zoochlorellae and favor a higher proportion of zooxanthellae in this microhabitat. Despite pronounced seasonal fluctuations in temperature, symbiont composition, density, and dietary carbon sources remained remarkably con sistent. Stable isotope analysis showed that A. xanthogrammica received a greater proportion of dietary carbon from zoochlorellae (62−70%) than from heterotrophic feeding on Mytilus californianus mussels (31−38%). This study shows that dense concentrations of zoochlorellae are found in A. xanthogrammica tentacles in cooler microhabitats, and that this symbiont can contribute substantially to anemone nutrition. KEY WORDS: Zoochlorellae · Zooxanthellae · Temperate symbiosis · Anthopleura xanthogrammica Resale or republication not permitted without written consent of the publisherMar Ecol Prog Ser 453: [79][80][81][82][83][84][85][86][87][88][89][90][91][92][93][94] 2012 dominate at high shore heights, mixed zoochlorellae and zooxanthellae populations are found at intermediate shore heights, and zoochlorellae occur primarily at low shore heights (Bates 2000, Kitaeff 2007. This pattern for A. xanthogrammica is also evident on a latitudinal scale, with zooxanthellate anemones found at low latitudes, mixed anemones at intermediate latitudes, and zoochlorellate anemones at high latitudes (Secord & Augustine 2000, Kitaeff 2007.Field distributions of symbionts in Anthopleura elegantissima further support a 'cool' and 'warm' symbiont distribution, with this anemone's generally smaller, and therefore warmer , body containing more zooxanthellae throughout its range, with an exclusion of zoochlorellae seen at lower latitudes and upper shore heights, than in A. xantho grammica (Secord & Augustine 2000). In A. elegantissima, algal distributions remain stable seasonally despite considerable variation in aerial temperature and irr...

Symbiont physiology and population dynamics before and during symbiont shifts in a flexible algal‐cnidarian symbiosis

“…This tendency for stability over change has raised questions as to whether symbiont shifts are a viable acclimatization strategy for symbiotic cnidarians (Goulet 2006, Thornhill et al 2006). On the other hand, experimental manipulations that simulate environmental change often elicit symbiont shifts (e.g., Rowan et al 1997, Bates 2000, Baker 2001, this study) in symbioses that have been found to be largely stable in nature (Thornhill et al 2006, Levine and Muller-Parker 2012, suggesting that symbiont shifts require environmental perturbations of greater severity or duration than have been commonly observed in nature. Indeed, Baird et al (2007) argue that when forced to acclimatize to enduring environmental changes, such as transplantation experiments or geographical climate gradients, hosts often have the capacity to do so by associating with different algal symbionts.…”

“…Anthopleura symbioses provide an excellent case study of the paradoxically stable yet dynamic nature of cnidarian symbioses: typically characterized by a single dominant symbiont, they are temporally stable over short (annual) time scales (Dimond et al. , Levine and Muller‐Parker ), yet vary geographically (Secord and Augustine ), can be forced to shift experimentally (Saunders and Muller‐Parker , Bates , this study), and are forecasted to shift naturally over longer time scales (Verde and McCloskey , Dimond et al. , Levine and Muller‐Parker ).…”

“…, Dimond et al. , Levine and Muller‐Parker ), suggesting that symbiont shifts require environmental perturbations of greater severity or duration than have been commonly observed in nature. Indeed, Baird et al.…”

“…Therefore, as climatic warming ensues, the likely replacement of E. marina by S. muscatinei (Dimond et al. , Levine and Muller‐Parker ) may have significant ecological consequences for A. elegantissima .…”

“…Host fidelity to a single dominant symbiont appears to be the most common form of relationship (Goulet 2006), but increasingly sensitive molecular techniques continue to reveal background populations of other symbionts in hospite, suggesting that the potential to engage in viable symbioses with more than one symbiont may be greater than previously thought (Mieog et al 2007, Silverstein et al 2012). However, even well-known examples of so-called flexible symbioses are often characterized by a high degree of spatial and temporal stability of just one dominant symbiont, even when challenged with bleaching or large seasonal environmental fluctuations (Thornhill et al 2006, Levine and Muller-Parker 2012, McGinley et al 2012). This tendency for stability over change has raised questions as to whether symbiont shifts are a viable acclimatization strategy for symbiotic cnidarians (Goulet 2006, Thornhill et al 2006).…”