Seasonal stability of a flexible algal–cnidarian symbiosis in a highly variable temperate environment

Abstract

We evaluated the seasonal stability of two algal symbiont populations in the temperate intertidal sea anemone Anthopleura elegantissima on San Juan Island, Washington, where the relatively thermally tolerant dinoflagellate Symbiodinium muscatinei coexists with the less thermally tolerant chlorophyte Elliptochloris marina. Random collection of anemones along repeatedly sampled transects over four seasons and three shore heights revealed S. muscatinei to be the dominant symbiont, with E. marina mostly limited to anemones in the lower intertidal zone. At the lowest shore height sampled (+0.2 m), the proportion of E. marina was between 40% and 50% of the total symbiont population throughout the year. Symbiont distribution patterns persisted despite considerable seasonal variation in aerial exposure, temperature, irradiance, nutrients, and phytoplankton concentration, as well as a high potential for symbiont shuffling, with mixed-symbiont assemblages occurring in 51% of all anemones sampled. Symbiont density in anemones also changed little despite three-to fourfold-higher division frequencies of both symbionts during July and November. Although the intertidal zonation of these symbionts was stable over an annual period, we predict that their spatial distributions will be responsive to longer-term environmental change, and anticipate that this anemone symbiosis will be a useful and highly tractable barometer for future climate change, with this study serving as a baseline.A diverse array of shallow-water cnidarians, including sea anemones, corals, jellyfish, and hydroids, engage in endosymbioses with phototrophic dinoflagellates (Symbiodinium spp.) that translocate photosynthetic products to their host. Many of these symbioses exhibit plasticity with respect to both the population density and genetic identity of the dinoflagellate partner, allowing them to exploit a wide range of conditions that vary spatially and temporally. In tropical systems, where cnidarian symbioses are particularly well studied, many hosts show depth-related differences in symbiont density and physiology, and also undergo predictable seasonal fluctuations in symbiont density and physiology that are correlated with environ-

Thicker host tissues moderate light stress in a cnidarian endosymbiont

“…Another consideration is that E. marina chlorophyll content does not always change predictably in response to changes in irradiance. Elliptochloris marina living within A. elegantissima show little seasonal variation in cell-specific chlorophyll content despite large fluctuations in irradiance (Verde and McCloskey, 2007;Dimond et al, 2011). We have also found that E. marina chlorophyll content within A. elegantissima does not consistently increase during long-term experimental shading (J.L.D., B.L.B.…”

“…and chlorophyte (Elliptochloris marina) symbionts. Relative to Symbiodinium muscatinei, E. marina exhibits low tolerance of high light and temperature, and is typically found in cooler, low-light habitats (Bates, 2000;Verde and McCloskey, 2001;Verde and McCloskey, 2002;Secord and Muller-Parker, 2005;Dimond et al, 2011). Interestingly, however, E. marina occurs approximately 6degrees of latitude farther south and much higher in the intertidal zone in A. xanthogrammica than in A. elegantissima (Secord and Augustine, 2000), indicating that host factors have an important effect on symbiont distribution patterns.…”

“…For both analyses, symbiont cell suspensions were obtained by homogenizing frozen (-70°C) excised tentacles in filtered seawater with a motorized Teflon tissue grinder. Spectrophotometry was performed according to methods described by Dimond et al (Dimond et al, 2011). Flow cytometry was performed using a BD FACSCalibur instrument (BD Biosciences, Franklin Lakes, NJ, USA) with a 488nm excitation laser.…”

Symbiotic state influences life-history strategy of a clonal cnidarian

“…This bears some similarity to Hydra viridis (green hydra), which produces female gonads only if the Chlorella algal symbiont is present [40]. Although E. marina is less tolerant of high temperature and irradiance [17][18][19] and consistently less productive than S. muscatinei on a per-cell basis [41], the growth rate of E. marina is higher [19,21], and in habitats where irradiance and temperature are low year round, A. elegantissima commonly hosts E. marina at up to twice the density of S. muscatinei [20,28]. Thus, zoochlorellate A. elegantissima may be nearly as productive as zooxanthellate individuals under some conditions [19,28], but appear to direct more energy to sexual reproduction.…”

“…Locally, A. elegantissima begin developing gonads in January, spawn from August to October [27] and are exposed to the harshest physical stresses during mid-day summer low tides [28]. Shields were used to reduce natural irradiance in each of three treatment groups, approximating conditions that favour zooxanthellate, zoochlorellate and aposymbiotic anemones, respectively [20]: ultraviolet (UV)-transparent acrylic shield for 85% irradiance, UV-transparent acrylic shield plus a layer of window screen for 43% irradiance and opaque grey PVC shield for 2% irradiance.…”