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

Abstract

For cnidarians that can undergo shifts in algal symbiont relative abundance, the underlying algal physiological changes that accompany these shifts are not well known. The sea anemone Anthopleura elegantissima associates with the dinoflagellate Symbiodinium muscatinei and the chlorophyte Elliptochloris marina, symbionts with very different tolerances to light and temperature. We compared the performance of these symbionts in anemones maintained in an 8-11.5 month outdoor common garden experiment with simulated intertidal conditions and three levels of shading (2, 43, and 85% ambient irradiance). Symbiont densities, mitotic indices, photophysiology and pigments were assessed at three time points during the summer, a period of high irradiance and solar heating during aerial exposure. Whereas S. muscatinei was either neutrally or positively affected by higher irradiance treatments, E. marina responded mostly negatively to high irradiance. E. marina in the 85% irradiance treatment exhibited significantly reduced Pmax and chlorophyll early in the summer, but it was not until nearly 3 months later that a shift in symbiont relative abundance toward S. muscatinei occurred, coincident with bleaching. Symbiont densities and proportions remained largely stable in all other treatments over time, and displacement of S. muscatinei by E. marina was not observed in the 2% irradiance treatment despite the potentially better performance of E. marina. While our results support the view that rapid changes in symbiont relative abundance are typically associated with symbiont physiological dysfunction and bleaching, they also show that significant temporal lags may occur between the onset of symbiont stress and shifts in symbiont relative abundances.

Symbiotic state influences life-history strategy of a clonal cnidarian

“…However, persistent changes in irradiance or temperature can change symbiont composition [22] or, in extreme cases, lead to bleaching [20,28,45]. Thus, shifts in symbiont dominance are likely to occur in response to climate change [28], with the more heat-tolerant zooxanthellae replacing zoochlorellae where air and seawater temperatures increase.…”

“…The symbiont changes that occurred in anemones excluded from analyses and the effects of the treatments on the symbionts themselves are described elsewhere [22]. Final symbiotic state was assessed by homogenizing the anemones and using a haemocytometer to identify and count 80-100 symbiont cells in each of four replicate homogenate subsamples (or up to 16 haemocytometer chambers if densities were low).…”

“…These symbionts, which can occur singly or together in individual anemones, have different physiologies, growth rates and biotrophic relationships with their hosts [17 -21]. Under high irradiance and temperature conditions, zooxanthellae will supplant zoochlorellae in A. elegantissima, and intense, ongoing stress can lead to complete bleaching (loss of symbionts) and hosts that are functionally aposymbiotic [22]. Zooxanthellate A. elegantissima are generally more productive than individuals hosting zoochlorellae: annual net productivity is estimated at 92 and 60 g C m 22 y…”

Microbiome Variation in an Intertidal Sea Anemone Across Latitudes and Symbiotic States

“…Some cnidarians, such as the intertidal sea anemone Anthopleura elegantissima, experience extreme thermal variation in their natural habitat with no adverse effects to their symbiosis with the brown algal Symbiodinium (Bingham et al, 2011). A. elegantissima also occasionally hosts a green algal symbiont, Elliptochloris marina, but this symbiosis is highly susceptible to bleaching (Dimond et al, 2013). Observing the microbiota associated with A. elegantissima in these different symbiotic states may provide clues into the relationship between stability of bacterial communities and stability of cnidarian-algal symbioses.…”

Coral responses to temperature, irradiance and acidification stress: linking physiology to satellite remote sensing

“…In corals, F v /F m displays indications of a photoacclimation response, for instance, F v /F m decreases with decreasing depth (Warner et al 2002;Fitt et al 2000;Lesser and Gorbunov 2001). However, the interpretation of F v /F m data to infer photoacclimation is complicated by the fact that, whilst a depressed F v /F m can indicate a dysfunction of actual photosynthesis, in other circumstances F v /F m can be depressed and yet actual photosynthesis is still occurring at normal rates (Dimond et al 2013). This is because some photosynthetic organisms possess photoprotective mechanisms that result in depressed F v /F m but enable actual photosynthesis to continue unimpaired under light levels that would be otherwise damaging (Matsubara and Chow 2004). )…”