The existence of widespread species with the capacity to endure diverse, or variable, environments are of importance to ecological and genetic research, and conservation. Such “ecological generalists” are more likely to have key adaptations that allow them to better tolerate the physiological challenges of rapid climate change. Reef‐building corals are dependent on endosymbiotic dinoflagellates (Family: Symbiodiniaceae) for their survival and growth. While these symbionts are biologically diverse, certain genetic types appear to have broad geographic distributions and are mutualistic with various host species from multiple genera and families in the order Scleractinia that must acquire their symbionts through horizontal transmission. Despite the considerable ecological importance of putative host‐generalist symbionts, they lack formal species descriptions. In this study, we used molecular, ecological, and morphological evidence to verify the existence of five new host‐generalist species in the symbiodiniacean genus
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Abstract Cladocopium . Their geographic distribution and prevalence among host communities corresponds to prevailing environmental conditions at both regional and local scales. The influence that each species has on host physiology may partially explain regional differences in thermal sensitivities among coral communities. The potential increased prevalence of a generalist species that endures environmental instability is a consequential ecological response to warming oceans. Large‐scale shifts in symbiont dominance could ensure reef coral persistence and productivity in the near term. Ultimately, these formal designations should advance scientific communication and generate informed research questions on the physiology and ecology of coral‐dinoflagellate mutualisms. -
Abstract Coral reefs are declining worldwide, yet some coral populations are better adapted to withstand reductions in pH and the rising frequency of marine heatwaves. The nearshore reef habitats of Palau, Micronesia are a proxy for a future of warmer, more acidic oceans. Coral populations in these habitats can resist, and recover from, episodes of thermal stress better than offshore conspecifics. To explore the physiological basis of this tolerance, we compared tissue biomass (ash-free dry weight cm−2), energy reserves (i.e., protein, total lipid, carbohydrate content), and several important lipid classes in six coral species living in both offshore and nearshore environments. In contrast to expectations, a trend emerged of many nearshore colonies exhibiting lower biomass and energy reserves than colonies from offshore sites, which may be explained by the increased metabolic demand of living in a warmer, acidic, environment. Despite hosting different dinoflagellate symbiont species and having access to contrasting prey abundances, total lipid and lipid class compositions were similar in colonies from each habitat. Ultimately, while the regulation of colony biomass and energy reserves may be influenced by factors, including the identity of the resident symbiont, kind of food consumed, and host genetic attributes, these independent processes converged to a similar homeostatic set point under different environmental conditions.
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Abstract Reef‐building corals in the genus
Porites are one of the most important constituents of Indo‐Pacific reefs. Many species within this genus tolerate abnormally warm water and exhibit high specificity for particular kinds of endosymbiotic dinoflagellates that cope with thermal stress better than those living in other corals. Still, during extreme ocean heating, somePorites exhibit differences in their stress tolerance. While corals have different physiological qualities, it remains unknown whether the stability and performance of these mutualisms is influenced by the physiology and genetic relatedness of their symbionts. We investigated two ubiquitous Pacific reef corals,Porites rus andPorites cylindrica , from warmer inshore and cooler offshore reef systems in Palau. While these corals harbored a similar kind of symbiont in the genusCladocopium (within the ITS2C15 subclade), rapidly evolving genetic markers revealed evolutionarily diverged lineages corresponding to eachPorites species living in each reef habitat. Furthermore, these closely relatedCladocopium lineages were differentiated by their densities in host tissues, cell volume, chlorophyll concentration, gross photosynthesis, and photoprotective pathways. When assessed using several physiological proxies, these previously undifferentiated symbionts contrasted in their tolerance to thermal stress. Symbionts withinP .cylindrica were relatively unaffected by exposure to 32℃ for 14 days, whereasP .rus colonies lost substantial numbers of photochemically compromised symbionts. Heating reduced the ability of the offshore symbiont associated withP .rus to translocate carbon to the coral. By contrast, high temperatures enhanced symbiont carbon assimilation and delivery to the coral skeleton of inshoreP .cylindrica . This study indicates that large physiological differences exist even among closely related symbionts, with significant implications for thermal susceptibility among reef‐buildingPorites . -
Symbiotic mutualisms are essential to ecosystems and numerous species across the tree of life. For reef-building corals, the benefits of their association with endosymbiotic dinoflagellates differ within and across taxa, and nutrient exchange between these partners is influenced by environmental conditions. Furthermore, it is widely assumed that corals associated with symbionts in the genus
Durusdinium tolerate high thermal stress at the expense of lower nutrient exchange to support coral growth. We traced both inorganic carbon (H13CO3–) and nitrate (15NO3–) uptake by divergent symbiont species and quantified nutrient transfer to the host coral under normal temperatures as well as in colonies exposed to high thermal stress. Colonies representative of diverse coral taxa associated withDurusdinium trenchii orCladocopium spp. exhibited similar nutrient exchange under ambient conditions. By contrast, heat-exposed colonies withD. trenchii experienced less physiological stress than conspecifics withCladocopium spp. while high carbon assimilation and nutrient transfer to the host was maintained. This discovery differs from the prevailing notion that these mutualisms inevitably suffer trade-offs in physiological performance. These findings emphasize that many host–symbiont combinations adapted to high-temperature equatorial environments are high-functioning mutualisms; and why their increased prevalence is likely to be important to the future productivity and stability of coral reef ecosystems. -
Warming and nutrient limitation are stressors known to weaken the health of microalgae. In situations of stress, access to energy reserves can minimize physiological damage. Because of its widespread requirements in biochemical processes, iron is an important trace metal, especially for photosynthetic organisms. Lowered iron availability in oceans experiencing rising temperatures may contribute to the thermal sensitivity of reef‐building corals, which rely on mutualisms with dinoflagellates to survive. To test the influence of iron concentration on thermal sensitivity, the physiological responses of cultured symbiotic dinoflagellates (genus
Breviolum ; family Symbiodiniaceae) were evaluated when exposed to increasing temperatures (26 to 30°C) and iron concentrations ranging from replete (500 pM Fe’) to limiting (50 pM Fe’) under a diurnal light cycle with saturating radiance. Declines in photosynthetic efficiency at elevated temperatures indicated sensitivity to heat stress. Furthermore, five times the amount of iron was needed to reach exponential growth during heat stress (50 pM Fe′ at 26–28°C vs. 250 pM Fe′ at 30°C). In treatments where exponential growth was reached,Breviolum psygmophilum grew faster thanB .minutum , possibly due to greater cellular contents of iron and other trace metals. The metal composition ofB .psygmophilum shifted only at the highest temperature (30°C), whereas changes inB .minutum were observed at lower temperatures (28°C). The influence of iron availability in modulating each alga’s response to thermal stress suggests the importance of trace metals to the health of coral‐algal mutualisms. Ultimately, a greater ability to acquire scarce metals may improve the tolerance of corals to physiological stressors and contribute to the differences in performance associated with hosting one symbiont species over another.