Community dynamics and physiology of Symbiodinium associated with Orbicella (= Montastraea) faveolata were examined before, during, and after a thermally induced coral bleaching event in Puerto ...Morelos, Mexico. We combined microsampling molecular genotyping with in situ pulse-amplitude modulated fluorometry to correlate colony variability of Symbiodinium population identities and the phenomena of partial coral bleaching. Pigmented nonbleached portions of O. (=M.) faveolata were compared with bleached portions of the same colony. During bleaching, maximum quantum yield of photosystem II (PSII; Fv : Fm) was significantly lower and highly variable (range 0.110 to 0.680) compared with previous summers in which coral bleaching was absent (range 0.516 to 0.661) and recovery (range 0.480 to 0.716). Differential susceptibility to environmental perturbation of Fv : Fm corresponded to distinct genetic identities of Symbiodinium. Analysis of ribosomal deoxyribonucleic acid (rDNA) internal transcribed spacer 2 (ITS2) revealed regions of the coral colonies that had phylotype A3 prior to bleaching were more resistant to the bleaching perturbation than adjacent bleaching-prone patches that harbored phylotypes B17 and C7. During environmental perturbation, regions of the colonies containing predominantly Symbiodinium phylotypes A3 or D1a retained significantly higher Fv : Fm values than adjacent regions with phylotypes B17 and C7. Following bleaching, rapid recovery of symbiotic algal densities greatly exceeded normal seasonal oscillations. During recovery we document shifts in Symbiodinium populations and increase prevalence of Symbiodinium types A3 and D1a, phylotypes known to have enhanced thermal tolerances. Thermal tolerance of Symbiodinium spp. influences the changes of coral–Symbiodinium communities during disturbance events and the dynamics of coral–Symbiodinium repopulation.
The specific identity of endosymbiotic dinoflagellates (Symbiodinium spp.) from most zooxanthellate corals is unknown. In a survey of symbiotic cnidarians from the southern Great Barrier Reef (GBR), ...23 symbiont types were identified from 86 host species representing 40 genera. A majority (>85%) of these symbionts belong to a single phylogenetic clade or subgenus ("C") composed of closely related (as assessed by sequence data from the internal transcribed spacer region and the ribosomal large subunit gene), yet ecologically and physiologically distinct, types. A few prevalent symbiont types, or generalists, dominate the coral community of the southern GBR, whereas many rare and/or specific symbionts, or specialists, are found uniquely within certain host taxa. The comparison of symbiont diversity between southern GBR and Caribbean reefs shows an inverse relationship between coral diversity and symbiont diversity, perhaps as a consequence of more-rapid diversification of Caribbean symbionts. Among clade C types, generalists C1 and C3 are common to both Caribbean and southern GBR symbiont assemblages, whereas the rest are regionally endemic. Possibly because of environmental changes in the Caribbean after geographic isolation through the Quaternary period, a high proportion of Caribbean fauna associate with symbiont taxa from two other distantly related Symbiodinium clades (A and B) that rarely occur in Pacific hosts. The resilience of Porites spp. and the resistance of Montipora digitata to thermal stress and bleaching are partially explained by their association with a thermally tolerant symbiont type, whereas the indiscriminant widespread bleaching and death among certain Pacific corals, during E1 Niño Southern Oscillation events, are influenced by associations with symbionts possessing higher sensitivity to thermal stress.
Aim: This study examines the importance of geographic proximity, host life history and regional and local differences in environment (temperature and water clarity) in driving the ecological and ...evolutionary process underpinning the global patterns of diversity and distribution of symbiotic dinoflagellates. By comparing and contrasting coral—algal symbioses from isolated regions with differing environmental conditions, we may assess the potential of coral communities to respond to significant changes in climate. Location: Indian Ocean. Methods: Community assemblages of obligate symbiotic invertebrates were sampled at numerous sites from two regions, the north-eastern Indian Ocean (Andaman Sea, western Thailand) and the western Indian Ocean (Zanzibar, Tanzania). Molecular genetic methods, including denaturing gradient gel electrophoresis analysis of the ribosomal internal transcribed spacers, DNA sequencing and microsatellite genotyping, were used to characterize the 'species' diversity and evolutionary relationships of symbiotic dinoflagellates (genus Symbiodinium). Host—symbiont specificity, geographic isolation and local and regional environmental factors were evaluated in terms of their importance in governing the distribution and prevalence of certain symbiont taxa. Results: Host-generalist symbionts (C3u and D1-4, formerly D1a now designated Symbiodinium trenchi) frequently occurred alone and sometimes together in hosts with horizontal modes of symbiont acquisition. However, the majority of Symbiodinium diversity consisted of apparently host-specific 'species'. Clade C Symbiodinium were diverse and dominated host assemblages from sites sampled in the western Indian Ocean, a pattern analogous to symbiont communities on the Great Barrier Reef with similar environmental conditions. Clade D Symbiodinium were diverse and occurred frequently in hosts from the north-eastern Indian Ocean, especially at inshore locations, where temperatures are warmer, water turbidity is high and large tidal exchanges commonly expose coral populations to aerial desiccation. Main conclusions: Regional and local differences in cnidarian—algal combinations indicate that these symbioses are ecologically and evolutionarily responsive and can thrive under various environmental conditions. The high temperatures and turbid conditions of the north-eastern Indian Ocean partly explain the ecological success of Clade D Symbiodinium relative to Clade C. Phylogenetic, ecological and population genetic data further indicate that Clade D has undergone an adaptive radiation, especially in regions around Southeast Asia, during the Pleistocene.
Coral reefs of the Florida Keys typically experience seasonal temperatures of 20–31 °C. Deviation outside this range causes physiological impairment of reef‐building corals, potentially leading to ...coral colony death. In January and February 2010, two closely spaced cold fronts, possibly driven by an unusually extreme Arctic Oscillation, caused sudden and severe seawater temperature declines in the Florida Keys. Inshore coral reefs e.g., Admiral Reef (ADM) experienced lower sustained temperatures (i.e., < 12 °C) than those further offshore e.g., Little Grecian Reef (LG), minimum temperature = 17.2 °C. During February and March 2010, we surveyed ADM and observed a mass die‐off of reef‐building corals, whereas 12 km away LG did not exhibit coral mortality. We subsequently measured the physiological effects of low‐temperature stress on three common reef‐building corals (i.e., Montastraea faveolata, Porites astreoides, and Siderastrea siderea) over a range of temperatures that replicated the inshore cold‐water anomaly (i.e., from 20 to 16 to 12 °C and back to 20 °C). Throughout the temperature modulations, coral respiration as well as endosymbiont gross photosynthesis and maximum quantum efficiency of photosystem II were measured. In addition, Symbiodinium genotypic identity, cell densities, and chlorophyll a content were determined at the beginning and conclusion of the experiment. All corals were significantly affected at 12 °C, but species‐specific physiological responses were found indicating different coral and/or Symbiodinium cold tolerances. Montastraea faveolata and P. astreoides appeared to be most negatively impacted because, upon return to 20 °C, significant reductions in gross photosynthesis and dark respiration persisted. Siderastrea siderea, however, readily recovered to pre‐treatment rates of dark respiration and gross photosynthesis. Visual surveys of inshore reefs corroborated these results, with S. siderea being minimally affected by the cold‐water anomaly, whereas M. faveolata and P. astreoides exhibited nearly 100% mortality. This study highlights the importance of understanding the physiological attributes of genotypically distinct coral‐Symbiodinium symbioses that contribute to tolerance, recovery, and consequences to an environmental perturbation. These data also document effects of a rarely studied environmental stressor, possibly initiated by remote global climate events, on coral‐Symbiodinium symbioses and coral reef communities.
Coral bleaching has been defined as a general phenomenon, whereby reef corals turn visibly pale because of the loss of their symbiotic dinoflagellates and/or algal pigments during periods of exposure ...to elevated seawater temperatures. During the summer of 1997, seawater temperatures in the Florida Keys remained at or above 30 degrees C for more than 6 weeks, and extensive coral bleaching was observed. Bleached colonies of the dominant Caribbean reef-building species, Montastrea faveolata and Montastrea franksi, were sampled over a depth gradient from 1 to 17 m during this period of elevated temperature and contained lower densities of symbiotic dinoflagellates in deeper corals than seen in previous "nonbleaching" years. Fluorescence analysis by pulse-amplitude modulation fluorometry revealed severe damage to photosystem II (PSII) in remaining symbionts within the corals, with greater damage indicated at deeper depths. Dinoflagellates with the greatest loss in PSII activity also showed a significant decline in the D1 reaction center protein of PSII, as measured by immunoblot analysis. Laboratory experiments on the temperature-sensitive species Montastrea annularis, as well as temperature-sensitive and temperature-tolerant cultured symbiotic dinoflagellates, confirmed the temperature-dependent loss of PSII activity and concomitant decrease in D1 reaction center protein seen in symbionts collected from corals naturally bleached on the reef. In addition, variation in PSII repair was detected, indicating that perturbation of PSII protein turnover rates during photoinhibition at elevated temperatures underlies the physiological collapse of symbionts in corals susceptible to heat-induced bleaching.
The dinoflagellate genus Symbiodinium forms symbioses with numerous protistan and invertebrate metazoan hosts. However, few data on symbiont genetic structure are available, hindering predictions of ...how these populations and their host associations will fair in the face of global climate change.
Here, Symbiodinium population structure from two of the Caribbean's ecologically dominant scleractinian corals, Montastraea faveolata and M. annularis, was examined. Tagged colonies on Florida Keys and Bahamian (i.e., Exuma Cays) reefs were sampled from 2003-2005 and their Symbiodinium diversity assessed via internal transcribed spacer 2 (ITS2) rDNA and three Symbiodinium Clade B-specific microsatellite loci. Generally, the majority of host individuals at a site harbored an identical Symbiodinium ITS2 "type" B1 microsatellite genotype. Notably, symbiont genotypes were largely reef endemic, suggesting a near absence of dispersal between populations. Relative to the Bahamas, sympatric M. faveolata and M. annularis in the Florida Keys harbored unique Symbiodinium populations, implying regional host specificity in these relationships. Furthermore, within-colony Symbiodinium population structure remained stable through time and environmental perturbation, including a prolonged bleaching event in 2005.
Taken together, the population-level endemism, specificity and stability exhibited by Symbiodinium raises concerns about the long-term adaptive capacity and persistence of these symbioses in an uncertain future of climate change.
Increased sea-surface temperatures linked to warming climate threaten coral reef ecosystems globally. To better understand how corals and their endosymbiotic dinoflagellates (Symbiodinium spp.) ...respond to environmental change, tissue biomass and Symbiodinium density of seven coral species were measured on various reefs approximately every four months for up to thirteen years in the Upper Florida Keys, United States (1994-2007), eleven years in the Exuma Cays, Bahamas (1995-2006), and four years in Puerto Morelos, Mexico (2003-2007). For six out of seven coral species, tissue biomass correlated with Symbiodinium density. Within a particular coral species, tissue biomasses and Symbiodinium densities varied regionally according to the following trends: Mexico≥Florida Keys≥Bahamas. Average tissue biomasses and symbiont cell densities were generally higher in shallow habitats (1-4 m) compared to deeper-dwelling conspecifics (12-15 m). Most colonies that were sampled displayed seasonal fluctuations in biomass and endosymbiont density related to annual temperature variations. During the bleaching episodes of 1998 and 2005, five out of seven species that were exposed to unusually high temperatures exhibited significant decreases in symbiotic algae that, in certain cases, preceded further decreases in tissue biomass. Following bleaching, Montastraea spp. colonies with low relative biomass levels died, whereas colonies with higher biomass levels survived. Bleaching- or disease-associated mortality was also observed in Acropora cervicornis colonies; compared to A. palmata, all A. cervicornis colonies experienced low biomass values. Such patterns suggest that Montastraea spp. and possibly other coral species with relatively low biomass experience increased susceptibility to death following bleaching or other stressors than do conspecifics with higher tissue biomass levels.
Worldwide decline in coral populations has led to the development of numerous coral conservation and restoration groups. These groups have established successful methods for propagating and growing ...corals in nurseries for outplanting to degraded reefs. However, the environment within land-based nurseries differs from natural reef environments since nursery conditions are optimized to aid coral health and accelerate growth. This study compares the physiological condition of Mote Marine Laboratory’s land-based nursery corals to over two decades of coral physiology data collected seasonally from wild conspecific populations of the Florida Keys. Coral metabolism metrics suggest that nursery corals are similar to wild conspecifics. Despite this, coral biomass and symbiotic algae pigmentation suggest that Mote’s land-based nursery corals are acclimated to low light, and maintain different Symbiodiniaceae populations compared to wild conspecifics. Our findings elucidate how the biology and physiology of corals raised in land-based nurseries are different from wild coral populations and indicate nursery corals likely incur substantial photoacclimation processes during outplanting. These insights provide a physiological framework for coral conservation and management efforts that can be used when considering the condition of nursery-raised corals before outplanting to a reef.
Photoinhibition, exacerbated by elevated temperatures, underlies coral bleaching, but sensitivity to photosynthetic loss differs among various phylotypes of Symbiodinium, their dinoflagellate ...symbionts. Symbiodinium is a common symbiont in many cnidarian species including corals, jellyfish, anemones, and giant clams. Here, we provide evidence that most members of clade A Symbiodinium, but not clades B-D or F, exhibit enhanced capabilities for alternative photosynthetic electron-transport pathways including cyclic electron transport (CET). Unlike other clades, clade A Symbiodinium also undergo pronounced light-induced dissociation of antenna complexes from photosystem II (PSII) reaction centers. We propose these attributes promote survival of most cnidarians with clade A symbionts at high light intensities and confer resistance to bleaching conditions that conspicuously impact deeper dwelling corals that harbor non-clade A SYMBIODINIUM:
Reef-building corals import inorganic carbon (Ci) to build their calcium carbonate skeletons and to support photosynthesis by the symbiotic algae that reside in their tissue. The internal pathways ...that deliver Ci for both photosynthesis and calcification are known to involve the enzyme carbonic anhydrase (CA), which interconverts CO2 and HCO3 (-). We have developed a method for absolute quantification of internal CA (iCA) activity in coral tissue based on the rate of (18)O-removal from labeled Ci. The method was applied to three Caribbean corals (Orbicella faveolata, Porites astreoides and Siderastrea radians) and showed that these species have similar iCA activities per unit surface area, but that S. radians has ∼10-fold higher iCA activity per unit tissue volume. A model of coral Ci processing shows that the measured iCA activity is sufficient to support the proposed roles for iCA in Ci transport for photosynthesis and calcification. This is the case even when iCA activity is homogeneously distributed throughout the coral, but the model indicates that it would be advantageous to concentrate iCA in the spaces where calcification (the calcifying fluid) and photosynthesis (the oral endoderm) take place. We argue that because the rates of photosynthesis and calcification per unit surface area are similar among the corals studied here, the areal iCA activity used to deliver Ci for these reactions should also be similar. The elevated iCA activity per unit volume of S. radians compared with that of the other species is probably due to the thinner effective tissue thickness in this species.
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