Coral bleaching has been defined as a general phenomenon, whereby reef corals turn visibly pale because of the loss of their symbiotic dinof lagellates and͞or 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°C for more than 6 weeks, and extensive coral bleaching was observed. Bleached colonies of the dominant Caribbean reefbuilding 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 dinof lagellates in deeper corals than seen in previous ''nonbleaching'' years. Fluorescence analysis by pulse-amplitude modulation f luorometry revealed severe damage to photosystem II (PSII) in remaining symbionts within the corals, with greater damage indicated at deeper depths. Dinof lagellates 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 dinof lagellates, 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.Global episodes of coral bleaching, where reef-building corals lose their endosymbiotic dinoflagellates and͞or algal pigments during summertime elevation of seawater temperature, are recurring with increasing frequency and severity (1, 2). Previous studies have shown that symbiotic dinoflagellates maintained in culture and within the host are susceptible to thermal stress (3-5). Likewise, photosynthetically active radiation (PAR) and UV radiation may act in concert with elevated temperatures to elicit a bleaching response (6, 7), yet the underlying biochemical causes for these phenomena remain obscure. Numerous components of the photosynthetic pathway are known to be susceptible to damage by elevated temperature, especially at points within photosystem II (PSII). These include the oxygen-evolving complex (8, 9), the reaction center (10), as well as connectivity between the lightharvesting complex and the reaction center of PSII (11). In plants and green algae, thermal perturbation can predispose the photosynthetic apparatus to damage by PAR, thus inducing a state of photoinhibition (12). The primary target of photoinhibitory damage at the PSII reaction center is the D1 protein (13), which normally exhibits high rates of turnover involving light-dependent inactivation and degradation coupled with de novo synthesis and in...
Diazotrophic marine cyanobacteria in the genus Trichodesmium contribute a large fraction of the new nitrogen entering the oligotrophic oceans, but little is known about how they respond to shifts in global change variables such as carbon dioxide (CO 2 ) and temperature. We compared Trichodesmium dinitrogen (N 2 ) and CO 2 fixation rates during steady-state growth under past, current, and future CO 2 scenarios, and at two relevant temperatures. At projected CO 2 levels of year 2100 (76 Pa, 750 ppm), N 2 fixation rates of Pacific and Atlantic isolates increased 35-100%, and CO 2 fixation rates increased 15-128% relative to present day CO 2 conditions (39 Pa, 380 ppm). CO 2 -mediated rate increases were of similar relative magnitude in both phosphorus (P)-replete and P-limited cultures, suggesting that this effect may be independent of resource limitation. Neither isolate could grow at 15 Pa (150 ppm) CO 2 , but N 2 and CO 2 fixation rates, growth rates, and nitrogen : phosophorus (N : P) ratios all increased significantly between 39 Pa and 152 Pa (1500 ppm). In contrast, these parameters were affected only minimally or not at all by a 4uC temperature change. Photosynthesis versus irradiance parameters, however, responded to both CO 2 and temperature but in different ways for each isolate. These results suggest that by the end of this century, elevated CO 2 could substantially increase global Trichodesmium N 2 and CO 2 fixation, fundamentally altering the current marine N and C cycles and potentially driving some oceanic regimes towards P limitation. CO 2 limitation of Trichodesmium diazotrophy during past glacial periods could also have contributed to setting minimum atmospheric CO 2 levels through downregulation of the biological pump. The relationship between marine N 2 fixation and atmospheric CO 2 concentration appears to be more complex than previously realized and needs to be considered in the context of the rapidly changing oligotrophic oceans.
Tissue biomass (ash-free dry weight) and symbiotic dinoflagellates (density, chlorophyll a cell Ϫ1 or cm Ϫ2 of coral surface area) of five species of reef-building corals were monitored seasonally for up to 4 yr at three different depths in the Bahamas. The lowest values of all tissue biomass and algal symbiont parameters occurred during the late summer-fall sample periods. In contrast, the highest densities and pigment content of symbionts usually occurred during the winter, whereas tissue biomass peaked most often in the spring, the time lag implying a functional relationship between these variables. Corals living in shallow water often (but not always) had higher levels of all parameters measured compared to deeper corals, except chlorophyll a content, which usually displayed the opposite trend. The results show that corals from all depths exhibited bleaching (loss of symbiotic dinoflagellates and/or their pigments) every year, regardless of whether they appeared white, tan, or mottled to the human eye. We speculate that these patterns are driven by seasonal changes in light and temperature on algal and animal physiology. Furthermore, we hypothesize that all tropical reef-building corals, world-wide, exhibit similar predictable cycles in their tissue biomass and symbiotic algae.
Mass coral bleaching events caused by elevated seawater temperatures result in extensive coral loss throughout the tropics, and are projected to increase in frequency and severity. If bleaching becomes an annual event later in this century, more than 90% of coral reefs worldwide may be at risk of long-term degradation. While corals can recover from single isolated bleaching and can acclimate to recurring bleaching events that are separated by multiple years, it is currently unknown if and how they will survive and possibly acclimatize to annual coral bleaching. Here, we demonstrate for the first time that annual coral bleaching can dramatically alter thermal tolerance in Caribbean corals. We found that high coral energy reserves and changes in the dominant algal endosymbiont type (Symbiodinium spp.) facilitated rapid acclimation in Porites divaricata, whereas low energy reserves and a lack of algal phenotypic plasticity significantly increased susceptibility in Porites astreoides to bleaching the following year. Phenotypic plasticity in the dominant endosymbiont type of Orbicella faveolata did not prevent repeat bleaching, but may have facilitated rapid recovery. Thus, coral holobiont response to an isolated single bleaching event is not an accurate predictor of its response to bleaching the following year. Rather, the cumulative impact of annual coral bleaching can turn some coral species 'winners' into 'losers', and can also facilitate acclimation and turn some coral species 'losers' into 'winners'. Overall, these findings indicate that cumulative impact of annual coral bleaching could result in some species becoming increasingly susceptible to bleaching and face a long-term decline, while phenotypically plastic coral species will acclimatize and persist. Thus, annual coral bleaching and recovery could contribute to the selective loss of coral diversity as well as the overall decline of coral reefs in the Caribbean.
Little is known about the combined impacts of future CO 2 and temperature increases on the growth and physiology of marine picocyanobacteria. We incubated Synechococcus and Prochlorococcus under present-day (380 ppm) or predicted year-2100 CO 2 levels (750 ppm), and under normal versus elevated temperatures (+4°C) in semicontinuous cultures. Increased temperature stimulated the cell division rates of Synechococcus but not Prochlorococcus. Doubled CO 2 combined with elevated temperature increased maximum chl a-normalized photosynthetic rates of Synechococcus four times relative to controls. Temperature also altered other photosynthetic parameters (a, F max , E k , and DF =F 0 m ) in Synechococcus, but these changes were not observed for Prochlorococcus. Both increased CO 2 and temperature raised the phycobilin and chl a content of Synechococcus, while only elevated temperature increased divinyl chl a in Prochlorococcus. Cellular carbon (C) and nitrogen (N) quotas, but not phosphorus (P) quotas, increased with elevated CO 2 in Synechococcus, leading to 20% higher C:P and N:P ratios. In contrast, Prochlorococcus elemental composition remained unaffected by CO 2 , but cell volume and elemental quotas doubled with increasing temperature while maintaining constant stoichiometry. Synechococcus showed a much greater response to CO 2 and temperature increases for most parameters measured, compared with Prochlorococcus. Our results suggest that global change could influence the dominance of Synechococcus and Prochlorococcus ecotypes, with likely effects on oligotrophic food-web structure. However, individual picocyanobacteria strains may respond quite differently to future CO 2 and temperature increases, and caution is needed when generalizing their responses to global change in the ocean.
We examined the effects of increased temperature, pCO 2 , and irradiance on a calcifying strain of the marine coccolithophore Emiliania huxleyi in semi-continuous laboratory cultures. Emiliania huxleyi CCMP 371 was cultured in four temperature and pCO 2 treatments at both low and high irradiance (50 and 400 mmol photons m À2 s À1): (i) 20 C and 375 ppm CO 2 (ambient control); (ii) 20 C and 750 ppm CO 2 (high pCO 2 ); (iii) 24 C and 375 ppm CO 2 (high temperature); and (iv) 24 C and 750 ppm CO 2 ('greenhouse'). The growth of E. huxleyi was greatly accelerated by elevated temperature at low irradiance. Photosynthesis was significantly promoted by increases in both pCO 2 and temperature at both irradiances. Higher cellular C/P ratios were found in the higher CO 2 treatments at high irradiance, indicating a reduced requirement for P. The PIC/POC (particulate inorganic to organic carbon) ratio remained constant at low light, regardless of CO 2 or temperature conditions. However, both the cellular PIC content and PIC/POC ratio were greatly decreased by elevated irradiance, and were further decreased by increased pCO 2 only at high light, indicating a combined effect of CO 2 and light on calcification. These results suggest that future trends of CO 2 enrichment, sea-surface warming and exposure to higher mean irradiances from intensified stratification will have a large influence on the growth of Emiliania huxleyi, and potentially on the PIC/POC 'rain ratio'. Our study demonstrates that it is possible to obtain a more complete picture of global change impacts on marine phytoplankton by designing experiments that consider multiple global change variables and their mutual interactions.
Bleaching of reef corals is a phenomenon linked to temperature stress which involves loss of the symbiotic algae of the coral, which are known as zooxanthellae, and/or loss of algal pigments. The photosynthetic efficiency of zooxanthellae within the corals Montastrea annularis, Agaricia lamarki, Agaricia agaricites and Siderastrea radians was examined by pulse‐amplitude modulation fluorometry (PAM) during exposure to elevated temperatures (30–36°C). Zooxanthellae within M. annularis and A. lamarki were found to be more sensitive to elevated temperature, virtually complete disruption of photosynthesis being noted during exposure to temperatures of 32 and 34°C. The photosynthetic efficiency of zooxanthellae within S. radians and A. agaricites decreased to a lesser extent. Differences in the loss of algal cells on an aerial basis and in the cellular chlorophyll concentration were also found between these species. By combining the non‐invasive PAM technique with whole‐cell fluorescence of freshly isolated zooxanthellae, we have identified fundamental differences in the physiology of the symbionts within different species of coral. Zooxanthellae within M. annularis appear to be more susceptible to heat‐induced damage at or near the reaction centre of Photosystem II, while zooxanthellae living in S. radians remain capable of dissipating excess excitation energy through non‐photochemical pathways, thereby protecting the photosystem from damage during heat exposure.
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