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Journal ArticleDOI

Excess algal symbionts increase the susceptibility of reef corals to bleaching

01 Mar 2013-Nature Climate Change (Nature Publishing Group)-Vol. 3, Iss: 3, pp 259-262
TL;DR: This paper showed that corals with high symbiont cell densities are more susceptible to bleaching, indicating that environmental conditions which increase symbionts densities could exacerbate climate-induced coral bleaching.
Abstract: Understanding the factors that influence coral susceptibility to thermally induced bleaching may aid reef management efforts. Now corals with high symbiont cell densities are shown to be more susceptible to bleaching, indicating that environmental conditions which increase symbiont densities—such as nutrient pollution—could exacerbate climate-induced coral bleaching.
Citations
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Journal ArticleDOI
TL;DR: Experimental evidence that chronic nutrient exposure leads to increases in both disease prevalence and severity and coral bleaching in scleractinian corals, the major habitat-forming organisms in tropical reefs is presented and simple improvements to water quality may be an effective way to mitigate some coral disease epizootics and the corresponding loss of coral cover in the future.
Abstract: Nutrient loading is one of the strongest drivers of marine habitat degradation. Yet, the link between nutrients and disease epizootics in marine organisms is often tenuous and supported only by correlative data. Here, we present experimental evidence that chronic nutrient exposure leads to increases in both disease prevalence and severity and coral bleaching in scleractinian corals, the major habitat-forming organisms in tropical reefs. Over 3 years, from June 2009 to June 2012, we continuously exposed areas of a coral reef to elevated levels of nitrogen and phosphorus. At the termination of the enrichment, we surveyed over 1200 scleractinian corals for signs of disease or bleaching. Siderastrea siderea corals within enrichment plots had a twofold increase in both the prevalence and severity of disease compared with corals in unenriched control plots. In addition, elevated nutrient loading increased coral bleaching; Agaricia spp. of corals exposed to nutrients suffered a 3.5-fold increase in bleaching frequency relative to control corals, providing empirical support for a hypothesized link between nutrient loading and bleaching-induced coral declines. However, 1 year later, after nutrient enrichment had been terminated for 10 months, there were no differences in coral disease or coral bleaching prevalence between the previously enriched and control treatments. Given that our experimental enrichments were well within the ranges of ambient nutrient concentrations found on many degraded reefs worldwide, these data provide strong empirical support to the idea that coastal nutrient loading is one of the major factors contributing to the increasing levels of both coral disease and coral bleaching. Yet, these data also suggest that simple improvements to water quality may be an effective way to mitigate some coral disease epizootics and the corresponding loss of coral cover in the future.

402 citations


Cites background from "Excess algal symbionts increase the..."

  • ...For example, Cunning & Baker (2012) used lab experiments to show that increased Symbiodinium density in corals results in higher susceptibility to bleaching....

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  • ...…corals’ susceptibility to bleaching as elevated nutrient availability may increase abundance of algal symbionts (Marubini & Davies, 1996), which may make corals more susceptible to bleaching when sea surface temperatures rise (Wooldridge, 2009b; Cunning & Baker, 2012; Wiedenmann et al., 2012)....

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Journal ArticleDOI
TL;DR: In this article, the authors integrate direct and indirect effects of nutrient enrichment on corals in a model that explains why healthy coral reefs can exist over a rather broad range of natural nutrient environments at the lower end of the concentration scale and that anthropogenic nutrient enrichment can disturb the finely balanced processes via multiple pathways.

341 citations

Journal ArticleDOI
TL;DR: Investigating the role of diverse and mutable symbiotic partnerships in increasing corals' ability to thrive in high temperature conditions indicates that increased thermotolerance post-bleaching resulted from symbiont community composition changes, not prior heat exposure.
Abstract: Mutualistic organisms can be particularly susceptible to climate change stress, as their survivorship is often limited by the most vulnerable partner However, symbiotic plasticity can also help organisms in changing environments by expanding their realized niche space Coral–algal (Symbiodinium spp) symbiosis exemplifies this dichotomy: the partnership is highly susceptible to ‘bleaching’ (stress-induced symbiosis breakdown), but stress-tolerant symbionts can also sometimes mitigate bleaching Here, we investigate the role of diverse and mutable symbiotic partnerships in increasing corals' ability to thrive in high temperature conditions We conducted repeat bleaching and recovery experiments on the coral Montastraea cavernosa, and used quantitative PCR and chlorophyll fluorometry to assess the structure and function of Symbiodinium communities within coral hosts During an initial heat exposure (32 °C for 10 days), corals hosting only stress-sensitive symbionts (Symbiodinium C3) bleached, but recovered (at either 24 °C or 29 °C) with predominantly (>90%) stress-tolerant symbionts (Symbiodinium D1a), which were not detected before bleaching (either due to absence or extreme low abundance) When a second heat stress (also 32 °C for 10 days) was applied 3 months later, corals that previously bleached and were now dominated by D1a Symbiodinium experienced less photodamage and symbiont loss compared to control corals that had not been previously bleached, and were therefore still dominated by Symbiodinium C3 Additional corals that were initially bleached without heat by a herbicide (DCMU, at 24 °C) also recovered predominantly with D1a symbionts, and similarly lost fewer symbionts during subsequent thermal stress Increased thermotolerance was also not observed in C3-dominated corals that were acclimated for 3 months to warmer temperatures (29 °C) before heat stress These findings indicate that increased thermotolerance post-bleaching resulted from symbiont community composition changes, not prior heat exposure Moreover, initially undetectable D1a symbionts became dominant only after bleaching, and were critical to corals' resilience after stress and resistance to future stress

250 citations


Cites background or methods from "Excess algal symbionts increase the..."

  • ...…calculating absolute numbers of symbiont cells per host cell, e.g. Mieog et al., © 2014 John Wiley & Sons Ltd, Global Change Biology, 21, 236–249 2009; Cunning & Baker, 2013, is not necessary for the analyses presented here, as we compare only relative changes in symbiont abundance over time…...

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  • ...In both heat and DCMU treatments, corals with higher initial symbiont abundances lost a greater proportion of their symbiont communities during stress (Cunning & Baker, 2013)....

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  • ...Clade-specific assays for clade C and clade D symbionts were performed following the methods of (Cunning & Baker, 2013), modified for 10 ll reaction volumes....

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Book ChapterDOI
01 Jan 2015
TL;DR: In this chapter, ecological and physiological aspects of the interactions between corals and their symbiotic algae are reviewed in light of recent advances in knowledge of the diversity of these symbionts and cost-benefit analysis is suggested.
Abstract: The mutualistic relationship between corals and their dinoflagellate endosymbionts is a key factor in the evolutionary success of hermatypic (reef building) corals. The endosymbiotic algae benefit corals in numerous ways that have contributed to the long term persistence of coral reefs over geologic time. In this chapter we review ecological and physiological aspects of the interactions between corals and their symbiotic algae in light of recent advances in our knowledge of the diversity of these symbionts. While the role of symbiont diversity in promoting coral survival during environmental bleaching events has been a major focus of recent research, its importance in other physiological and ecological contexts such as inorganic nutrient dynamics and photosynthetic carbon fluxes has received much less attention. We suggest that cost-benefit analysis is a useful approach to examine these symbioses in the context of environmental change and human impacts upon corals and coral reefs. Weighing the costs versus the benefits of the symbiotic association under specific environmental perturbations has potential for use as an indicator of the health of not only corals but indeed the whole coral reef ecosystem. Drastic changes in the stability of the symbiosis, evidenced by changes in the ratio of zooxanthellae to animal biomass in corals, may turn out to be a useful diagnostic indicator of stresses to coral reefs. By using new tools developed to assess the stability of the symbiosis, we may be better able to understand and predict the effects of future stressors and perturbations that threaten these beautiful reef ecosystems.

236 citations

Journal ArticleDOI
TL;DR: This review examines the photobiology of the coral–algal symbiosis with particular focus on the photophysiological responses and timescales of corals and Symbiodinium, and summarizes the light environment and its dynamics, the vulnerability of the symbiosis to oxidative stress, the abiotic and biotic factors influencing photosynthesis, the diversity of the reef, and recent advances in the field.
Abstract: Coral reef ecosystems thrive in tropical oligotrophic oceans because of the relationship between corals and endosymbiotic dinoflagellate algae called Symbiodinium. Symbiodinium convert sunlight and carbon dioxide into organic carbon and oxygen to fuel coral growth and calcification, creating habitat for these diverse and productive ecosystems. Light is thus a key regulating factor shaping the productivity, physiology and ecology of the coral holobiont. Similar to all oxygenic photoautotrophs, Symbiodinium must safely harvest sunlight for photosynthesis and dissipate excess energy to prevent oxidative stress. Oxidative stress is caused by environmental stressors such as those associated with global climate change, and ultimately leads to breakdown of the coral-algal symbiosis known as coral bleaching. Recently, large-scale coral bleaching events have become pervasive and frequent threatening and endangering coral reefs. Because the coral-algal symbiosis is the biological engine producing the reef, the future of coral reef ecosystems depends on the ecophysiology of the symbiosis. This review examines the photobiology of the coral-algal symbiosis with particular focus on the photophysiological responses and timescales of corals and Symbiodinium. Additionally, this review summarizes the light environment and its dynamics, the vulnerability of the symbiosis to oxidative stress, the abiotic and biotic factors influencing photosynthesis, the diversity of the coral-algal symbiosis and recent advances in the field. Studies integrating physiology with the developing “omics” fields will provide new insights into the coral-algal symbiosis. Greater physiological and ecological understanding of the coral-algal symbiosis is needed for protection and conservation of coral reefs.

228 citations


Cites background from "Excess algal symbionts increase the..."

  • ...…implicated in increasing the susceptibility of corals to bleaching because of the higher ROS production relative to corals’ antioxidant capacity (Cunning and Baker, 2013); however, high densities of Symbiodinium also result in significant self-shading, lower rates of oxygen evolution, and…...

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References
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Journal ArticleDOI
14 Dec 2007-Science
TL;DR: As the International Year of the Reef 2008 begins, scaled-up management intervention and decisive action on global emissions are required if the loss of coral-dominated ecosystems is to be avoided.
Abstract: Atmospheric carbon dioxide concentration is expected to exceed 500 parts per million and global temperatures to rise by at least 2 degrees C by 2050 to 2100, values that significantly exceed those of at least the past 420,000 years during which most extant marine organisms evolved. Under conditions expected in the 21st century, global warming and ocean acidification will compromise carbonate accretion, with corals becoming increasingly rare on reef systems. The result will be less diverse reef communities and carbonate reef structures that fail to be maintained. Climate change also exacerbates local stresses from declining water quality and overexploitation of key species, driving reefs increasingly toward the tipping point for functional collapse. This review presents future scenarios for coral reefs that predict increasingly serious consequences for reef-associated fisheries, tourism, coastal protection, and people. As the International Year of the Reef 2008 begins, scaled-up management intervention and decisive action on global emissions are required if the loss of coral-dominated ecosystems is to be avoided.

4,422 citations

Journal ArticleDOI
TL;DR: This paper reviews and evaluates the current state of knowledge on the direct effects of terrestrial runoff on hard coral colonies, coral reproduction and recruitment, and organisms that interact with coral populations and summarises geographic and biological factors that determine local and regional levels of resistance and resilience to degradation.

1,913 citations

Journal ArticleDOI
TL;DR: The short- and long-term ecological impacts of coral bleaching on reef ecosystems are reviewed, and recovery data worldwide is quantitatively synthesized to maintain ecosystem resilience by restoring healthy levels of herbivory, macroalgal cover, and coral recruitment.
Abstract: Since the early 1980s, episodes of coral reef bleaching and mortality, due primarily to climate-induced ocean warming, have occurred almost annually in one or more of the world's tropical or subtropical seas. Bleaching is episodic, with the most severe events typically accompanying coupled ocean–atmosphere phenomena, such as the El Nino-Southern Oscillation (ENSO), which result in sustained regional elevations of ocean temperature. Using this extended dataset (25+ years), we review the short- and long-term ecological impacts of coral bleaching on reef ecosystems, and quantitatively synthesize recovery data worldwide. Bleaching episodes have resulted in catastrophic loss of coral cover in some locations, and have changed coral community structure in many others, with a potentially critical influence on the maintenance of biodiversity in the marine tropics. Bleaching has also set the stage for other declines in reef health, such as increases in coral diseases, the breakdown of reef framework by bioeroders, and the loss of critical habitat for associated reef fishes and other biota. Secondary ecological effects, such as the concentration of predators on remnant surviving coral populations, have also accelerated the pace of decline in some areas. Although bleaching severity and recovery have been variable across all spatial scales, some reefs have experienced relatively rapid recovery from severe bleaching impacts. There has been a significant overall recovery of coral cover in the Indian Ocean, where many reefs were devastated by a single large bleaching event in 1998. In contrast, coral cover on western Atlantic reefs has generally continued to decline in response to multiple smaller bleaching events and a diverse set of chronic secondary stressors. No clear trends are apparent in the eastern Pacific, the central-southern-western Pacific or the Arabian Gulf, where some reefs are recovering and others are not. The majority of survivors and new recruits on regenerating and recovering coral reefs have originated from broadcast spawning taxa with a potential for asexual growth, relatively long distance dispersal, successful settlement, rapid growth and a capacity for framework construction. Whether or not affected reefs can continue to function as before will depend on: (1) how much coral cover is lost, and which species are locally extirpated; (2) the ability of remnant and recovering coral communities to adapt or acclimatize to higher temperatures and other climatic factors such as reductions in aragonite saturation state; (3) the changing balance between reef accumulation and bioerosion; and (4) our ability to maintain ecosystem resilience by restoring healthy levels of herbivory, macroalgal cover, and coral recruitment. Bleaching disturbances are likely to become a chronic stress in many reef areas in the coming decades, and coral communities, if they cannot recover quickly enough, are likely to be reduced to their most hardy or adaptable constituents. Some degraded reefs may already be approaching this ecological asymptote, although to date there have not been any global extinctions of individual coral species as a result of bleaching events. Since human populations inhabiting tropical coastal areas derive great value from coral reefs, the degradation of these ecosystems as a result of coral bleaching and its associated impacts is of considerable societal, as well as biological concern. Coral reef conservation strategies now recognize climate change as a principal threat, and are engaged in efforts to allocate conservation activity according to geographic-, taxonomic-, and habitat-specific priorities to maximize coral reef survival. Efforts to forecast and monitor bleaching, involving both remote sensed observations and coupled ocean–atmosphere climate models, are also underway. In addition to these efforts, attempts to minimize and mitigate bleaching impacts on reefs are immediately required. If significant reductions in greenhouse gas emissions can be achieved within the next two to three decades, maximizing coral survivorship during this time may be critical to ensuring healthy reefs can recover in the long term.

1,098 citations

Journal ArticleDOI
TL;DR: It is shown that adult corals, at least in some circumstances, are capable of acquiring increased thermal tolerance and that the increased tolerance is a direct result of a change in the symbiont type dominating their tissues from Symbiodinium type C to D.
Abstract: The ability of coral reefs to survive the projected increases in temperature due to global warming will depend largely on the ability of corals to adapt or acclimatize to increased temperature extr...

1,047 citations

Journal ArticleDOI
Rob Rowan1
12 Aug 2004-Nature
TL;DR: It is shown that some corals have adapted to higher temperatures, at least in part, by hosting specifically adapted Symbiodinium, which might help them adapt to warmer habitats relatively easily.
Abstract: Many corals bleach as a result of increased seawater temperature, which causes them to lose their vital symbiotic algae (Symbiodinium spp.) - unless these symbioses are able to adapt to global warming, bleaching threatens coral reefs worldwide. Here I show that some corals have adapted to higher temperatures, at least in part, by hosting specifically adapted Symbiodinium. If other coral species can host these or similar Symbiodinium taxa, they might adapt to warmer habitats relatively easily.

636 citations