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1.
The juxtaposition of highly productive coral reef ecosystems in oligotrophic waters has spurred substantial interest and progress in our understanding of macronutrient uptake, exchange, and recycling among coral holobiont partners (host coral, dinoflagellate endosymbiont, endolithic algae, fungi, viruses, bacterial communities). By contrast, the contribution of trace metals to the physiological performance of the coral holobiont and, in turn, the functional ecology of reef-building corals remains unclear. The coral holobiont's trace metal economy is a network of supply, demand, and exchanges upheld by cross-kingdom symbiotic partnerships. Each partner has unique trace metal requirements that are central to their biochemical functions and the metabolic stability of the holobiont. Organismal homeostasis and the exchanges among partners determine the ability of the coral holobiont to adjust to fluctuating trace metal supplies in heterogeneous reef environments. This review details the requirements for trace metals in core biological processes and describes how metal exchanges among holobiont partners are key to sustaining complex nutritional symbioses in oligotrophic environments. Specifically, we discuss how trace metals contribute to partner compatibility, ability to cope with stress, and thereby to organismal fitness and distribution. Beyond holobiont trace metal cycling, we outline how the dynamic nature of the availability of environmental trace metal supplies can be influenced by a variability of abiotic factors (e.g. temperature, light, pH, etc.). Climate change will have profound consequences on the availability of trace metals and further intensify the myriad stressors that influence coral survival. Lastly, we suggest future research directions necessary for understanding the impacts of trace metals on the coral holobiont symbioses spanning subcellular to organismal levels, which will inform nutrient cycling in coral ecosystems more broadly. Collectively, this cross-scale elucidation of the role of trace metals for the coral holobiont will allow us to improve forecasts of future coral reef function.  相似文献   

2.
Improving coral reef conservation requires heightened understanding of the mechanisms by which coral cope with changing environmental conditions to maintain optimal health. We used a long‐term (10 month) in situ experiment with two phylogenetically diverse scleractinians (Acropora palmata and Porites porites) to test how coral–symbiotic algal interactions changed under real‐world conditions that were a priori expected to be beneficial (fish‐mediated nutrients) and to be harmful, but non‐lethal, for coral (fish + anthropogenic nutrients). Analyzing nine response variables of nutrient stoichiometry and stable isotopes per coral fragment, we found that nutrients from fish positively affected coral growth, and moderate doses of anthropogenic nutrients had no additional effects. While growing, coral maintained homeostasis in their nutrient pools, showing tolerance to the different nutrient regimes. Nonetheless, structural equation models revealed more nuanced relationships, showing that anthropogenic nutrients reduced the diversity of coral–symbiotic algal interactions and caused nutrient and carbon flow to be dominated by the symbiont. Our findings show that nutrient and carbon pathways are fundamentally “rewired” under anthropogenic nutrient regimes in ways that could increase corals’ susceptibility to further stressors. We hypothesize that our experiment captured coral in a previously unrecognized transition state between mutualism and antagonism. These findings highlight a notable parallel between how anthropogenic nutrients promote symbiont dominance with the holobiont, and how they promote macroalgal dominance at the coral reef scale. Our findings suggest more realistic experimental conditions, including studies across gradients of anthropogenic nutrient enrichment as well as the incorporation of varied nutrient and energy pathways, may facilitate conservation efforts to mitigate coral loss.  相似文献   

3.
The productivity of coral reefs in oligotrophic tropical waters is sustained by an efficient uptake and recycling of nutrients. In reef‐building corals, the engineers of these ecosystems, this nutrient recycling is facilitated by a constant exchange of nutrients between the animal host and endosymbiotic photosynthetic dinoflagellates (zooxanthellae), bacteria, and other microbes. Due to the complex interactions in this so‐called coral holobiont, it has proven difficult to understand the environmental limitations of productivity in corals. Among others, the micronutrient iron has been proposed to limit primary productivity due to its essential role in photosynthesis and bacterial processes. Here, we tested the effect of iron enrichment on the physiology of the coral Pocillopora verrucosa from the central Red Sea during a 12‐day experiment. Contrary to previous reports, we did not see an increase in zooxanthellae population density or gross photosynthesis. Conversely, respiration rates were significantly increased, and microbial nitrogen fixation was significantly decreased. Taken together, our data suggest that iron is not a limiting factor of primary productivity in Red Sea corals. Rather, increased metabolic demands in response to iron enrichment, as evidenced by increased respiration rates, may reduce carbon (i.e., energy) availability in the coral holobiont, resulting in reduced microbial nitrogen fixation. This decrease in nitrogen supply in turn may exacerbate the limitation of other nutrients, creating a negative feedback loop. Thereby, our results highlight that the effects of iron enrichment appear to be strongly dependent on local environmental conditions and ultimately may depend on the availability of other nutrients.  相似文献   

4.
Anthropogenic increases in atmospheric carbon dioxide concentration have caused global average sea surface temperature (SST) to increase by approximately 0.11°C per decade between 1971 and 2010 – a trend that is projected to continue through the 21st century. A multitude of research studies have demonstrated that increased SSTs compromise the coral holobiont (cnidarian host and its symbiotic algae) by reducing both host calcification and symbiont density, among other variables. However, we still do not fully understand the role of heterotrophy in the response of the coral holobiont to elevated temperature, particularly for temperate corals. Here, we conducted a pair of independent experiments to investigate the influence of heterotrophy on the response of the temperate scleractinian coral Oculina arbuscula to thermal stress. Colonies of O. arbuscula from Radio Island, North Carolina, were exposed to four feeding treatments (zero, low, moderate, and high concentrations of newly hatched Artemia sp. nauplii) across two independent temperature experiments (average annual SST (20°C) and average summer temperature (28°C) for the interval 2005–2012) to quantify the effects of heterotrophy on coral skeletal growth and symbiont density. Results suggest that heterotrophy mitigated both reduced skeletal growth and decreased symbiont density observed for unfed corals reared at 28°C. This study highlights the importance of heterotrophy in maintaining coral holobiont fitness under thermal stress and has important implications for the interpretation of coral response to climate change.  相似文献   

5.
Indo‐Pacific reef corals growing for years in closed‐system aquaria provide an alternate means to investigate host–symbiont specificity and stability. The diversity of dinoflagellate endosymbionts (Symbiodinium spp.) from coral communities in private and public aquaria was investigated using molecular‐genetic analyses. Of the 29 symbiont types (i.e., species) identified, 90% belonged to the most prevalent group of Symbiodinium harbored by Indo‐Pacific reef corals, Clade C, while the rest belonged to Clade D. Sixty‐five percent of all types were known from field surveys conducted throughout the Pacific and Indian oceans. Because specific coral–dinoflagellate partnerships appear to have defined geographic distributions, correspondence of the same symbionts in aquarium and field‐collected specimens identifies regions where particular colonies must have been collected in the wild. Symbiodinium spp. in clade D, believed to be “stress‐tolerant” and/or “opportunistic,” occurred in a limited number of individual colonies. The absence of a prevalent, or “weedy,” symbiont suggests that conditions under which aquarium corals are grown do not favor competitive replacements of their native symbiont populations. The finding of typical and diverse assemblages of Symbiodinium spp. among aquarium corals living many years under variable chemical/physical conditions, artificial and natural light, while undergoing fragmentation periodically, indicates that individual colonies maintain stable, long‐term symbiotic associations.  相似文献   

6.
In preparation for a large-scale coral restoration project, we surveyed host population genetic structure and symbiont diversity of two reef-building corals in four reef zones along the Florida reef tract (FRT). There was no evidence for coral population subdivision along the FRT in Acropora cervicornis or Montastraea faveolata based on microsatellite markers. However, in A. cervicornis, significant genetic differentiation was apparent when extending the analysis to broader scales (Caribbean). Clade diversity of the zooxanthellae differed along the FRT. A. cervicornis harbored mostly clade A with clade D zooxanthellae being prominent in colonies growing inshore and in the mid-channel zones that experience greater temperature fluctuations and receive significant nutrient and sediment input. M. faveolata harbored a more diverse array of symbionts, and variation in symbiont diversity among four habitat zones was more subtle but still significant. Implications of these results are discussed for ongoing restoration and conservation work.  相似文献   

7.
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.  相似文献   

8.
Despite recent advances in identifying the causative agents of disease in corals and understanding the impact of epizootics on reef communities, little is known regarding the interactions among diseases, corals, and their dinoflagellate endosymbionts (Symbiodinium spp.). Since the genotypes of both corals and their resident Symbiodinium contribute to colony-level phenotypes, such as thermotolerance, symbiont genotypes might also contribute to the resistance or susceptibility of coral colonies to disease. To explore this, Symbiodinium were identified using the internal transcribed spacer-2 region of ribosomal DNA from diseased and healthy tissues within individual coral colonies infected with black band disease (BB), dark spot syndrome (DSS), white plague disease (WP), or yellow blotch disease (YB) in the Florida Keys (USA) and the US Virgin Islands. Most of the diseased colonies sampled contained B1, B5a, or C1 (depending on host species), while apparently healthy colonies of the same coral species frequently hosted these types and/or additional symbiont diversity. No potentially “parasitic” Symbiodinium types, uniquely associated with diseased coral tissue, were detected. Within most individual colonies, the same dominant Symbiodinium type was detected in diseased and visually healthy tissues. These data indicate that specific Symbiodinium types are not correlated with the infected tissues of diseased colonies and that DSS and WP onset do not trigger symbiont shuffling within infected tissues. However, few diseased colonies contained clade D symbionts suggesting a negative correlation between hosting Symbiodinium clade D and disease incidence in scleractinian corals. Understanding the influence of Symbiodinium diversity on colony phenotypes may play a critical role in predicting disease resistance and susceptibility in scleractinian corals.  相似文献   

9.
Yu  Xiaopeng  Yu  Kefu  Chen  Biao  Liao  Zhiheng  Liang  Jiayuan  Yao  Qiucui  Qin  Zhenjun  Wang  Hao  Yu  Jiaoyang 《Coral reefs (Online)》2021,40(6):1697-1711

Ecological surveys observe coral “winners” and “losers” in global coral bleaching events. However, the key contributors to holobiont tolerance and interactions between symbionts remain unclear. Herein, we compared bleaching and unbleaching Acropora pruinosa corals from Weizhou Island, during an extreme high-temperature event in the northern South China Sea in 2020. We found the dominant Symbiodiniaceae subclade in the bleaching and unbleaching corals to be C1; however, the density of Symbiodiniaceae in the latter was significantly higher than that in the former. Additionally, the symbiotic bacteria α diversity in the unbleaching coral was significantly higher than that in the bleaching coral, with a reorganized bacterial community structure. Core microbiome analyses revealed 55 bacterial core operational taxonomic units (OTUs), of which 10 were significantly differentially enriched between the two coral groups. The significantly enriched bacterial core OTUs in the unbleaching coral were primarily nitrogen cycling related, while those enriched in the bleaching coral were associated with antimicrobial activity. RNA-Seq analyses revealed that significantly upregulated genes in the bleaching coral were primarily associated with diseases and autophagy, while those in the unbleaching coral were associated with immune defense and maintenance of the symbiotic relationship between corals and symbionts. We propose that the differences in tolerance of A. pruinosa result from the cooperation between coral host, Symbiodiniaceae, and symbiotic bacteria. In extreme high-temperature events, unbleaching corals may maintain stable symbiotic relationships by increasing the diversity of symbiotic bacteria, regulating the structure of the symbiotic bacteria community, improving the interaction between coral host and symbiont and enhancing host immunity, thus avoiding coral bleaching. This study illuminates the relationship between the coral symbiont and tolerance differences of coral holobionts, providing new insights for further exploration into the adaptability of scleractinian corals in the context of global warming.

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10.
By the century's end, many tropical seas will reach temperatures exceeding most coral species' thermal tolerance on an annual basis. The persistence of corals in these regions will, therefore, depend on their abilities to tolerate recurrent thermal stress. Although ecologists have long recognized that positive interspecific interactions can ameliorate environmental stress to expand the realized niche of plants and animals, coral bleaching studies have largely overlooked how interactions with community members outside of the coral holobiont shape the bleaching response. Here, we subjected a common coral, Pocillopora grandis, to 10 days of thermal stress in aquaria with and without the damselfish Dascyllus flavicaudus (yellowtail dascyllus), which commonly shelter within these corals, to examine how interactions with damselfish impacted coral thermal tolerance. Corals often benefit from nutrients excreted by animals they interact with and prior to thermal stress, corals grown with damselfish showed improved photophysiology (Fv/Fm) and developed larger endosymbiont populations. When exposed to thermal stress, corals with fish performed as well as control corals maintained at ambient temperatures without fish. In contrast, corals exposed to thermal stress without fish experienced photophysiological impairment, a more than 50% decline in endosymbiont density, and a 36% decrease in tissue protein content. At the end of the experiment, thermal stress caused average calcification rates to decrease by over 80% when damselfish were absent but increase nearly 25% when damselfish were present. Our study indicates that damselfish-derived nutrients can increase coral thermal tolerance and are consistent with the Stress Gradient Hypothesis, which predicts that positive interactions become increasingly important for structuring communities as environmental stress increases. Because warming of just a few degrees can exceed corals' temperature tolerance to trigger bleaching and mortality, positive interactions could play a critical role in maintaining some coral species in warming regions until climate change is aggressively addressed.  相似文献   

11.
12.
Montastrea annularis, the major Caribbean reef building coral, was severely affected by the unprecedented 1987–1988 bleaching event. Most colonies on the fore reef were affected but few were bleached in the back reef. Skeletal growth rates of M. annularis populations were measured non-destructively in the field at Discovery Bay, Jamaica, from the peak of bleaching in Nov. 1987 until recovery was almost complete, in May 1988. Unbleached corals grew at normal rates. Partially bleached corals survived but skeletal growth ceased through this period.  相似文献   

13.
Tolerance of environmental variables differs between corals and their dinoflagellate symbionts (Symbiodinium spp.), controlling the holobiont’s (host and symbiont combined) resilience to environmental stress. However, the ecological role that environmental variables play in holobiont distribution remains poorly understood. We compared the drivers of symbiont and coral species distributions at Palmyra Atoll, a location with a range of reef environments from low to high sediment concentrations (1–52 g dry weight m−2 day−1). We observed uniform holobiont partnerships across the atoll (e.g. Montipora spp. with Symbiodinium type C15 at all sites). Multivariate analysis revealed that field-based estimates of settling sediment predominantly explained the spatial variation of coral species among sites (P < 0.01). However, none of the environmental variables measured (sedimentation, temperature, chlorophyll concentration, salinity) affected symbiont distribution. The discord between environmental variables and symbiont distributions suggests that the symbionts are physiologically tolerant of the variable environmental regime across this location and that the distribution of different host–symbiont combinations present is largely dependent on coral rather than Symbiodinium physiology. The data highlight the importance of host tolerance to environmental stressors, which should be considered simultaneously with symbiont sensitivity when considering the impact of variations in environmental conditions on coral communities.  相似文献   

14.
The symbiosis between reef-building corals and their algal endosymbionts (zooxanthellae of the genus Symbiodinium) is highly sensitive to temperature stress, which makes coral reefs vulnerable to climate change. Thermal tolerance in corals is known to be substantially linked to the type of zooxanthellae they harbour and, when multiple types are present, the relative abundance of types can be experimentally manipulated to increase the thermal limits of individual corals. Although the potential exists for this to translate into substantial thermal acclimatization of coral communities, to date there is no evidence to show that this takes place under natural conditions. In this study, we show field evidence of a dramatic change in the symbiont community of Acropora millepora, a common and widespread Indo-Pacific hard coral species, after a natural bleaching event in early 2006 in the Keppel Islands (Great Barrier Reef). Before bleaching, 93.5% (n=460) of the randomly sampled and tagged colonies predominantly harboured the thermally sensitive Symbiodinium type C2, while the remainder harboured a tolerant Symbiodinium type belonging to clade D or mixtures of C2 and D. After bleaching, 71% of the surviving tagged colonies that were initially C2 predominant changed to D or C1 predominance. Colonies that were originally C2 predominant suffered high mortality (37%) compared with D-predominant colonies (8%). We estimate that just over 18% of the original A. millepora population survived unchanged leaving 29% of the population C2 and 71% D or C1 predominant six months after the bleaching event. This change in the symbiont community structure, while it persists, is likely to have substantially increased the thermal tolerance of this coral population. Understanding the processes that underpin the temporal changes in symbiont communities is key to assessing the acclimatization potential of reef corals.  相似文献   

15.
Scleractinian corals are assumed to be stenohaline osmoconformers, although they are frequently subjected to variations in seawater salinity due to precipitation, freshwater run‐off and other processes. Observed responses to altered salinity levels include differences in photosynthetic performance, respiration and increased bleaching and mortality of the coral host and its algal symbiont, but a study looking at bacterial community changes is lacking. Here, we exposed the coral Fungia granulosa to strongly increased salinity levels in short‐ and long‐term experiments to disentangle temporal and compartment effects of the coral holobiont (i.e. coral host, symbiotic algae and associated bacteria). Our results show a significant reduction in calcification and photosynthesis, but a stable microbiome after short‐term exposure to high‐salinity levels. By comparison, long‐term exposure yielded unchanged photosynthesis levels and visually healthy coral colonies indicating long‐term acclimation to high‐salinity levels that were accompanied by a major coral microbiome restructuring. Importantly, a bacterium in the family Rhodobacteraceae was succeeded by Pseudomonas veronii as the numerically most abundant taxon. Further, taxonomy‐based functional profiling indicates a shift in the bacterial community towards increased osmolyte production, sulphur oxidation and nitrogen fixation. Our study highlights that bacterial community composition in corals can change within days to weeks under altered environmental conditions, where shifts in the microbiome may enable adjustment of the coral to a more advantageous holobiont composition.  相似文献   

16.
Infectious diseases are recognized as significant contributors to the dramatic loss of corals observed worldwide. However, the causes of increased coral disease prevalence and severity are not well understood. One potential factor is elevated nutrient concentration related to localized anthropogenic activities such as inadequate waste water treatment or terrestrial runoff. In this study the effect of nutrient enrichment on the progression of black band disease (BBD) was investigated using both in situ and laboratory experiments. Experimental increases in localized nutrient availability using commercial time release fertilizer in situ resulted in doubling of BBD progression and coral tissue loss in the common reef framework coral Siderastrea siderea. Laboratory experiments in which artificially infected S. siderea colonies were exposed to increased nitrate concentrations (up to 3 μM) demonstrated similar increases in BBD progression. These findings provide evidence that the impacts of this disease on coral populations are exacerbated by nutrient enrichment and that management to curtail excess nutrient loading may be important for reducing coral cover loss due to BBD.  相似文献   

17.
The mutualistic symbioses between reef‐building corals and micro‐algae form the basis of coral reef ecosystems, yet recent environmental changes threaten their survival. Diversity in host‐symbiont pairings on the sub‐species level could be an unrecognized source of functional variation in response to stress. The Caribbean elkhorn coral, Acropora palmata, associates predominantly with one symbiont species (Symbiodiniumfitti’), facilitating investigations of individual‐level (genotype) interactions. Individual genotypes of both host and symbiont were resolved across the entire species’ range. Most colonies of a particular animal genotype were dominated by one symbiont genotype (or strain) that may persist in the host for decades or more. While Symbiodinium are primarily clonal, the occurrence of recombinant genotypes indicates sexual recombination is the source of this genetic variation, and some evidence suggests this happens within the host. When these data are examined at spatial scales spanning the entire distribution of A. palmata, gene flow among animal populations was an order of magnitude greater than among populations of the symbiont. This suggests that independent micro‐evolutionary processes created dissimilar population genetic structures between host and symbiont. The lower effective dispersal exhibited by the dinoflagellate raises questions regarding the extent to which populations of host and symbiont can co‐evolve during times of rapid and substantial climate change. However, these findings also support a growing body of evidence, suggesting that genotype‐by‐genotype interactions may provide significant physiological variation, influencing the adaptive potential of symbiotic reef corals to severe selection.  相似文献   

18.

Some reef corals form stable, dominant or codominant associations with multiple endosymbiotic dinoflagellate species (family Symbiodiniaceae). Given the immense genetic and physiological diversity within this family, Symbiodiniaceae community composition has the potential to impact the nutritional physiology and fitness of the cnidarian host and all associated symbionts. Here we assessed the impact of the symbiont community composition on the metabolome of the coral Montipora capitata in Kāne‘ohe Bay, Hawai‘i, where different colonies can be dominated by stress-tolerant Durusdinium glynnii or stress-sensitive Cladocopium spp. Based on our existing knowledge of these symbiont taxa, we hypothesised that the metabolite profile of D. glynnii-dominated corals would be consistent with poorer nutritional support of the host relative to those corals dominated by Cladocopium spp. However, comparative metabolite profiling revealed that the metabolite pools of the host and symbiont were unaffected by differences in the abundance of the two symbionts within the community. The abundance of the individual metabolites was the same in the host and in the endosymbiont regardless of whether the host was populated with D. glynnii or Cladocopium spp. These results suggest that coral-dinoflagellate symbioses have the potential to undergo physiological adjustments over time to accommodate differences in their resident symbionts. Such mechanisms may involve host heterotrophic compensation (increasing the level of nutrition generated by feeding relative to delivery from the algae), dynamic regulation of metabolic pathways when exchange of metabolites between the organisms differs, and/or modification of both the type and quantity of metabolites that are exchanged. We discuss these adjustments and the implications for the physiology and survival of reef corals under changing environmental regimes.

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19.
The degree to which coral reef ecosystems will be impacted by global climate change depends on regional and local differences in corals’ susceptibility and resilience to environmental stressors. Here, we present data from a reciprocal transplant experiment using the common reef building coral Porites lobata between a highly fluctuating back reef environment that reaches stressful daily extremes, and a more stable, neighbouring forereef. Protein biomarker analyses assessing physiological contributions to stress resistance showed evidence for both fixed and environmental influence on biomarker response. Fixed influences were strongest for ubiquitin‐conjugated proteins with consistently higher levels found in back reef source colonies both pre and post‐transplant when compared with their forereef conspecifics. Additionally, genetic comparisons of back reef and forereef populations revealed significant population structure of both the nuclear ribosomal and mitochondrial genomes of the coral host (FST = 0.146 P < 0.0001, FST = 0.335 P < 0.0001 for rDNA and mtDNA, respectively), whereas algal endosymbiont populations were genetically indistinguishable between the two sites. We propose that the genotype of the coral host may drive limitations to the physiological responses of these corals when faced with new environmental conditions. This result is important in understanding genotypic and environmental interactions in the coral algal symbiosis and how corals may respond to future environmental changes.  相似文献   

20.
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