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1.
Repeat marine heat wave‐induced mass coral bleaching has decimated reefs in Seychelles for 35 years, but how coral‐associated microbial diversity (microalgal endosymbionts of the family Symbiodiniaceae and bacterial communities) potentially underpins broad‐scale bleaching dynamics remains unknown. We assessed microbiome composition during the 2016 heat wave peak at two contrasting reef sites (clear vs. turbid) in Seychelles, for key coral species considered bleaching sensitive (Acropora muricata, Acropora gemmifera) or tolerant (Porites lutea, Coelastrea aspera). For all species and sites, we sampled bleached versus unbleached colonies to examine how microbiomes align with heat stress susceptibility. Over 30% of all corals bleached in 2016, half of which were from Acropora sp. and Pocillopora sp. mass bleaching that largely transitioned to mortality by 2017. Symbiodiniaceae ITS2‐sequencing revealed that the two Acropora sp. and P. lutea generally associated with C3z/C3 and C15 types, respectively, whereas C. aspera exhibited a plastic association with multiple D types and two C3z types. 16S rRNA gene sequencing revealed that bacterial communities were coral host‐specific, largely through differences in the most abundant families, Hahellaceae (comprising Endozoicomonas), Rhodospirillaceae, and Rhodobacteraceae. Both Acropora sp. exhibited lower bacterial diversity, species richness, and community evenness compared to more bleaching‐resistant P. lutea and C. aspera. Different bleaching susceptibility among coral species was thus consistent with distinct microbiome community profiles. These profiles were conserved across bleached and unbleached colonies of all coral species. As this pattern could also reflect a parallel response of the microbiome to environmental changes, the detailed functional associations will need to be determined in future studies. Further understanding such microbiome‐environmental interactions is likely critical to target more effective management within oceanically isolated reefs of Seychelles.  相似文献   

2.
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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3.
Dinoflagellates of the family Symbiodiniaceae form mutualistic symbioses with marine invertebrates such as reef‐building corals, but also inhabit reef environments as free‐living cells. Most coral species acquire Symbiodiniaceae horizontally from the surrounding environment during the larval and/or recruitment phase, however the phylogenetic diversity and ecology of free‐living Symbiodiniaceae on coral reefs is largely unknown. We coupled environmental DNA sequencing and genus‐specific qPCR to resolve the community structure and cell abundances of free‐living Symbiodiniaceae in the water column, sediment, and macroalgae and compared these to coral symbionts. Sampling was conducted at two time points, one of which coincided with the annual coral spawning event when recombination between hosts and free‐living Symbiodiniaceae is assumed to be critical. Amplicons of the internal transcribed spacer (ITS2) region were assigned to 12 of the 15 Symbiodiniaceae genera or genera‐equivalent lineages. Community compositions were separated by habitat, with water samples containing a high proportion of sequences corresponding to coral symbionts of the genus Cladocopium, potentially as a result of cell expulsion from in hospite populations. Sediment‐associated Symbiodiniaceae communities were distinct, potentially due to the presence of exclusively free‐living species. Intriguingly, macroalgal surfaces displayed the highest cell abundances of Symbiodiniaceae, suggesting a key role for macroalgae in ensuring the ecological success of corals through maintenance of a continuum between environmental and symbiotic populations of Symbiodiniaceae.  相似文献   

4.
Symbiodiniaceae are a diverse family of marine dinoflagellates, well known as coral endosymbionts. Isolation and in vitro culture of Symbiodiniaceae strains for physiological studies is a widely adopted tool, especially in the context of understanding how environmental stress perturbs Symbiodiniaceae cell functioning. While the bacterial microbiomes of corals often correlate with coral health, the bacterial communities co-cultured with Symbiodiniaceae isolates have been largely overlooked, despite the potential of bacteria to significantly influence the emergent physiological properties of Symbiodiniaceae cultures. We examined the physiological response to heat stress by Symbiodiniaceae isolates (spanning three genera) with well-described thermal tolerances, and combined these observations with matched changes in bacterial composition and abundance through 16S rRNA metabarcoding. Under thermal stress, there were Symbiodiniaceae strain-specific changes in maximum quantum yield of photosystem II (proxy for health) and growth rates that were accompanied by changes in the relative abundance of multiple Symbiodiniaceae-specific bacteria. However, there were no Symbiodiniaceae-independent signatures of bacterial community reorganisation under heat stress. Notably, the thermally tolerant Durusdinium trenchii (ITS2 major profile D1a) had the most stable bacterial community under heat stress. Ultimately, this study highlights the complexity of Symbiodiniaceae-bacteria interactions and provides a first step towards uncoupling their relative contributions towards Symbiodiniaceae physiological functioning.  相似文献   

5.
《Genomics》2021,113(4):2717-2729
Corals live with complex assemblages of microbes including bacteria, the dinoflagellate Symbiodiniaceae, fungi and viruses in a coral holobiont. These coral-associated microorganisms play an important role in their host fitness and survival. Here, we investigated the structure and diversity of algal and bacterial communities associated with five Indo-Pacific coral species, using full-length 16S rRNA and internal transcribed spacer sequences. While the dinoflagellate communities associated with Porites lutea were dominated with Symbiodiniaceae genus Cladocopium, the other four coral hosts were associated mainly with members of the Durusdinium genus, suggesting that host species was one of the underlying factors influencing the structure and composition of dinoflagellate communities associated with corals in the Gulf of Thailand. Alphaproteobacteria dominated the microbiomes of Pocillopora spp. while Pavona frondifera and P. lutea were associated primarily with Gammaproteobacteria. Finally, we demonstrated a superior performance of full-length 16S rRNA sequences in achieving species-resolution taxonomic classification of coral-associated microbiota.  相似文献   

6.
Early establishment of coral–microbial symbioses is fundamental to the fitness of corals, but comparatively little is known about the onset and succession of bacterial communities in their early life history stages. In this study, bacterial associates of the coral Acropora millepora were characterized throughout the first year of life, from larvae and 1‐week‐old juveniles reared in laboratory conditions in the absence of the dinoflagellate endosymbiont Symbiodinium to field‐outplanted juveniles with established Symbiodinium symbioses, and sampled at 2 weeks and at 3, 6 and 12 months. Using an amplicon pyrosequencing approach, the diversity of both nitrogen‐fixing bacteria and of bacterial communities overall was assessed through analysis of nifH and 16S rRNA genes, respectively. The consistent presence of sequences affiliated with diazotrophs of the order Rhizobiales (23–58% of retrieved nifH sequences; 2–12% of 16S rRNA sequences), across all samples from larvae to 12‐month‐old coral juveniles, highlights the likely functional importance of this nitrogen‐fixing order to the coral holobiont. Dominance of Roseobacter‐affiliated sequences (>55% of retrieved 16S rRNA sequences) in larvae and 1‐week‐old juveniles, and the consistent presence of sequences related to Oceanospirillales and Altermonadales throughout all early life history stages, signifies their potential importance as coral associates. Increased diversity of bacterial communities once juveniles were transferred to the field, particularly of Cyanobacteria and Deltaproteobacteria, demonstrates horizontal (environmental) uptake of coral‐associated bacterial communities. Although overall bacterial communities were dynamic, bacteria with likely important functional roles remain stable throughout early life stages of Acropora millepora.  相似文献   

7.
Microbial associations with corals are common and are most likely symbiotic, although their diversity and relationships with environmental factors and host species remain unclear. In this study, we adopted a 16S rRNA gene tag-pyrosequencing technique to investigate the bacterial communities associated with three stony Scleractinea and two soft Octocorallia corals from three locations in the Red Sea. Our results revealed highly diverse bacterial communities in the Red Sea corals, with more than 600 ribotypes detected and up to 1,000 species estimated from a single coral species. Altogether, 21 bacterial phyla were recovered from the corals, of which Gammaproteobacteria was the most dominant group, and Chloroflexi, Chlamydiae, and the candidate phylum WS3 were reported in corals for the first time. The associated bacterial communities varied greatly with location, where environmental conditions differed significantly. Corals from disturbed areas appeared to share more similar bacterial communities, but larger variations in community structures were observed between different coral species from pristine waters. Ordination methods identified salinity and depth as the most influential parameters affecting the abundance of Vibrio, Pseudoalteromonas, Serratia, Stenotrophomonas, Pseudomonas, and Achromobacter in the corals. On the other hand, bacteria such as Chloracidobacterium and Endozoicomonas were more sensitive to the coral species, suggesting that the host species type may be influential in the associated bacterial community, as well. The combined influences of the coral host and environmental factors on the associated microbial communities are discussed. This study represents the first comparative study using tag-pyrosequencing technology to investigate the bacterial communities in Red Sea corals.  相似文献   

8.
Aim We examined data on corals and reef fishes to determine how particular local habitat types contribute to variation in community structure across regions covering gradients in species richness and how consistent this was over time. Location Great Barrier Reef (GBR), Australia. Methods We compared large‐scale (1300 km), long‐term (11 years) data on fishes and corals that were collected annually at fixed sites in three habitats (inshore, mid‐shelf and outer‐shelf reefs) and six regions (latitudinal sectors) along a gradient of regional species richness in both communities. We used canonical approaches to partition variation in community structure (sites × species abundance data matrices) into components associated with habitat, region and time and Procrustes analyses to assess the degree of concordance between coral and fish community structure. Results Remarkably similar patterns emerged for both fish and coral communities occupying the same sites. Reefs that had similar coral communities also had similar fish communities. The fraction of the community data that could be explained by regional effects, independent of pure habitat effects, was similar in both fish (33%) and coral (36.9%) communities. Pure habitat effects were slightly greater in the fish (31.3%) than in the coral (20.1%) community. Time explained relatively little variation (fish = 7.9%, corals = 9.6%) compared with these two spatial factors. Conclusions Our results indicate either that fish and coral communities were structured in similar ways by processes associated with region, habitat and time, or that the variation in fish community structure tracked variation associated with the coral communities at these sites and thereby reflects an indirect link between the environment and the structure of fish communities mediated by corals. Irrespective of the causes of such commonality, we demonstrate that community structure, not just species richness, can be related to both habitat differences and regional setting simultaneously.  相似文献   

9.
Reef-building corals may be seen as holobiont organisms, presenting diverse associated microbial communities. Best known is the symbiotic relationship with zooxanthellae, but Archaea, Bacteria, fungi, viruses, and algal plastids are also abundant. Until now, there is little information concerning microbial communities associated with Brazilian corals. The present study aims to describe the diversity of Archaea, Bacteria, and eukaryotic algal plastid communities associated with two sympatric species, Siderastrea stellata and Mussismilia hispida, from Southeastern Brazil, using 16S rRNA gene libraries. Since corals present a high number of other associated invertebrates, coral barcoding (COI) was performed to confirm the exclusive occurrence of coral DNA in our samples. Our analysis yielded 354 distinct microbial OTUs, represented mainly by novel phylotypes. Richness (Chao1 and ACE) and diversity (H') estimations of the microbial communities associated with both species were high and comparable to other studies. Rarefaction analyses showed that microbial diversity of S. stellata is higher than that of M. hispida. Libshuff comparative analyses showed that the highest microbial community similarity between the two coral species occurred in the bacterial libraries, while archaeal and plastidial communities were significantly different. Crenarchaeota dominated archaeal communities, while Proteobacteria was the most abundant bacterial phylum, dominated by alpha-Proteobacteria. Plastids were also represented by novel phylotypes and did not match with any 16S rRNA sequences of Cyanobacteria and zooxanthellae from GenBank. Our data improves the pool of available information on Brazilian coral microbes and shows corals as sources of diverse prokaryotic and picoeukaryotic communities.  相似文献   

10.
Reef-building corals form associations with a huge diversity of microorganisms, which are essential for the survival and well-being of their host. While the acquisition patterns of Symbiodiniaceae microalgal endosymbionts are strongly linked to the coral's reproductive strategy, few studies have investigated the transmission mode of bacteria, especially in brooding species. Here, we relied on 16S rRNA gene and Internal Transcribed Spacer 2 marker metabarcoding in conjunction with fluorescence in situ hybridisation microscopy to describe the onset of microbial associations in the common brooding coral Pocillopora acuta. We analysed the bacterial and Symbiodiniaceae community composition in five adult colonies, their larvae, and 4-day old recruits. Larvae and recruits inherited Symbiodiniaceae, as well as a small number of bacterial strains, from their parents. Rhodobacteraceae and Endozoicomonas were among the most abundant taxa that were likely maternally transmitted to the offspring. The presence of bacterial aggregates in newly released larvae was observed with confocal microscopy, confirming the occurrence of vertical transmission of bacteria in P. acuta. We concluded that host factors, as well as the environmental bacterial pool influenced the microbiome of P. acuta.  相似文献   

11.
Corals are sessile eukaryotic hosts which provide a unique surface for microbial colonization. Culture independent studies show that the coral mucus and tissue harbour diverse and abundant prokaryotic communities. However, little is known about the diversity of bacteria associated with the corals of Gulf of Mannar. The present study characterised the bacterial diversity associated with the mucus of the coral Acropora digitifera from the Gulf of Mannar by 16S rRNA gene clone library construction. The bacterial communities of the mucus of A. digitifera were diverse, with representatives within the Alphaproteobacteria, Gammaproteobacteria, Actinobacteria, Firmicutes and several unclassified bacteria. The culture independent bacterial population was totally different from our previous culture dependent study of the mucus and tissue of the same coral. 36% of the bacteria in the clone library of A. digitifera were found to be novel after full length sequencing of the 16S rRNA gene wherein several clones were found to be novel at the Genus and species level. The current study further supports the findings that Actinobacteria amount to a certain proportion among bacterial communities associated with corals.  相似文献   

12.
13.
The complex symbiotic relationship between corals and their dinoflagellate partner Symbiodinium is believed to be sustained through close associations with mutualistic bacterial communities, though little is known about coral associations with bacterial groups able to fix nitrogen (diazotrophs). In this study, we investigated the diversity of diazotrophic bacterial communities associated with three common coral species (Acropora millepora, Acropora muricata, and Pocillopora damicormis) from three midshelf locations of the Great Barrier Reef (GBR) by profiling the conserved subunit of the nifH gene, which encodes the dinitrogenase iron protein. Comparisons of diazotrophic community diversity among coral tissue and mucus microenvironments and the surrounding seawater revealed that corals harbor diverse nifH phylotypes that differ between tissue and mucus microhabitats. Coral mucus nifH sequences displayed high heterogeneity, and many bacterial groups overlapped with those found in seawater. Moreover, coral mucus diazotrophs were specific neither to coral species nor to reef location, reflecting the ephemeral nature of coral mucus. In contrast, the dominant diazotrophic bacteria in tissue samples differed among coral species, with differences remaining consistent at all three reefs, indicating that coral-diazotroph associations are species specific. Notably, dominant diazotrophs for all coral species were closely related to the bacterial group rhizobia, which represented 71% of the total sequences retrieved from tissue samples. The species specificity of coral-diazotroph associations further supports the coral holobiont model that bacterial groups associated with corals are conserved. Our results suggest that, as in terrestrial plants, rhizobia have developed a mutualistic relationship with corals and may contribute fixed nitrogen to Symbiodinium.  相似文献   

14.
The significance of bacteria for eukaryotic functioning is increasingly recognized. Coral reef ecosystems critically rely on the relationship between coral hosts and their intracellular photosynthetic dinoflagellates, but the role of the associated bacteria remains largely theoretical. Here, we set out to relate coral‐associated bacterial communities of the fungid host species Ctenactis echinata to environmental settings (geographic location, substrate cover, summer/winter, nutrient and suspended matter concentrations) and coral host abundance. We show that bacterial diversity of C. echinata aligns with ecological differences between sites and that coral colonies sampled at the species’ preferred habitats are primarily structured by one bacterial taxon (genus Endozoicomonas) representing more than 60% of all bacteria. In contrast, host microbiomes from lower populated coral habitats are less structured and more diverse. Our study demonstrates that the content and structure of the coral microbiome aligns with environmental differences and denotes habitat adequacy. Availability of a range of coral host habitats might be important for the conservation of distinct microbiome structures and diversity.  相似文献   

15.
The importance of Symbiodinium algal endosymbionts and a diverse suite of bacteria for coral holobiont health and functioning are widely acknowledged. Yet, we know surprisingly little about microbial community dynamics and the stability of host‐microbe associations under adverse environmental conditions. To gain insight into the stability of coral host‐microbe associations and holobiont structure, we assessed changes in the community structure of Symbiodinium and bacteria associated with the coral Pocillopora verrucosa under excess organic nutrient conditions. Pocillopora‐associated microbial communities were monitored over 14 days in two independent experiments. We assessed the effect of excess dissolved organic nitrogen (DON) and excess dissolved organic carbon (DOC). Exposure to excess nutrients rapidly affected coral health, resulting in two distinct stress phenotypes: coral bleaching under excess DOC and severe tissue sloughing (>90% tissue loss resulting in host mortality) under excess DON. These phenotypes were accompanied by structural changes in the Symbiodinium community. In contrast, the associated bacterial community remained remarkably stable and was dominated by two Endozoicomonas phylotypes, comprising on average 90% of 16S rRNA gene sequences. This dominance of Endozoicomonas even under conditions of coral bleaching and mortality suggests the bacterial community of P. verrucosa may be rather inflexible and thereby unable to respond or acclimatize to rapid changes in the environment, contrary to what was previously observed in other corals. In this light, our results suggest that coral holobionts might occupy structural landscapes ranging from a highly flexible to a rather inflexible composition with consequences for their ability to respond to environmental change.  相似文献   

16.
Increased frequency of disturbances and anthropogenic activities are predicted to have a devastating impact on coral reefs that will ultimately change the composition of reef associated fish communities. We reviewed and analysed studies that document the effects of disturbance‐mediated coral loss on coral reef fishes. Meta‐analysis of 17 independent studies revealed that 62% of fish species declined in abundance within 3 years of disturbances that resulted in >10% decline in coral cover. Abundances of species reliant on live coral for food and shelter consistently declined during this time frame, while abundance of some species that feed on invertebrates, algae and/or detritus increased. The response of species, particularly those expected to benefit from the immediate loss of coral, is, however, variable and is attributed to erratic replenishment of stocks, ecological versatility of species and sublethal responses, such as changes in growth, body condition and feeding rates. The diversity of fish communities was found to be negatively and linearly correlated to disturbance‐mediated coral loss. Coral loss >20% typically resulted in a decline in species richness of fish communities, although diversity may initially increase following small declines in coral cover from high coverage. Disturbances that result in an immediate loss of habitat complexity (e.g. severe tropical storms), have a greater impact on fishes from all trophic levels, compared with disturbances that kill corals, but leave the reef framework intact (e.g. coral bleaching and outbreaks of Acanthaster planci). This is most evident among small bodied species and suggests the long‐term consequences of coral loss through coral bleaching and crown‐of‐thorn starfish outbreaks may be much more substantial than the short‐term effects currently documented.  相似文献   

17.
The health and functioning of reef‐building corals is dependent on a balanced association with prokaryotic and eukaryotic microbes. The coral skeleton harbours numerous endolithic microbes, but their diversity, ecological roles and responses to environmental stress, including ocean acidification (OA), are not well characterized. This study tests whether pH affects the diversity and structure of prokaryotic and eukaryotic algal communities associated with skeletons of Porites spp. using targeted amplicon (16S rRNA gene, UPA and tufA) sequencing. We found that the composition of endolithic communities in the massive coral Porites spp. inhabiting a naturally high pCO2 reef (avg. pCO2 811 μatm) is not significantly different from corals inhabiting reference sites (avg. pCO2 357 μatm), suggesting that these microbiomes are less disturbed by OA than previously thought. Possible explanations may be that the endolithic microhabitat is highly homeostatic or that the endolithic micro‐organisms are well adapted to a wide pH range. Some of the microbial taxa identified include nitrogen‐fixing bacteria (Rhizobiales and cyanobacteria), algicidal bacteria in the phylum Bacteroidetes, symbiotic bacteria in the family Endozoicomoniaceae, and endolithic green algae, considered the major microbial agent of reef bioerosion. Additionally, we test whether host species has an effect on the endolithic community structure. We show that the endolithic community of massive Porites spp. is substantially different and more diverse than that found in skeletons of the branching species Seriatopora hystrix and Pocillopora damicornis. This study reveals highly diverse and structured microbial communities in Porites spp. skeletons that are possibly resilient to OA.  相似文献   

18.
19.

Background

Coral-associated bacteria are increasingly considered to be important in coral health, and altered bacterial community structures have been linked to both coral disease and bleaching. Despite this, assessments of bacterial communities on corals rarely apply sufficient replication to adequately describe the natural variability. Replicated data such as these are crucial in determining potential roles of bacteria on coral.

Methodology/Principal Findings

Denaturing Gradient Gel Electrophoresis (DGGE) of the V3 region of the 16S ribosomal DNA was used in a highly replicated approach to analyse bacterial communities on both healthy and diseased corals. Although site-specific variations in the bacterial communities of healthy corals were present, host species-specific bacterial associates within a distinct cluster of gamma-proteobacteria could be identified, which are potentially linked to coral health. Corals affected by “White Syndrome” (WS) underwent pronounced changes in their bacterial communities in comparison to healthy colonies. However, the community structure and bacterial ribotypes identified in diseased corals did not support the previously suggested theory of a bacterial pathogen as the causative agent of the syndrome.

Conclusions/Significance

This is the first study to employ large numbers of replicated samples to assess the bacterial communities of healthy and diseased corals, and the first culture-independent assessment of bacterial communities on WS affected Acroporid corals on the GBR. Results indicate that a minimum of 6 replicate samples are required in order to draw inferences on species, spatial or health-related changes in community composition, as a set of clearly distinct bacterial community profiles exist in healthy corals. Coral bacterial communities may be both site and species specific. Furthermore, a cluster of gamma-proteobacterial ribotypes may represent a group of specific common coral and marine invertebrate associates. Finally, the results did not support the contention that a single bacterial pathogen may be the causative agent of WS Acroporids on the GBR.  相似文献   

20.
The high biodiversity of coral reefs is attributable to the many invertebrate groups which live in symbiotic relationships with other reef organisms, particularly those which associate with the living coral habitat. However, few studies have examined the diversity and community structure of coral-dwelling invertebrates and how they vary among coral species. This study quantified the species richness and composition of animals associated with four common species of branching corals (Acropora nasuta, A. millepora, Pocillopora damicornis, and Seriatopora hystrix) at Lizard Island in the northern Great Barrier Reef. One hundred and seventy-eight nominal species from 12 different phyla were extracted across 50 replicate colonies of each coral host. A single coral colony, approximately 20 cm in diameter, harbored as many as 73 individuals and 24 species. There were substantial differences in invertebrate species composition among coral hosts of different families as well as genera. Twenty-seven species (15% of all taxa collected) were found on only one of the four different coral species, which may potentially indicate some level of specialization among coral hosts. The distinct assemblages on different coral species, and the presence of potential specialists, suggests invertebrate communities will be sensitive to the differential loss of branching coral species resulting from coral reef degradation.  相似文献   

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