Episodic Eruptions of Volcanic Ash Trigger a Reversible Cascade of Nuisance Species Outbreaks in Pristine Coral Habitats

Volcanically active islands abound in the tropical Pacific and harbor complex coral communities. Whereas lava streams and deep ash deposits are well-known to devastate coral communities through burial and smothering, little is known about the effect of moderate amounts of small particulate ash deposits on reef communities. Volcanic ash contains a diversity of chemical compounds that can induce nutrient enrichments triggering changes in benthic composition. Two independently collected data sets on the marine benthos of the pristine and remote reefs around Pagan Island, Northern Mariana Islands, reveal a sudden critical transition to cyanobacteria-dominated communities in 2009–2010, which coincides with a period of continuous volcanic ash eruptions. Concurrently, localized outbreaks of the coral-killing cyanobacteriosponge Terpios hoshinota displayed a remarkable symbiosis with filamentous cyanobacteria, which supported the rapid overgrowth of massive coral colonies and allowed the sponge to colonize substrate types from which it has not been documented before. The chemical composition of tephra from Pagan indicates that the outbreak of nuisance species on its reefs might represent an early succession stage of iron enrichment (a.k.a. “black reefs”) similar to that caused by anthropogenic debris like ship wrecks or natural events like particulate deposition from wildfire smoke plumes or desert dust storms. Once Pagan''s volcanic activity ceased in 2011, the cyanobacterial bloom disappeared. Another group of well-known nuisance algae in the tropical Pacific, the pelagophytes, did not reach bloom densities during this period of ash eruptions but new species records for the Northern Mariana Islands were documented. These field observations indicate that the study of population dynamics of pristine coral communities can advance our understanding of the resilience of tropical reef systems to natural and anthropogenic disturbances.     

Rapid coral colonization of a recent lava flow following a volcanic eruption,Banda Islands,Indonesia

Compared to the catastrophic impacts of various environmental disturbances and the subsequent recovery of scleractinian coral communities from these events, little is known about the early successional dynamics of coral communities following major volcanic eruptions. The 1988 volcanic eruption of Gunung Api, Banda Islands, Indonesia, provided a unique opportunity to study the rate at which a reef-building coral community develops on an andesitic lava flow. Coral colonization was studied at three locations varying in substrate characteristics. Five years after the eruption, the sheltered lava flow supported a diverse coral community (124 species) with high coral cover . Tabulate acroporids were a dominant component of the lava flow coral community, with some colonies measuring over 90 cm in diameter. Higher average coral diversity, coral abundance and cover were recorded on the andesitic lava flow than on an adjacent carbonate reef not covered by the lava, and on a substrate of unstable pyroclastic deposits located on the southwestern coast of the volcano. In some areas of high coral diversity and environmental stability, andesitic lava flows may create local hot-spots of coral diversity by providing a structurally complex, predator-free and stable substrate for the recruitment of coral species from the adjacent and regional species pools.     

Effects of volcanic ash deposits on four functional groups of a coral reef

The immediate effects of pyroclastic deposits (ash fall) on reef communities after volcanic eruptions on remote tropical islands have never been critically examined. This study discusses findings from an interdisciplinary research expedition to the island of Anatahan (Commonwealth of the Northern Mariana Islands), 4 months after its first recorded volcanic eruption. Deep ash completely obliterated any trace of reef communities off the northeastern shores of the island; however, reefs in other areas, although still blanketed with ash deposits, fared better. Mean fish biomass recorded around Anatahan after the eruption was 0.22 kg 100 m⁻², a value three times lower than at Sarigan, the closest neighbor island. Similarly, average percent cover of live coral (7.9%), crustose coralline red algal (7.7%), and macroalgal (14.3%) populations was 2.3, 1.4, and 3.0 times lower than at Sarigan, respectively.     

Effect of substrate type on bacterial community composition in biofilms from the Great Barrier Reef

Natural and anthropogenic impacts such as terrestrial runoff, influence the water quality along the coast of the Great Barrier Reef (GBR) and may in turn affect coral reef communities. Associated bacterial biofilms respond rapidly to environmental conditions and are potential bioindicators for changes in water quality. As a prerequisite to study the effects of water quality on biofilm communities, appropriate biofilm substrates for deployment in the field must be developed and evaluated. This study investigates the effect of different settlement substrates (i.e. glass slides, ceramic tiles, coral skeletons and reef sediments) on bacterial biofilm communities grown in situ for 48 days at two locations in the Whitsunday Island Group (Central GBR) during two sampling times. Bacterial communities associated with the biofilms were analysed using terminal restriction fragment length polymorphism (T-RFLP) and clone library analyses of 16S rRNA genes. Findings revealed that substrate type had little influence on bacterial community composition. Of particular relevance, glass slides and coral skeletons exhibited very similar communities during both sampling times, suggesting the suitability of standardized glass slides for long-term biofilm indicator studies in tropical coral reef ecosystems.     

Drivers of bacterial diversity dynamics in permeable carbonate and silicate coral reef sands from the Red Sea

Permeable sediments and associated microbial communities play a fundamental role in nutrient recycling within coral reef ecosystems by ensuring high levels of primary production in oligotrophic environments. A previous study on organic matter degradation within biogenic carbonate and terrigenous silicate reef sands in the Red Sea suggested that observed sand-specific differences in microbial activity could be caused by variations in microbial biomass and diversity. Here, we tested this hypothesis by comparing bacterial abundance and community structure in both sand types, and by further exploring the structuring effects of time (season) and space (sediment depth, in/out-reef). Changes in bacterial community structure, as determined via automated ribosomal intergenic spacer analysis (ARISA), were primarily driven by sand mineralogy at specific seasons, sediment depths and reef locations. By coupling ARISA with 16S-ITS rRNA sequencing, we detected significant community shifts already at the bacterial class level, with Proteobacteria (Gamma-, Delta-, Alpha-) and Actinobacteria being prominent members of the highly diverse communities. Overall, our findings suggest that reef sand-associated bacterial communities vary substantially with sand type. Especially in synergy with environmental variation over time and space, mineralogical differences seem to play a central role in maintaining high levels of bacterial community heterogeneity. The local co-occurrence of carbonate and silicate sands may thus significantly increase the availability of microbial niches within a single coral reef ecosystem.     

Disentangling the complex microbial community of coral reefs using standardized Autonomous Reef Monitoring Structures (ARMS)

Autonomous Reef Monitoring Structures (ARMS) have been applied worldwide to describe eukaryotic cryptic reef fauna. Conversely, bacterial communities, which are critical components of coral reef ecosystem functioning, remain largely overlooked. Here we deployed 56 ARMS across the 2,000‐km spread of the Red Sea to assay biodiversity, composition and inferred underlying functions of coral reef‐associated bacterial communities via 16S rRNA gene sequencing. We found that bacterial community structure and diversity aligned with environmental differences. Indeed, sea surface temperature and macroalgae cover were key in explaining bacterial relative abundance. Importantly, taxonomic and functional alpha diversity decreased under more extreme environmental conditions (e.g., higher temperatures) in the southern Red Sea. This may imply a link between bacterial community diversity and functional capabilities, with implications for conservation management. Our study demonstrates the utility of ARMS to investigate the response of coral reef‐associated bacterial communities to environmental change.     

Microbiome structure of the fungid coral Ctenactis echinata aligns with environmental differences

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.     

Spatial scales of bacterial diversity in cold-water coral reef ecosystems

Background

Cold-water coral reef ecosystems are recognized as biodiversity hotspots in the deep sea, but insights into their associated bacterial communities are still limited. Deciphering principle patterns of bacterial community variation over multiple spatial scales may however prove critical for a better understanding of factors contributing to cold-water coral reef stability and functioning.

Methodology/Principal Findings

Bacterial community structure, as determined by Automated Ribosomal Intergenic Spacer Analysis (ARISA), was investigated with respect to (i) microbial habitat type and (ii) coral species and color, as well as the three spatial components (iii) geomorphologic reef zoning, (iv) reef boundary, and (v) reef location. Communities revealed fundamental differences between coral-generated (branch surface, mucus) and ambient microbial habitats (seawater, sediments). This habitat specificity appeared pivotal for determining bacterial community shifts over all other study levels investigated. Coral-derived surfaces showed species-specific patterns, differing significantly between Lophelia pertusa and Madrepora oculata, but not between L. pertusa color types. Within the reef center, no community distinction corresponded to geomorphologic reef zoning for both coral-generated and ambient microbial habitats. Beyond the reef center, however, bacterial communities varied considerably from local to regional scales, with marked shifts toward the reef periphery as well as between different in- and offshore reef sites, suggesting significant biogeographic imprinting but weak microbe-host specificity.

Conclusions/Significance

This study presents the first multi-scale survey of bacterial diversity in cold-water coral reefs, spanning a total of five observational levels including three spatial scales. It demonstrates that bacterial communities in cold-water coral reefs are structured by multiple factors acting at different spatial scales, which has fundamental implications for the monitoring of microbial diversity and function in those ecosystems.     

Coral reefs in a clastic sedimentary environment: Fossil (Miocene,S.W. Turkey) and modern (Recent,Red Sea) analogues

Summary The Miocene sequences of southwestern Turkey and the Recent Red Sea are characterised by an unusual and distinct sedimentary association. In both cases near-shore patch and fringing reefs occur along the margins of alluvial fans and braidplains developed under semiarid climatic conditions. In such an environment reef location, morphology and internal structure are controlled primarily by the clastic sedimentary system rather than the independent growth of the framework builders as in normal reef environments. The primary control is a morphological one, the reefs adopting the overall geometry of the sediment body forming a fan shaped arcuate belt. Irregularities in reef morphology are clearly related to the presence of fluvial channels on the fans. The coarse grained gravel of the fans provide an ideal substrate for coral colonisation, this is reflected in the lack of a pioneer community in the Miocene reefs. Periodic rapid burial of the reefs terminates the production of carbonate debris by mechanical and biological erosion resulting in preservation of a relatively unaltered primary framework. The inter-reef sediment consists exclusively of terrigenous sediment.     

Mass coral bleaching causes biotic homogenization of reef fish assemblages

Global climate change is altering community composition across many ecosystems due to nonrandom species turnover, typically characterized by the loss of specialist species and increasing similarity of biological communities across spatial scales. As anthropogenic disturbances continue to alter species composition globally, there is a growing need to identify how species responses influence the establishment of distinct assemblages, such that management actions may be appropriately assigned. Here, we use trait‐based analyses to compare temporal changes in five complementary indices of reef fish assemblage structure among six taxonomically distinct coral reef habitats exposed to a system‐wide thermal stress event. Our results revealed increased taxonomic and functional similarity of previously distinct reef fish assemblages following mass coral bleaching, with changes characterized by subtle, but significant, shifts toward predominance of small‐bodied, algal‐farming habitat generalists. Furthermore, while the taxonomic or functional richness of fish assemblages did not change across all habitats, an increase in functional originality indicated an overall loss of functional redundancy. We also found that prebleaching coral composition better predicted changes in fish assemblage structure than the magnitude of coral loss. These results emphasize how measures of alpha diversity can mask important changes in the structure and functioning of ecosystems as assemblages reorganize. Our findings also highlight the role of coral species composition in structuring communities and influencing the diversity of responses of reef fishes to disturbance. As new coral species configurations emerge, their desirability will hinge upon the composition of associated species and their capacity to maintain key ecological processes in spite of ongoing disturbances.     

Consistent nutrient storage and supply mediated by diverse fish communities in coral reef ecosystems

Corals thrive in low nutrient environments and the conservation of these globally imperiled ecosystems is largely dependent on mitigating the effects of anthropogenic nutrient enrichment. However, to better understand the implications of anthropogenic nutrients requires a heightened understanding of baseline nutrient dynamics within these ecosystems. Here, we provide a novel perspective on coral reef nutrient dynamics by examining the role of fish communities in the supply and storage of nitrogen (N) and phosphorus (P). We quantified fish‐mediated nutrient storage and supply for 144 species and modeled these data onto 172 fish communities (71 729 individual fish), in four types of coral reefs, as well as seagrass and mangrove ecosystems, throughout the Northern Antilles. Fish communities supplied and stored large quantities of nutrients, with rates varying among ecosystem types. The size structure and diversity of the fish communities best predicted N and P supply and storage and N : P supply, suggesting that alterations to fish communities (e.g., overfishing) will have important implications for nutrient dynamics in these systems. The stoichiometric ratio (N : P) for storage in fish mass (~8 : 1) and supply (~20 : 1) was notably consistent across the four coral reef types (but not seagrass or mangrove ecosystems). Published nutrient enrichment studies on corals show that deviations from this N : P supply ratio may be associated with poor coral fitness, providing qualitative support for the hypothesis that corals and their symbionts may be adapted to specific ratios of nutrient supply. Consumer nutrient stoichiometry provides a baseline from which to better understand nutrient dynamics in coral reef and other coastal ecosystems, information that is greatly needed if we are to implement more effective measures to ensure the future health of the world's oceans.     

Benthic N2 fixation in coral reefs and the potential effects of human‐induced environmental change

Tropical coral reefs are among the most productive and diverse ecosystems, despite being surrounded by ocean waters where nutrients are in short supply. Benthic dinitrogen (N₂) fixation is a significant internal source of “new” nitrogen (N) in reef ecosystems, but related information appears to be sparse. Here, we review the current state (and gaps) of knowledge on N₂ fixation associated with coral reef organisms and their ecosystems. By summarizing the existing literature, we show that benthic N₂ fixation is an omnipresent process in tropical reef environments. Highest N₂ fixation rates are detected in reef‐associated cyanobacterial mats and sea grass meadows, clearly showing the significance of these functional groups, if present, to the input of new N in reef ecosystems. Nonetheless, key benthic organisms such as hard corals also importantly contribute to benthic N₂ fixation in the reef. Given the usually high coral coverage of healthy reef systems, these results indicate that benthic symbiotic associations may be more important than previously thought. In fact, mutualisms between carbon (C) and N₂ fixers have likely evolved that may enable reef communities to mitigate N limitation. We then explore the potential effects of the increasing human interferences on the process of benthic reef N₂ fixation via changes in diazotrophic populations, enzymatic activities, or availability of benthic substrates favorable to these microorganisms. Current knowledge indicates positive effects of ocean acidification, warming, and deoxygenation and negative effects of increased ultraviolet radiation on the amount of N fixed in coral reefs. Eutrophication may either boost or suppress N₂ fixation, depending on the nutrient becoming limiting. As N₂ fixation appears to play a fundamental role in nutrient‐limited reef ecosystems, these assumptions need to be expanded and confirmed by future research efforts addressing the knowledge gaps identified in this review.     

Patterns of environmental variability influence coral‐associated bacterial and algal communities on the Mesoamerican Barrier Reef

A coral's capacity to alter its microbial symbionts may enhance its fitness in the face of climate change. Recent work predicts exposure to high environmental variability may increase coral resilience and adaptability to future climate conditions. However, how this heightened environmental variability impacts coral‐associated microbial communities remains largely unexplored. Here, we examined the bacterial and algal symbionts associated with two coral species of the genus Siderastrea with distinct life history strategies from three reef sites on the Belize Mesoamerican Barrier Reef System with low or high environmental variability. Our results reveal bacterial community structure, as well as alpha‐ and beta‐diversity patterns, vary by host species. Differences in bacterial communities between host species were partially explained by high abundance of Deltaproteobacteria and Rhodospirillales and high bacterial diversity in Siderastrea radians. Our findings also suggest Siderastrea spp. have dynamic core bacterial communities that likely drive differences observed in the entire bacterial community, which may play a critical role in rapid acclimatization to environmental change. Unlike the bacterial community, Symbiodiniaceae composition was only distinct between host species at high thermal variability sites, suggesting that different factors shape bacterial versus algal communities within the coral holobiont. Our findings shed light on how domain‐specific shifts in dynamic microbiomes may allow for unique methods of enhanced host fitness.     

Human impacts decouple a fundamental ecological relationship—The positive association between host diversity and parasite diversity

Human impacts on ecosystems can decouple the fundamental ecological relationships that create patterns of diversity in free‐living species. Despite the abundance, ubiquity, and ecological importance of parasites, it is unknown whether the same decoupling effects occur for parasitic species. We investigated the influence of fishing on the relationship between host diversity and parasite diversity for parasites of coral reef fishes on three fished and three unfished islands in the central equatorial Pacific. Fishing was associated with a shallowing of the positive host‐diversity–parasite‐diversity relationship. This occurred primarily through negative impacts of fishing on the presence of complex life‐cycle parasites, which created a biologically impoverished parasite fauna of directly transmitted parasites resilient to changes in host biodiversity. Parasite diversity appears to be decoupled from host diversity by fishing impacts in this coral reef ecosystem, which suggests that such decoupling might also occur for parasites in other ecosystems affected by environmental change.     

Species richness of motile cryptofauna across a gradient of reef framework erosion

Coral reef ecosystems contain exceptionally high concentrations of marine biodiversity, potentially encompassing millions of species. Similar to tropical rainforests and their insects, the majority of reef animal species are small and cryptic, living in the cracks and crevices of structural taxa (trees and corals). Although the cryptofauna make up the majority of a reef??s metazoan biodiversity, we know little about their basic ecology. We sampled motile cryptofaunal communities from both live corals and dead carbonate reef framework across a gradient of increasing erosion on a reef in Pacific Panamá. A total of 289 Operational Taxonomic Units (OTUs) from six phyla were identified. We used species-accumulation models fitted to individual- and sample-based rarefaction curves, as well as seven nonparametric richness estimators to estimate species richness among the different framework types. All procedures predicted the same trends in species richness across the differing framework types. Estimated species richness was higher in dead framework (261?C370 OTUs) than in live coral substrates (112?C219 OTUs). Surprisingly, richness increased as framework structure was eroded: coral rubble contained the greatest number of species (227?C320 OTUs) and the lowest estimated richness of 47?C115 OTUs was found in the zone where the reef framework had the greatest vertical relief. This contradicts the paradigm that abundant live coral indicates the apex of reef diversity.     

Threatened Corals Provide Underexplored Microbial Habitats

Contemporary in-depth sequencing of environmental samples has provided novel insights into microbial community structures, revealing that their diversity had been previously underestimated. Communities in marine environments are commonly composed of a few dominant taxa and a high number of taxonomically diverse, low-abundance organisms. However, studying the roles and genomic information of these “rare” organisms remains challenging, because little is known about their ecological niches and the environmental conditions to which they respond. Given the current threat to coral reef ecosystems, we investigated the potential of corals to provide highly specialized habitats for bacterial taxa including those that are rarely detected or absent in surrounding reef waters. The analysis of more than 350,000 small subunit ribosomal RNA (16S rRNA) sequence tags and almost 2,000 nearly full-length 16S rRNA gene sequences revealed that rare seawater biosphere members are highly abundant or even dominant in diverse Caribbean corals. Closely related corals (in the same genus/family) harbored similar bacterial communities. At higher taxonomic levels, however, the similarities of these communities did not correlate with the phylogenetic relationships among corals, opening novel questions about the evolutionary stability of coral-microbial associations. Large proportions of OTUs (28.7–49.1%) were unique to the coral species of origin. Analysis of the most dominant ribotypes suggests that many uncovered bacterial taxa exist in coral habitats and await future exploration. Our results indicate that coral species, and by extension other animal hosts, act as specialized habitats of otherwise rare microbes in marine ecosystems. Here, deep sequencing provided insights into coral microbiota at an unparalleled resolution and revealed that corals harbor many bacterial taxa previously not known. Given that two of the coral species investigated are listed as threatened under the U.S. Endangered Species Act, our results add an important microbial diversity-based perspective to the significance of conserving coral reefs.     

Recognizing diversity in coral symbiotic dinoflagellate communities

A detailed understanding of how diversity in endosymbiotic dinoflagellate communities maps onto the physiological range of coral hosts is critical to predicting how coral reef ecosystems will respond to climate change. Species-level taxonomy of the dinoflagellate genus Symbiodinium has been predominantly examined using the internal transcribed spacer (ITS) region of the nuclear ribosomal array (rDNA ITS2) and downstream screening for dominant types using denaturing gradient gel electrophoresis (DGGE). Here, ITS2 diversity in the communities of Symbiodinium harboured by two Hawaiian coral species was explored using direct sequencing of clone libraries. We resolved sixfold to eightfold greater diversity per coral species than previously reported, the majority of which corresponds to a novel and distinct phylogenetic lineage. We evaluated how these sequences migrate in DGGE and demonstrate that this method does not effectively resolve this diversity. We conclude that the Porites spp. examined here harbour diverse assemblages of novel Symbiodinium types and that cloning and sequencing is an effective methodological approach for resolving the complexity of endosymbiotic dinoflagellate communities harboured by reef corals.     

Life histories predict coral community disassembly under multiple stressors

Climate change is reshaping biological communities against a background of existing human pressure. Evaluating the impacts of multiple stressors on community dynamics can be particularly challenging in species‐rich ecosystems, such as coral reefs. Here, we investigate whether life‐history strategies and cotolerance to different stressors can predict community responses to fishing and temperature‐driven bleaching using a 20‐year time series of coral assemblages in Kenya. We found that the initial life‐history composition of coral taxa largely determined the impacts of bleaching and coral loss. Prior to the 1998 bleaching event, coral assemblages within no‐take marine reserves were composed of three distinct life histories – competitive, stress‐tolerant and weedy– and exhibited strong declines following bleaching with limited subsequent recovery. In contrast, fished reefs had lower coral cover, fewer genera and were composed of stress‐tolerant and weedy corals that were less affected by bleaching over the long term. Despite these general patterns, we found limited evidence for cotolerance as coral genera and life histories were variable in their sensitivities to fishing and bleaching. Overall, fishing and bleaching have reduced coral diversity and led to altered coral communities of ‘survivor’ species with stress‐tolerant and weedy life histories. Our findings are consistent with expectations that climate change interacting with existing human pressure will result in the loss of coral diversity and critical reef habitat.     

Community involvement in management for maintaining coral reef resilience and biodiversity in southern Caribbean marine protected areas

Climate change is posing new challenges to conservation because management policies on protected coral reefs are less effective than they were before the current ecosystem degradation. Coral reefs, the most diverse and complex marine ecosystem provide economic services for millions, but are seriously threatened worldwide because reef-building corals are experiencing bleaching phenomena and a steady decline in abundance. The resources of a Marine Protected Area (MPA) in Cartagena, Colombia, are in constant decline, despite a current management plan and on-site staff, urging new conservation actions. A multidisciplinary team gathered to evaluate management effectiveness including biophysical, socioeconomic and governance indicators. Coral cover and fish diversity and abundance were low both inside and outside the MPA, which suggests a limited efficiency of management. Currently, the MPA is a reef with low coral cover and high algae cover as well as large dead coral areas, which are generally signs of highly degraded reef habitats. Live coral cover in the MPA was represented by pioneer coral species such as Agaricia tenuifolia and Porites astreoides. Nonetheless, 35% of the scleractinian species sampled in the area harbored more than one zooxanthellae symbiont, which suggests potential resistance and resilience against coral bleaching. Maintenance of trophic structure and functional diversity is an important endeavor that should be a priority for management in order to allow ecosystem resilience. Social and governance indicators showed low-income levels and few opportunities for communities living in and around the park, low governability, weak communication among stakeholders and with authorities at different levels. As a result, problems related to over exploitation of resources were commonplace in the MPA. These results reflect low adaptive capacity of communities to comply with restrictive conservation rules, showing that establishment of a protected area is a necessary but insufficient condition to guarantee conservation goals. Ignoring the role of local communities only will exacerbate the problems associated with natural resources. Involvement of communities in strategic ecosystems management appears to be a requisite to improve effectiveness of protected areas, and participatory strategies, such as co-management, offer opportunities to improve governability while letting communities adapt to MPA needs.