Every refuge has its price: Ostreobium as a model for understanding how algae can live in rock and stay in business.

Ostreobium is a siphonous green alga in the Bryopsidales (Chlorophyta) that burrows into calcium carbonate (CaCO3) substrates. In this habitat, it lives under environmental conditions unusual for an alga (i.e., low light and low oxygen) and it is a major agent of carbonate reef bioerosion. In coral skeletons, Ostreobium can form conspicuous green bands recognizable by the naked eye and it is thought to contribute to the coral's nutritional needs. With coral reefs in global decline, there is a renewed focus on understanding Ostreobium biology and its roles in the coral holobiont. This review summarizes knowledge on Ostreobium's morphological structure, biodiversity and evolution, photosynthesis, mechanism of bioerosion and its role as a member of the coral holobiont. We discuss the resources available to study Ostreobium biology, lay out some of the uncharted territories in Ostreobium biology and offer perspectives for future research.

New occurrences of the bone-eating worm Osedax from Late Cretaceous marine reptiles and implications for its biogeography and diversification.

The bone-eating worm Osedax is a speciose and globally distributed clade, primarily found on whale carcasses in marine environments. The earliest fossil evidence for Osedax borings was previously described in plesiosaur and sea turtle bones from the mid-Cretaceous of the United Kingdom, representing the only unequivocal pre-Oligocene occurrences. Confirming through CT scanning, we present new evidence of Osedax borings in three plesiosaur specimens and, for the first time, identify borings in two mosasaur specimens. All specimens are from the Late Cretaceous: one from the Cenomanian of the United Kingdom, two from the Campanian of the southeastern United States, and two from the Maastrichtian of Belgium. This extends the geographic range of Osedax in the Cretaceous to both sides of the northern Atlantic Ocean. The bones contain five borehole morphotypes, potentially created by different species of Osedax, with the Cenomanian specimen containing three morphotypes within a single tooth. This combined evidence of heightened species diversity by the Cenomanian and broad geographic range by the Campanian potentially indicates an earlier origin and diversification for this clade than previously hypothesized. Preservational biases indicate that Osedax was probably even more widely distributed and speciose in the Cretaceous than apparent in the fossil record.

Rubble persistence under ocean acidification threatened by accelerated bioerosion and lower-density coral skeletons.

As the balance between erosional and constructive processes on coral reefs tilts in favor of framework loss under human-induced local and global change, many reef habitats worldwide degrade and flatten. The resultant generation of coral rubble and the beds they form can have lasting effects on reef communities and structural complexity, threatening the continuity of reef ecological functions and the services they provide. To comprehensively capture changing framework processes and predict their evolution in the context of climate change, heavily colonized rubble fragments were exposed to ocean acidification (OA) conditions for 55 days. Controlled diurnal pH oscillations were incorporated in the treatments to account for the known impact of diel carbonate chemistry fluctuations on calcification and dissolution response to OA. Scenarios included contemporary pH (8.05 ± 0.025 diel fluctuation), elevated OA (7.90 ± 0.025), and high OA (7.70 ± 0.025). We used a multifaceted approach, combining chemical flux analyses, mass alteration measurements, and computed tomography scanning images to measure total and chemical bioerosion, as well as chemically driven secondary calcification. Rates of net carbonate loss measured in the contemporary conditions (1.36 kg m-2 year-1) were high compared to literature and increased in OA scenarios (elevated: 1.84 kg m-2 year-1 and high: 1.59 kg m-2 year-1). The acceleration of these rates was driven by enhanced chemical dissolution and reduced secondary calcification. Further analysis revealed that the extent of these changes was contingent on the density of the coral skeleton, in which the micro- and macroborer communities reside. Findings indicated that increased mechanical bioerosion rates occurred in rubble with lower skeletal density, which is of note considering that corals form lower-density skeletons under OA. These direct and indirect effects of OA on chemical and mechanical framework-altering processes will influence the permanence of this crucial habitat, carrying implications for biodiversity and reef ecosystem function.

New insights into endolithic palaeocommunity development in mobile hard substrate using CT imaging of bioeroded clasts from the Pliocene (Almería, SE Spain).

Bioeroded carbonate clasts from a Pliocene shallow-marine succession of Almería (SE Spain, Betic Cordillera) were analysed with computed tomography (CT). This revealed the detailed 3D architecture of bioerosion structures hidden within and allowed for their ichnotaxonomic identification (14 ichnospecies of 5 ichnogenera) and quantification. Borings are produced by worms, mostly polychaetes and sipunculids dominated, followed by bivalves and lastly by sponges. The crosscutting relationship between the borings and their preservation characteristics points to a complex colonization history of the clasts with repeated bioerosive episodes interrupted by physical disturbances, including overturning and abrasion of the clasts followed by their recolonization. Our findings facilitated paleoenvironmental interpretation and can be compared to analogous modern-day ecological succession. The sharp dominance of worm borings - early successional species - may be related to frequent, periodic, physical disturbance that possibly prevented the cobble-dwelling macroboring community from being overtaken by sponges - late successional taxa. CT, hand sample and petrographic observations detected, aside from borings, other irregularly shaped pores which are interpreted to be generated by diagenetic processes including dolomitization, silicification and dissolution, representing an intraparticle moldic and moldic enlarged porosity. Boring porosity crosscutting the diagenetically altered grains suggests the later occurrence of bioerosion processes. Irregular shapes ranging from roughly spherical, elongate sub-polyhedral to amoeboid resemble morphologies produced by modern sponges. Moldic pores possibly acted as primary domiciles for boring sponges, which infested, altered and enlarged pre-existing pores as they grew (as happens in the modern), providing an example of how biological and non-biological processes interacted and together influenced endolithic palaeocommunity development.

The influences of diurnal variability and ocean acidification on the bioerosion rates of two reef-dwelling Caribbean sponges.

Ocean acidification (OA) is expected to modify the structure and function of coral reef ecosystems by reducing calcification, increasing bioerosion, and altering the physiology of many marine organisms. Much of our understanding of these relationships is based on experiments with static OA treatments, although evidence suggests that the magnitude of diurnal fluctuations in carbonate chemistry may modulate the calcification response to OA. These light-mediated swings in seawater pH are projected to become more extreme with OA, yet their impact on bioerosion remains unknown. We evaluated the influence of diurnal carbonate chemistry variability on the bioerosion rates of two Caribbean sponges: the zooxanthellate Cliona varians and azooxanthellate Cliothosa delitrix. Replicate fragments from multiple colonies of each species were exposed to four precisely controlled pH treatments: contemporary static (8.05 ± 0.00; mean pH ± diurnal pH oscillation), contemporary variable (8.05 ± 0.10), future OA static (7.80 ± 0.00), and future OA variable (7.80 ± 0.10). Significantly enhanced bioerosion rates, determined using buoyant weight measurements, were observed under more variable conditions in both the contemporary and future OA scenarios for C. varians, whereas the same effect was only apparent under contemporary pH conditions for C. delitrix. These results indicate that variable carbonate chemistry has a stimulating influence on sponge bioerosion, and we hypothesize that bioerosion rates evolve non-linearly as a function of pCO2 resulting in different magnitudes and directions of rate enhancement/reduction between day and night, even with an equal fluctuation around the mean. This response appeared to be intensified by photosymbionts, evident by the consistently higher percent increase in bioerosion rates for photosynthetic C. varians across all treatments. These findings further suggest that more variable natural ecosystems may presently experience elevated sponge bioerosion rates and that the heightened impact of OA enhanced bioerosion on reef habitat could occur sooner than prior predictions.

The past, present, and future of coral reef growth in the Florida Keys.

Coral-reef degradation is driving global-scale reductions in reef-building capacity and the ecological, geological, and socioeconomic functions it supports. The persistence of those essential functions will depend on whether coral-reef management is able to rebalance the competing processes of reef accretion and erosion. Here, we reconstructed census-based carbonate budgets of 46 reefs throughout the Florida Keys from 1996 to 2019. We evaluated the environmental and ecological drivers of changing budget states and compared historical trends in reef-accretion potential to millennial-scale baselines of accretion from reef cores and future projections with coral restoration. We found that historically, most reefs had positive carbonate budgets, and many had reef-accretion potential comparable to the ~3 mm year-1 average accretion rate during the peak of regional reef building ~7000 years ago; however, declines in reef-building Acropora palmata and Orbicella spp. corals following a series of thermal stress events and coral disease outbreaks resulted in a shift from positive to negative budgets for most reefs in the region. By 2019, only ~15% of reefs had positive net carbonate production. Most of those reefs were in inshore, Lower Keys patch-reef habitats with low water clarity, supporting the hypothesis that environments with naturally low irradiance may provide a refugia from thermal stress. We caution that our estimated carbonate budgets are likely overly optimistic; comparison of reef-accretion potential to measured accretion from reef cores suggests that, by not accounting for the role of nonbiological physical and chemical erosion, census-based carbonate budgets may underestimate total erosion by ~1 mm year-1 (-1.15 kg CaCO3 m-2 year-1 ). Although the present state of Florida's reefs is dire, we demonstrate that the restoration of reef-building corals has the potential to help mitigate declines in reef accretion in some locations, which could allow some key ecosystem functions to be maintained until the threat of global climate change is addressed.

Global distribution and diversity of marine euendolithic cyanobacteria.

Euendolithic, or true-boring, cyanobacteria actively erode carbonate-containing substrata in a wide range of environments and pose significant risks to calcareous marine fauna. Their boring activities cause structural damage and increase susceptibility to disease and are projected to only intensify with global climate change. Most research has, however, focused on tropical coral systems, and limited information exists on the global distribution, diversity, and substratum specificity of euendoliths. This metastudy aimed to collate existing 16S rRNA gene surveys along with novel data from the south coast of South Africa to investigate the global distribution and genetic diversity of endoliths to identify a "core endolithic cyanobacterial microbiome" and assess global diversification of euendolithic cyanobacteria. The cyanobacterial families Phormidesmiaceae, Nodosilineaceae, Nostocaceae, and Xenococcaceae were the most prevalent, found in >92% of categories surveyed. All four known euendolith clusters were detected in both intertidal and subtidal habitats, in the North Atlantic, Mediterranean, and South Pacific oceans, across temperate latitudes, and within rock, travertine tiles, coral, shell, and coralline algae substrata. Analysis of the genetic variation within clusters revealed many organisms to be unique to substratum type and location, suggesting high diversity and niche specificity. Euendoliths are known to have important effects on their hosts. This is particularly important when hosts are globally significant ecological engineers or habitat-forming species. The findings of this study indicate high ubiquity and diversity of euendolithic cyanobacteria, suggesting high adaptability, which may lead to increased community and ecosystem-level effects with changing climatic conditions favoring the biochemical mechanisms of cyanobacterial bioerosion.

Two decades of carbonate budget change on shifted coral reef assemblages: are these reefs being locked into low net budget states?

The ecology of coral reefs is rapidly shifting from historical baselines. One key-question is whether under these new, less favourable ecological conditions, coral reefs will be able to sustain key geo-ecological processes such as the capacity to accumulate carbonate structure. Here, we use data from 34 Caribbean reef sites to examine how the carbonate production, net erosion and net carbonate budgets, as well as the organisms underlying these processes, have changed over the past 15 years in the absence of further severe acute disturbances. We find that despite fundamental benthic ecological changes, these ecologically shifted coral assemblages have exhibited a modest but significant increase in their net carbonate budgets over the past 15 years. However, contrary to expectations this trend was driven by a decrease in erosion pressure, largely resulting from changes in the abundance and size-frequency distribution of parrotfishes, and not by an increase in rates of coral carbonate production. Although in the short term, the carbonate budgets seem to have benefitted marginally from reduced parrotfish erosion, the absence of these key substrate grazers, particularly of larger individuals, is unlikely to be conducive to reef recovery and will thus probably lock these reefs into low budget states.

The evolution of traits and functions in herbivorous coral reef fishes through space and time.

Herbivory by fishes has been identified as a key ecological process shaping coral reefs through time. Although taxonomically limited, herbivorous reef fishes display a wide range of traits, which results in varied ecosystem functions on reefs around the world. Yet, we understand little about how these trait combinations and functions in ecosystems changed through time and across biogeographic realms. Here, we used fossils and phylogenies in a functional ecological framework to reveal temporal changes in nominally herbivorous fish assemblages among oceanic basins in both trait space and lineage richness among functions. We show that the trait space occupied by extant herbivorous fishes in the Indo-Pacific resulted from an expansion of traits from the ancestral Tethyan assemblages. By contrast, trait space in the Atlantic is the result of lineage turnover, with relatively recent colonization by lineages that arose in the east Tethys/Indo-Pacific. From an ecosystem function perspective, the Atlantic supports a depauperate fauna, with few extant herbivorous reef fish lineages performing each function. Indo-Pacific fishes support both more functions and more lineages within each function, with a marked Miocene to Pleistocene expansion. These disparities highlight the importance of history in explaining global variation in fish functional composition on coral reefs.

Single-cell visualization indicates direct role of sponge host in uptake of dissolved organic matter.

Marine sponges are set to become more abundant in many near-future oligotrophic environments, where they play crucial roles in nutrient cycling. Of high importance is their mass turnover of dissolved organic matter (DOM), a heterogeneous mixture that constitutes the largest fraction of organic matter in the ocean and is recycled primarily by bacterial mediation. Little is known, however, about the mechanism that enables sponges to incorporate large quantities of DOM in their nutrition, unlike most other invertebrates. Here, we examine the cellular capacity for direct processing of DOM, and the fate of the processed matter, inside a dinoflagellate-hosting bioeroding sponge that is prominent on Indo-Pacific coral reefs. Integrating transmission electron microscopy with nanoscale secondary ion mass spectrometry, we track 15N- and 13C-enriched DOM over time at the individual cell level of an intact sponge holobiont. We show initial high enrichment in the filter-feeding cells of the sponge, providing visual evidence of their capacity to process DOM through pinocytosis without mediation of resident bacteria. Subsequent enrichment of the endosymbiotic dinoflagellates also suggests sharing of host nitrogenous wastes. Our results shed light on the physiological mechanism behind the ecologically important ability of sponges to cycle DOM via the recently described sponge loop.

Extreme spatial heterogeneity in carbonate accretion potential on a Caribbean fringing reef linked to local human disturbance gradients.

The capacity of coral reefs to maintain their structurally complex frameworks and to retain the potential for vertical accretion is vitally important to the persistence of their ecological functioning and the ecosystem services they sustain. However, datasets to support detailed along-coast assessments of framework production rates and accretion potential do not presently exist. Here, we estimate, based on gross bioaccretion and bioerosion measures, the carbonate budgets and resultant estimated accretion rates (EAR) of the shallow reef zone of leeward Bonaire - between 5 and 12 m depth - at unique fine spatial resolution along this coast (115 sites). Whilst the fringing reef of Bonaire is often reported to be in a better ecological condition than most sites throughout the wider Caribbean region, our data show that the carbonate budgets of the reefs and derived EAR varied considerably across this ~58 km long fringing reef complex. Some areas, in particular the marine reserves, were indeed still dominated by structurally complex coral communities with high net carbonate production (>10 kg CaCO3  m-2  year-1 ), high live coral cover and complex structural topography. The majority of the studied sites, however, were defined by relatively low budget states (<2 kg CaCO3  m-2  year-1 ) or were in a state of net erosion. These data highlight the marked spatial heterogeneity that can occur in budget states, and thus in reef accretion potential, even between quite closely spaced areas of individual reef complexes. This heterogeneity is linked strongly to the degree of localized land-based impacts along the coast, and resultant differences in the abundance of reef framework building coral species. The major impact of this variability is that those sections of reef defined by low-accretion rates will have limited capacity to maintain their structural integrity and to keep pace with current projections of climate change induced sea-level rise (SLR), thus posing a threat to reef functioning and biodiversity, potentially leading to trophic cascades. Since many Caribbean reefs are more severely degraded than those found around Bonaire, it is to be expected that the findings presented here are rather the rule than the exception, but the study also highlights the need for similar high spatial resolution (along-coast) assessments of budget states and accretion rates to meaningfully explore increasing coastal risk at the country level. The findings also more generally underline the significance of reducing local anthropogenic disturbance and restoring framework building coral assemblages. Appropriately focussed local preservation efforts may aid in averting future large-scale above reef water depth increases on Caribbean coral reefs and will limit the social and economic implications associated with the loss of reef goods and services.

Identity of coral reef herbivores drives variation in ecological processes over multiple spatial scales.

Overexploitation of key species can negatively impact ecosystem processes, so understanding the ecological roles of individual species is critical for improving ecosystem management. Here, we use coral reefs and the process of herbivory as a model to examine how species identity of consumers influence ecosystem processes to inform management of these consumers. Herbivorous fishes can facilitate the recruitment, growth, and recovery of corals by controlling the fast-growing algae that can outcompete corals for space. However, herbivorous fish guilds are species rich with important differences among species in diet, movement, and habitat preferences. Yet, we lack a general understanding of (1) how these species-specific differences in feeding and behavior scale up to reef-wide rates of ecosystem processes and (2) how species identity and diversity impact these processes. To address these knowledge gaps, we used field observations to derive key species- and size-specific foraging parameters for nine herbivorous parrotfish species on coral reefs in the Florida Keys, USA. We then combined these foraging parameters with fish survey data spanning multiple spatial scales to estimate the rates of three ecosystem processes: area of reef grazed, amount of macroalgae removed, and rate of bioerosion. We found that predicted rates of ecological processes varied dramatically among habitats and among reef zones within habitats, driven primarily by variation in abundance among species with different foraging behaviors. In some cases, assemblages with similar levels of total biomass had different rates of ecological processes, and in others, assemblages with different biomass had similar rates of ecological processes. Importantly, our models of herbivory using species-specific parameters differed from those using genus-level parameters by up to 300% in rates of ecological processes, highlighting the importance of herbivore identity in this system. Our results indicate that there may be little overlap in the roles species play, suggesting that some systems may be vulnerable to loss of ecological function with the reduction or loss of just a few species. This work provides a framework that can be applied across the region to predict how changes in management may affect the ecological impact of these important herbivores.

Decoupled evolution of soft and hard substrate communities during the Cambrian Explosion and Great Ordovician Biodiversification Event.

Contrasts between the Cambrian Explosion (CE) and the Great Ordovician Biodiversification Event (GOBE) have long been recognized. Whereas the vast majority of body plans were established as a result of the CE, taxonomic increases during the GOBE were manifested at lower taxonomic levels. Assessing changes of ichnodiversity and ichnodisparity as a result of these two evolutionary events may shed light on the dynamics of both radiations. The early Cambrian (series 1 and 2) displayed a dramatic increase in ichnodiversity and ichnodisparity in softground communities. In contrast to this evolutionary explosion in bioturbation structures, only a few Cambrian bioerosion structures are known. After the middle to late Cambrian diversity plateau, ichnodiversity in softground communities shows a continuous increase during the Ordovician in both shallow- and deep-marine environments. This Ordovician increase in bioturbation diversity was not paralleled by an equally significant increase in ichnodisparity as it was during the CE. However, hard substrate communities were significantly different during the GOBE, with an increase in ichnodiversity and ichnodisparity. Innovations in macrobioerosion clearly lagged behind animal-substrate interactions in unconsolidated sediment. The underlying causes of this evolutionary decoupling are unclear but may have involved three interrelated factors: (i) a Middle to Late Ordovician increase in available hard substrates for bioerosion, (ii) increased predation, and (iii) higher energetic requirements for bioerosion compared with bioturbation.

Bioerosion in a changing world: a conceptual framework.

Bioerosion, the breakdown of hard substrata by organisms, is a fundamental and widespread ecological process that can alter habitat structure, biodiversity and biogeochemical cycling. Bioerosion occurs in all biomes of the world from the ocean floor to arid deserts, and involves a wide diversity of taxa and mechanisms with varying ecological effects. Many abiotic and biotic factors affect bioerosion by acting on the bioeroder, substratum, or both. Bioerosion also has socio-economic impacts when objects of economic or cultural value such as coastal defences or monuments are damaged. We present a unifying definition and advance a conceptual framework for (a) examining the effects of bioerosion on natural systems and human infrastructure and (b) identifying and predicting the impacts of anthropogenic factors (e.g. climate change, eutrophication) on bioerosion. Bioerosion is responding to anthropogenic changes in multiple, complex ways with significant and wide-ranging effects across systems. Emerging data further underscore the importance of bioerosion, and need for mitigating its impacts, especially at the dynamic land-sea boundary. Generalised predictions remain challenging, due to context-dependent effects and nonlinear relationships that are poorly resolved. An integrative and interdisciplinary approach is needed to understand how future changes will alter bioerosion dynamics across biomes and taxa.

A New Niche for Anoxygenic Phototrophs as Endoliths.

Anoxygenic phototrophic bacteria (APBs) occur in a wide range of aquatic habitats, from hot springs to freshwater lakes and intertidal microbial mats. Here, we report the discovery of a novel niche for APBs: endoliths within marine littoral carbonates. In a study of 40 locations around Isla de Mona, Puerto Rico, and Menorca, Spain, 16S rRNA high-throughput sequencing of endolithic community DNA revealed the presence of abundant phylotypes potentially belonging to well-known APB clades. An ad hoc phylogenetic classification of these sequences enabled us to refine the assignments more stringently. Even then, all locations contained such putative APBs, often reaching a significant proportion of all phototrophic sequences. In fact, in some 20% of samples, their contribution exceeded that of oxygenic phototrophs, previously regarded as the major type of endolithic microbe in carbonates. The communities contained representatives of APBs in the Chloroflexales, various proteobacterial groups, and Chlorobi The most abundant phylotypes varied with geography: on Isla de Mona, Roseiflexus and Chlorothrix-related phylotypes dominated, whereas those related to Erythrobacter were the most common in Menorca. The presence of active populations of APBs was corroborated through an analysis of photopigments: bacteriochlorophylls were detected in all samples, bacteriochlorophyll c and a being most abundant. We discuss the potential metabolism and geomicrobial roles of endolithic APBs. Phylogenetic inference suggests that APBs may be playing a role as photoheterotrophs, adding biogeochemical complexity to our understanding of such communities. Given the global extent of coastal carbonate platforms, they likely represent a very large and unexplored habitat for APBs.IMPORTANCE Endolithic microbial communities from carbonates, which have been explored for over 2 centuries in predominantly naturalistic studies, were thought to be primarily composed of eukaryotic algae and cyanobacteria. Our report represents a paradigm shift in this regard, at least for the marine environment, demonstrating the presence of ubiquitous and abundant populations of APBs in this habitat. It raises questions about the role of these organisms in the geological dynamics of coastal carbonates, including coral reefs.

A 3,000-year lag between the geological and ecological shutdown of Florida's coral reefs.

The global-scale degradation of coral reefs has reached a critical threshold wherein further declines threaten both ecological functionality and the persistence of reef structure. Geological records can provide valuable insights into the long-term controls on reef development that may be key to solving the modern coral-reef crisis. Our analyses of new and existing coral-reef cores from throughout the Florida Keys reef tract (FKRT) revealed significant spatial and temporal variability in reef development during the Holocene. Whereas maximum Holocene reef thickness in the Dry Tortugas was comparable to elsewhere in the western Atlantic, most of Florida's reefs had relatively thin accumulations of Holocene reef framework. During periods of active reef development, average reef accretion rates were similar throughout the FKRT at ~3 m/ky. The spatial variability in reef thickness was instead driven by differences in the duration of reef development. Reef accretion declined significantly from ~6,000 years ago to present, and by ~3,000 years ago, the majority of the FKRT was geologically senescent. Although sea level influenced the development of Florida's reefs, it was not the ultimate driver of reef demise. Instead, we demonstrate that the timing of reef senescence was modulated by subregional hydrographic variability, and hypothesize that climatic cooling was the ultimate cause of reef shutdown. The senescence of the FKRT left the ecosystem balanced at a delicate tipping point at which a veneer of living coral was the only barrier to reef erosion. Modern climate change and other anthropogenic disturbances have now pushed many reefs past that critical threshold and into a novel ecosystem state, in which reef structures built over millennia could soon be lost. The dominant role of climate in the development of the FKRT over timescales of decades to millennia highlights the potential vulnerability of both geological and ecological reef processes to anthropogenic climate change.

Acid secretion by the boring organ of the burrowing giant clam, Tridacna crocea.

The giant clam Tridacna crocea, native to Indo-Pacific coral reefs, is noted for its unique ability to bore fully into coral rock and is a major agent of reef bioerosion. However, T. crocea's mechanism of boring has remained a mystery despite decades of research. By exploiting a new, two-dimensional pH-sensing technology and manipulating clams to press their presumptive boring tissue (the pedal mantle) against pH-sensing foils, we show that this tissue lowers the pH of surfaces it contacts by greater than or equal to 2 pH units below seawater pH day and night. Acid secretion is likely mediated by vacuolar-type H+-ATPase, which we demonstrate (by immunofluorescence) is abundant in the pedal mantle outer epithelium. Our discovery of acid secretion solves this decades-old mystery and reveals that, during bioerosion, T. crocea can liberate reef constituents directly to the soluble phase, rather than producing sediment alone as earlier assumed.

Drivers and predictions of coral reef carbonate budget trajectories.

Climate change is one of the greatest threats to the long-term maintenance of coral-dominated tropical ecosystems, and has received considerable attention over the past two decades. Coral bleaching and associated mortality events, which are predicted to become more frequent and intense, can alter the balance of different elements that are responsible for coral reef growth and maintenance. The geomorphic impacts of coral mass mortality have received relatively little attention, particularly questions concerning temporal recovery of reef carbonate production and the factors that promote resilience of reef growth potential. Here, we track the biological carbonate budgets of inner Seychelles reefs from 1994 to 2014, spanning the 1998 global bleaching event when these reefs lost more than 90% of coral cover. All 21 reefs had positive budgets in 1994, but in 2005 budgets were predominantly negative. By 2014, carbonate budgets on seven reefs were comparable with 1994, but on all reefs where an ecological regime shift to macroalgal dominance occurred, budgets remained negative through 2014. Reefs with higher massive coral cover, lower macroalgae cover and lower excavating parrotfish biomass in 1994 were more likely to have positive budgets post-bleaching. If mortality of corals from the 2016 bleaching event is as severe as that of 1998, our predictions based on past trends would suggest that six of eight reefs with positive budgets in 2014 would still have positive budgets by 2030. Our results highlight that reef accretion and framework maintenance cannot be assumed from the ecological state alone, and that managers should focus on conserving aspects of coral reefs that support resilient carbonate budgets.

Environmental drivers of coral reef carbonate production and bioerosion: a multi-scale analysis.

The resilience of coral reefs depends on the balance between reef growth and reef breakdown, and their responses to changing environmental conditions. Across the 2500-km Hawaiian Archipelago, we quantified rates of carbonate production, bioerosion, and net accretion at regional, island, site, and within-site spatial scales and tested how these rates respond to environmental conditions across different spatial scales. Overall, there were four major outcomes from this study: (1) bioerosion rates were generally higher in the populated Main Hawaiian Islands (MHI) than the remote, protected Northwestern Hawaiian Islands (NWHI), while carbonate production rates did not vary significantly between the two regions; (2) variability in carbonate production, bioerosion, and net accretion rates was greatest at the smallest within-reef spatial scale; (3) carbonate production and bioerosion rates were associated with distinct sets of environmental parameters; and (4) the strongest correlates of carbonate production, bioerosion, and net accretion rates were different between the MHI region and the NWHI region: in the MHI, the dominant correlates were percent cover of macroalgae and herbivorous fish biomass for carbonate production and bioerosion, respectively, whereas in the NWHI, the top correlates were total alkalinity and benthic cover. This study highlights the need to understand accretion and erosion processes as well as local environmental conditions to predict net coral reef responses to future environmental changes.

Enhanced macroboring and depressed calcification drive net dissolution at high-CO2 coral reefs.

Ocean acidification (OA) impacts the physiology of diverse marine taxa; among them corals that create complex reef framework structures. Biological processes operating on coral reef frameworks remain largely unknown from naturally high-carbon-dioxide (CO2) ecosystems. For the first time, we independently quantified the response of multiple functional groups instrumental in the construction and erosion of these frameworks (accretion, macroboring, microboring, and grazing) along natural OA gradients. We deployed blocks of dead coral skeleton for roughly 2 years at two reefs in Papua New Guinea, each experiencing volcanically enriched CO2, and employed high-resolution micro-computed tomography (micro-CT) to create three-dimensional models of changing skeletal structure. OA conditions were correlated with decreased calcification and increased macroboring, primarily by annelids, representing a group of bioeroders not previously known to respond to OA. Incubation of these blocks, using the alkalinity anomaly methodology, revealed a switch from net calcification to net dissolution at a pH of roughly 7.8, within Intergovernmental Panel on Climate Change's (IPCC) predictions for global ocean waters by the end of the century. Together these data represent the first comprehensive experimental study of bioerosion and calcification from a naturally high-CO2 reef ecosystem, where the processes of accelerated erosion and depressed calcification have combined to alter the permanence of this essential framework habitat.