Seq' and ARMS shall find: DNA (meta)barcoding of Autonomous Reef Monitoring Structures across the tree of life uncovers hidden cryptobiome of tropical urban coral reefs.

Coral reefs are among the richest marine ecosystems on Earth, but there remains much diversity hidden within cavities of complex reef structures awaiting discovery. While the abundance of corals and other macroinvertebrates are known to influence the diversity of other reef-associated organisms, much remains unknown on the drivers of cryptobenthic diversity. A combination of standardized sampling with 12 units of the Autonomous Reef Monitoring Structure (ARMS) and high-throughput sequencing was utilized to uncover reef cryptobiome diversity across the equatorial reefs in Singapore. DNA barcoding and metabarcoding of mitochondrial cytochrome c oxidase subunit I, nuclear 18S and bacterial 16S rRNA genes revealed the taxonomic composition of the reef cryptobiome, comprising 15,356 microbial ASVs from over 50 bacterial phyla, and 971 MOTUs across 15 metazoan and 19 non-metazoan eukaryote phyla. Environmental factors across different sites were tested for relationships with ARMS diversity. Differences among reefs in diversity patterns of metazoans and other eukaryotes, but not microbial communities, were associated with biotic (coral cover) and abiotic (distance, temperature and sediment) environmental variables. In particular, ARMS deployed at reefs with higher coral cover had greater metazoan diversity and encrusting plate cover, with larger-sized non-coral invertebrates influencing spatial patterns among sites. Our study showed that DNA barcoding and metabarcoding of ARMS constitute a valuable tool for quantifying cryptobenthic diversity patterns and can provide critical information for the effective management of coral reef ecosystems.

Macroalgae exhibit diverse responses to human disturbances on coral reefs.

Scientists and managers rely on indicator taxa such as coral and macroalgal cover to evaluate the effects of human disturbance on coral reefs, often assuming a universally positive relationship between local human disturbance and macroalgae. Despite evidence that macroalgae respond to local stressors in diverse ways, there have been few efforts to evaluate relationships between specific macroalgae taxa and local human-driven disturbance. Using genus-level monitoring data from 1205 sites in the Indian and Pacific Oceans, we assess whether macroalgae percent cover correlates with local human disturbance while accounting for factors that could obscure or confound relationships. Assessing macroalgae at genus level revealed that no genera were positively correlated with all human disturbance metrics. Instead, we found relationships between the division or genera of algae and specific human disturbances that were not detectable when pooling taxa into a single functional category, which is common to many analyses. The convention to use percent cover of macroalgae as an indication of local human disturbance therefore likely obscures signatures of local anthropogenic threats to reefs. Our limited understanding of relationships between human disturbance, macroalgae taxa, and their responses to human disturbances impedes the ability to diagnose and respond appropriately to these threats.

Corals in the hottest reefs in the world exhibit symbiont fidelity not flexibility.

Reef-building corals are at risk of extinction from ocean warming. While some corals can enhance their thermal limits by associating with dinoflagellate photosymbionts of superior stress tolerance, the extent to which symbiont communities will reorganize under increased warming pressure remains unclear. Here we show that corals in the hottest reefs in the world in the Persian Gulf maintain associations with the same symbionts across 1.5 years despite extreme seasonal warming and acute heat stress (≥35°C). Persian Gulf corals predominantly associated with Cladocopium (clade C) and most also hosted Symbiodinium (clade A) and/or Durusdinium (clade D). This is in contrast to the neighbouring and milder Oman Sea, where corals associated with Durusdinium and only a minority hosted background levels of Cladocopium. During acute heat stress, the higher prevalence of Symbiodinium and Durusdinium in bleached versus nonbleached Persian Gulf corals indicates that genotypes of these background genera did not confer bleaching resistance. Within symbiont genera, the majority of ITS2 rDNA type profiles were unique to their respective coral species, confirming the existence of host-specific symbiont lineages. Notably, further differentiation among Persian Gulf sites demonstrates that symbiont populations are either isolated or specialized over tens to hundreds of kilometres. Thermal tolerance across coral species was associated with the prevalence of a single ITS2 intragenomic sequence variant (C3gulf), definitive of the Cladocopium thermophilum group. The abundance of C3gulf was highest in bleaching-resistant corals and at warmer sites, potentially indicating a specific symbiont genotype (or set of genotypes) that may play a role in thermal tolerance that warrants further investigation. Together, our findings indicate that co-evolution of host-Symbiodiniaceae partnerships favours fidelity rather than flexibility in extreme environments and under future warming.

Fear effects associated with predator presence and habitat structure interact to alter herbivory on coral reefs.

Non-consumptive fear effects are an important determinant of foraging decisions by consumers across a range of ecosystems. However, how fear effects associated with the presence of predators interact with those associated with habitat structure remain unclear. Here, we used predator fish models (Plectropomus leopardus) and experimental patches of the macroalga Sargassum ilicifolium of varying densities to investigate how predator- and habitat-associated fear effects influence herbivory on coral reefs. We found the removal of macroalgal biomass (i.e. herbivory) was shaped by the interaction between predator- and habitat-associated fear effects. Rates of macroalgal removal declined with increasing macroalgal density, likely due to increased visual occlusion by denser macroalgae patches and reduced ability of herbivorous fishes to detect the predators. The presence of the predator model reduced herbivory within low macroalgal density plots, but not within medium- and high-density macroalgal plots. Our results suggest that fear effects due to predator presence were greatest at low macroalgal density, yet these effects were lost at higher densities possibly due to greater predation risk associated with habitat structure and/or the inability of herbivorous fishes to detect the predator model.

Seasonal variation of Sargassum ilicifolium (Phaeophyceae) growth on equatorial coral reefs.

Temporal and spatial variations in Sargassum ilicifolium thallus density and length were investigated on equatorial coral reefs in Singapore from November 2011 to October 2012. Thalli density varied little throughout the year, however, we found strong seasonal patterns in thallus length and identified temperature as the significant driver. Sargassum ilicifolium reached maximum length in December (110.39 ± 2.37 cm) during periods of cooler water temperatures, and minimum length in May (9.88 ± 0.48 cm) during periods of warmer water temperatures. Significant spatial variation was also observed for both thallus density and length of S. ilicifolium among reefs. Within reefs, densities of S. ilicifolium were higher on reef flats (20.40 ± 0.40 individuals · 0.25 m-2 ) compared to upper reef slopes (5.66 ± 0.23 individuals · 0.25 m-2 ). Our findings highlight that marked seasonality in the growth of canopy-forming macroalgae can occur within equatorial reef systems where temperature ranges are restricted (<3°C).

Coral mass spawning predicted by rapid seasonal rise in ocean temperature.

Coral spawning times have been linked to multiple environmental factors; however, to what extent these factors act as generalized cues across multiple species and large spatial scales is unknown. We used a unique dataset of coral spawning from 34 reefs in the Indian and Pacific Oceans to test if month of spawning and peak spawning month in assemblages of Acropora spp. can be predicted by sea surface temperature (SST), photosynthetically available radiation, wind speed, current speed, rainfall or sunset time. Contrary to the classic view that high mean SST initiates coral spawning, we found rapid increases in SST to be the best predictor in both cases (month of spawning: R(2) = 0.73, peak: R(2) = 0.62). Our findings suggest that a rapid increase in SST provides the dominant proximate cue for coral mass spawning over large geographical scales. We hypothesize that coral spawning is ultimately timed to ensure optimal fertilization success.

Global human footprint on the linkage between biodiversity and ecosystem functioning in reef fishes.

Difficulties in scaling up theoretical and experimental results have raised controversy over the consequences of biodiversity loss for the functioning of natural ecosystems. Using a global survey of reef fish assemblages, we show that in contrast to previous theoretical and experimental studies, ecosystem functioning (as measured by standing biomass) scales in a non-saturating manner with biodiversity (as measured by species and functional richness) in this ecosystem. Our field study also shows a significant and negative interaction between human population density and biodiversity on ecosystem functioning (i.e., for the same human density there were larger reductions in standing biomass at more diverse reefs). Human effects were found to be related to fishing, coastal development, and land use stressors, and currently affect over 75% of the world's coral reefs. Our results indicate that the consequences of biodiversity loss in coral reefs have been considerably underestimated based on existing knowledge and that reef fish assemblages, particularly the most diverse, are greatly vulnerable to the expansion and intensity of anthropogenic stressors in coastal areas.

The growing need for sustainable ecological management of marine communities of the Persian Gulf.

The Persian Gulf is a semi-enclosed marine system surrounded by eight countries, many of which are experiencing substantial development. It is also a major center for the oil industry. The increasing array of anthropogenic disturbances may have substantial negative impacts on marine ecosystems, but this has received little attention until recently. We review the available literature on the Gulfs marine environment and detail our recent experience in the United Arab Emirates (U.A.E.) to evaluate the role of anthropogenic disturbance in this marine ecosystem. Extensive coastal development may now be the single most important anthropogenic stressor. We offer suggestions for how to build awareness of environmental risks of current practices, enhance regional capacity for coastal management, and build cooperative management of this important, shared marine system. An excellent opportunity exists for one or more of the bordering countries to initiate a bold and effective, long-term, international collaboration in environmental management for the Gulf.

Growth and carbonate production of crustose coralline algae on a degraded turbid reef system.

Crustose coralline algae (CCA) and other encrusting calcifiers drive carbonate production on coral reefs. However, little is known about the rates of growth and calcification of these organisms within degraded turbid reef systems. Here we deployed settlement cards (N = 764) across seven reefs in Singapore for two years to examine spatio-temporal variation in encrusting community composition and CCA carbonate production. Our results showed that CCA was the dominant encrusting taxa (63.7% ± 18.3SD) across reefs. CCA carbonate production rates (0.009-0.052 g cm-2 yr-1) were less than half of those reported for most Indo-Pacific reefs, but similar to other turbid reef systems. Highest CCA carbonate production rates were observed furthest from Singapore's main shipping port, due to a relative increase in CCA cover on the offshore reefs. Our results suggest that proximity to areas of high industrialisation and ship traffic may reduce the cover of encrusting calcifying organisms and CCA production rates which may have negative, long-term implications for the stabilisation of nearshore reefs in urbanised settings.

An Indo-Pacific coral spawning database.

The discovery of multi-species synchronous spawning of scleractinian corals on the Great Barrier Reef in the 1980s stimulated an extraordinary effort to document spawning times in other parts of the globe. Unfortunately, most of these data remain unpublished which limits our understanding of regional and global reproductive patterns. The Coral Spawning Database (CSD) collates much of these disparate data into a single place. The CSD includes 6178 observations (3085 of which were unpublished) of the time or day of spawning for over 300 scleractinian species in 61 genera from 101 sites in the Indo-Pacific. The goal of the CSD is to provide open access to coral spawning data to accelerate our understanding of coral reproductive biology and to provide a baseline against which to evaluate any future changes in reproductive phenology.

Effects of macroalgae on coral fecundity in a degraded coral reef system.

Global declines in live coral cover and the proliferation of macroalgae on coral reefs is leading to increased coral-macroalgal interactions that impact reef recovery. However, the effects of macroalgae on coral sexual reproduction-a fundamental life-history process for maintaining population abundances-have rarely been quantified. Here, we examined the direct effects of macroalgae contact on the fecundity (eggs mesentery-1) of two coral species, Echinopora lamellosa and Merulina ampliata, across three degraded reefs in Singapore. Increasing macroalgae contact from 5% to 25% significantly reduced fecundity in colonies of both species by 67-82%, and also reduced M. ampliata egg sizes by 11.4%. These results suggest the diversion of energy from reproduction towards other processes such as repair and defence, and also reveal potential differential energy allocation strategies among coral taxa. While corals on Singapore's impacted reefs continue to produce eggs, increasing macroalgae that suppresses coral fecundity may constrain future reef recovery.

National-scale marine bioregions for the Southwest Pacific.

Existing marine bioregions covering the Pacific Ocean are conceptualised at spatial scales that are too broad for national marine spatial planning. Here, we developed the first combined oceanic and coastal marine bioregionalisation at national scales, delineating 262 deep-water and 103 reef-associated bioregions across the southwest Pacific. The deep-water bioregions were informed by thirty biophysical environmental variables. For reef-associated environments, records for 806 taxa at 7369 sites were used to predict the probability of observing taxa based on environmental variables. Both deep-water and reef-associated bioregions were defined with cluster analysis applied to the environmental variables and predicted species observation probabilities, respectively to classify areas with high taxonomic similarity. Local experts further refined the delineation of the bioregions at national scales for four countries. This work provides marine bioregions that enable the design of ecologically representative national systems of marine protected areas within offshore and inshore environments in the Pacific.

Allelopathic effects of macroalgae on Pocillopora acuta coral larvae.

Allelopathy has been proposed as a key mechanism mediating coral-algal interactions; however, few studies have tested macroalgal allelochemicals on coral larvae. In this study, we examined the effects of crude extracts from four macroalgal species on Pocillopora acuta larvae under different exposure conditions. Larval mortality increased considerably with increasing concentrations of Bryopsis sp., Endosiphonia horrida, and Lobophora sp. extracts. Increasing E. horrida and Lobophora sp. extract concentrations also substantially decreased larval settlement. No detectable effects on larvae were observed in Hypnea pannosa extracts. Further, while larval mortality increased with exposure duration to Lobophora sp. extracts, larval settlement was enhanced at 12 h exposure, but reduced at shorter and longer durations. Our results emphasize that macroalgal chemical effects are highly dependent on macroalgal species and exposure conditions. On reefs dominated by allelopathic macroalgae, the survivorship and settlement of coral larvae are potentially constrained, thereby limiting the recovery of degraded reefs.

Social-environmental drivers inform strategic management of coral reefs in the Anthropocene.

Without drastic efforts to reduce carbon emissions and mitigate globalized stressors, tropical coral reefs are in jeopardy. Strategic conservation and management requires identification of the environmental and socioeconomic factors driving the persistence of scleractinian coral assemblages-the foundation species of coral reef ecosystems. Here, we compiled coral abundance data from 2,584 Indo-Pacific reefs to evaluate the influence of 21 climate, social and environmental drivers on the ecology of reef coral assemblages. Higher abundances of framework-building corals were typically associated with: weaker thermal disturbances and longer intervals for potential recovery; slower human population growth; reduced access by human settlements and markets; and less nearby agriculture. We therefore propose a framework of three management strategies (protect, recover or transform) by considering: (1) if reefs were above or below a proposed threshold of >10% cover of the coral taxa important for structural complexity and carbonate production; and (2) reef exposure to severe thermal stress during the 2014-2017 global coral bleaching event. Our findings can guide urgent management efforts for coral reefs, by identifying key threats across multiple scales and strategic policy priorities that might sustain a network of functioning reefs in the Indo-Pacific to avoid ecosystem collapse.

Urban coral reefs: Degradation and resilience of hard coral assemblages in coastal cities of East and Southeast Asia.

Given predicted increases in urbanization in tropical and subtropical regions, understanding the processes shaping urban coral reefs may be essential for anticipating future conservation challenges. We used a case study approach to identify unifying patterns of urban coral reefs and clarify the effects of urbanization on hard coral assemblages. Data were compiled from 11 cities throughout East and Southeast Asia, with particular focus on Singapore, Jakarta, Hong Kong, and Naha (Okinawa). Our review highlights several key characteristics of urban coral reefs, including "reef compression" (a decline in bathymetric range with increasing turbidity and decreasing water clarity over time and relative to shore), dominance by domed coral growth forms and low reef complexity, variable city-specific inshore-offshore gradients, early declines in coral cover with recent fluctuating periods of acute impacts and rapid recovery, and colonization of urban infrastructure by hard corals. We present hypotheses for urban reef community dynamics and discuss potential of ecological engineering for corals in urban areas.

Abundance and composition of juvenile corals reveals divergent trajectories for coral assemblages across the United Arab Emirates.

Marked shifts in the composition of coral assemblages are occurring at many locations, but it is unknown whether these are permanent shifts reinforced by patterns of population replenishment. This study examined the composition of juvenile coral assemblages across the United Arab Emirates (UAE). Densities of juvenile corals varied significantly among locations, but were highest where coral cover was highest. Juvenile coral assemblages within the Persian Gulf were dominated by Porites, while no Acropora were recorded. We expect therefore, continued declines in Acropora abundance, while observed dominance of Porites is likely to persist. In the Oman Sea, Pocillopora was the dominant juvenile coral, with Acropora and Stylophora also recorded. This study shows that taxonomic differences in replenishment are reinforcing temporal shifts in coral composition within the southern Persian Gulf, but not in the Oman Sea. Differences in environmental conditions and disturbance regimes likely explain the divergent responses between regions.

Macroalgal browsing on a heavily degraded, urbanized equatorial reef system.

The removal of macroalgal biomass is critical to the health of coral reef ecosystems. Previous studies on relatively intact reefs with diverse and abundant fish communities have quantified rapid removal of macroalgae by herbivorous fishes, yet how these findings relate to degraded reef systems where fish diversity and abundance are markedly lower and algal biomass substantially higher, is unclear. We surveyed roving herbivorous fish communities and quantified their capacity to remove the dominant macroalga Sargassum ilicifolium on seven reefs in Singapore; a heavily degraded urbanized reef system. The diversity and abundance of herbivorous fishes was extremely low, with eight species and a mean abundance ~1.1 individuals 60 m-2 recorded across reefs. Consumption of S. ilicifolium varied with distance from Singapore's main port with consumption being 3- to 17-fold higher on reefs furthest from the port (Pulau Satumu: 4.18 g h-1; Kusu Island: 2.38 g h-1) than reefs closer to the port (0.35-0.78 g h-1). Video observations revealed a single species, Siganus virgatus, was almost solely responsible for removing S. ilicifolium biomass, accounting for 83% of the mass-standardized bites. Despite low herbivore diversity and intense urbanization, macroalgal removal by fishes on some Singaporean reefs was directly comparable to rates reported for other inshore Indo-Pacific reefs.

Prickly business: abundance of sea urchins on breakwaters and coral reefs in Dubai.

Echinometra mathaei is a common echinoid on tropical reefs and where abundant plays an important role in the control of algal communities. Despite high prevalence of E. mathaei on southern Persian/Arabian Gulf reefs, their abundance and distribution is poorly known. Spatial and temporal patterns in population abundance were examined at 12 sites between breakwater and natural reef habitats in Dubai (UAE) every 3 months from 2008 to 2010. Within the breakwater habitat, densities were greatest at shallow wave-exposed sites, and reduced with both decreasing wave-exposure and increasing depth. Interestingly, E. mathaei were significantly more abundant on exposed breakwaters than natural reef sites, presumably due to differences in habitat structure and benthic cover. Population abundances differed seasonally, with peak abundances during summer (July-September) and lower abundances in winter (December-February). Seasonal fluctuations are likely the result of peak annual recruitment pulses coupled with increased fish predation from summer to winter.

The implications of recurrent disturbances within the world's hottest coral reef.

Determining how coral ecosystems are structured within extreme environments may provide insights into how coral reefs are impacted by future climate change. Benthic community structure was examined within the Persian Gulf, and adjacent Musandam and northern Oman regions across a 3-year period (2008-2011) in which all regions were exposed to major disturbances. Although there was evidence of temporal switching in coral composition within regions, communities predominantly reflected local environmental conditions and the disturbance history of each region. Gulf reefs showed little change in coral composition, being dominated by stress-tolerant Faviidae and Poritidae across the 3 years. In comparison, Musandam and Oman coral communities were comprised of stress-sensitive Acroporidae and Pocilloporidae; Oman communities showed substantial declines in such taxa and increased cover of stress-tolerant communities. Our results suggest that coral communities may persist within an increasingly disturbed future environment, albeit in a much more structurally simple configuration.

Species-specific trends in the reproductive output of corals across environmental gradients and bleaching histories.

Coral populations in the Persian Gulf have a reputation for being some of the toughest in the world yet little is known about the energetic constraints of living under temperature and salinity extremes. Energy allocation for sexual reproduction in Gulf corals was evaluated relative to conspecifics living under milder environmental conditions in the Oman Sea. Fecundity was depressed at Gulf sites in two Indo-Pacific merulinid species (Cyphastrea microphthalma and Platygyra daedalea) but not in a regionally endemic acroporid (Acropora downingi). Gulf populations of each species experienced high temperature bleaching at the onset of gametogenesis in the study but fecundity was only negatively impacted in P. daedalea and A. downingi. Large population sizes of C. microphthalma and P. daedalea in the Gulf are expected to buffer reductions on colony-level fecundity. However, depleted population sizes of A. downingi at some Gulf sites equate to low reef-wide fecundity and likely impede outcrossing success.