Density‐dependent effects on initial growth of a branching coral under restoration

Coral reef restoration aims to help threatened coral ecosystems recover from recent severe declines. Here we address whether coral fragments should be out‐planted individually or in larger aggregations. Theory suggests alternative possible outcomes: whereas out‐plants within aggregations might suffer from heightened negative interactions with neighbors (e.g. competition for space), they may alternatively benefit from positive interactions with neighbors (e.g. buffering wave disturbances). On a degraded reef in the Caribbean (St. Croix, USVI), using out‐plants of the critically endangered staghorn coral Acropora cervicornis, we experimentally tested how aggregation density (1–20 out‐planted coral fragments spaced at approximately 5 cm) influenced initial coral growth (over 3 months). Coral growth declined as a function of aggregation size, and out‐plants within larger aggregations had fewer and shorter secondary branches on average, indicative of horizontal competition for space. Our results therefore suggest that wide spacing of individuals will maximize the initial growth of out‐planted branching corals.     

Near‐term impacts of coral restoration on target species,coral reef community structure,and ecological processes

The global decline of corals has created an urgent need for effective, science‐based methods to augment coral populations and restore important ecosystem functions. To meet this challenge, the field of coral restoration has rapidly evolved over the past decade. However, despite widespread efforts to outplant corals and monitor survivorship, there is a shortage of information on the effects of coral restoration on reef communities or important ecosystem functions. To fill this knowledge gap, we examined the effects of restoration on three major criteria: diversity, community structure, and ecological processes. We conducted surveys of four restored sites in the Florida Keys ranging in restoration effort (500–2,300 corals outplanted) paired with surveys of nearby, unmanipulated control sites. Coral restoration successfully enhanced coral populations, increasing coral cover 4‐fold, but manifested in limited differences in coral and fish communities. Some restored sites had higher abundance of herbivorous fish, rates of herbivory, or more juvenile‐sized corals, but these effects were limited to individual reefs. Damselfish were consistently more abundant at restored compared to control sites. Despite augmenting target coral populations, 3 years of coral restoration has not facilitated many of the positive feedbacks that help reinforce coral success. In a time of increasingly frequent disturbances, it is urgent we hasten the speed at which reefs recover important ecological processes, such as herbivory and nutrient cycling, that make reefs more resistant and resilient if we are to achieve long‐term restoration success.     

Enhancing coral larval supply and seedling production using a special bundle collection system “coral larval cradle” for large‐scale coral restoration

Larval recruitment is essential for sustaining coral communities and a fundamental tool in some interventions for reef restoration. To improve larval supply and post‐settlement survival in sexually assisted coral restoration efforts, an integrated in situ collector system, the larval cradle, was designed to collect spawned gametes then culture the resulting larvae until settled on artificial substrates. The final design of the larval cradle was cylindrical, a nylon mesh structure with a volume of 9 m³, suspended in the sea and extending vertically toward the seabed. We found three key design features that improved the efficiency of the apparatus: (1) an open area of sea surface and mesh size of less than 100 μm produced high fertilization and optimal survival (>90%), (2) a special skirt‐shaped net (3 m in diameter) with a connection hose for attaching the cradle to collect bundles from many adult colonies over a wide area and at various depths, and (3) adding short square tube pieces, called square hollow sections, as a substrate for enhancing larval settlement and survival, to a larval cradle at 4 days after spawning was optimal for uniform settlement. This system allowed not only the collection of several million eggs, but also subsequent production of several thousand settled juvenile corals, without land facilities. Our design achieved several hundred times higher survival for early life stages of Acropora tenuis compared to nature.     

Recovery of plant communities after ecological restoration of forestry‐drained peatlands

Ecological restoration is expected to reverse the loss of biodiversity and ecosystem services. Due to the low number of well‐replicated field studies, the extent to which restoration recovers plant communities, and the factors underlying possible shortcomings, are not well understood even in medium term. We compared the plant community composition of 38 sites comprising pristine, forestry‐drained, and 5 or 10 years ago restored peatlands in southern Finland, with special interest in understanding spatial variation within studied sites, as well as the development of the numbers and the abundances of target species. Our results indicated a recovery of community composition 5–10 years after restoration, but there was significant heterogeneity in recovery. Plant communities farthest away from ditches were very similar to their pristine reference already 10 years after restoration. In contrast, communities in the ditches were as far from the target as the drained communities. The recovery appears to be characterized by a decline in the number and abundance of species typical to degraded conditions, and increase in the abundance of characteristic peatland species. However, we found no increase above the drained state in the number of characteristic peatland species. Our results suggest that there is a risk of drawing premature conclusions on the efficiency of ecological restoration with the current practice of short‐term monitoring. Our results also illustrate fine‐scale within‐site spatial variability in the degradation and recovery of the plant communities that should be considered when evaluating the success of restoration. Overall, we find the heterogeneous outcome of restoration observed here promising. However, low recovery in the number of characteristic species demonstrates the importance of prioritizing restoration sites, and addressing the uncertainty of recovery when setting restoration targets. It appears that it is easier to eradicate unwanted species than regain characteristic species by restoration.     

Effects of coral restoration on fish communities: snapshots of long‐term,multiregional responses and implications for practice

Coral restoration is widely used around the world to address dramatic declines in coral cover; however, very few studies have looked specifically at the temporal response of fish assemblages (i.e. abundance and diversity) to coral restoration. Several critical reef functions and processes are driven by fishes, thereby making their recovery and responses around restoration structures key indicators of success. This study evaluates fish abundance and community composition on restoration plots following 8–12 years of restoration activity, in four locations (two Caribbean and two Indo‐Pacific). Responses were very complex with region‐, site‐, and body size‐specific patterns. Overall, fish abundance only increased in Indo‐Pacific sites where damselfish responded positively to increased coral cover and topographic complexity. Restoration effects on other fish families and particularly on larger bodied reef fish were negative or neutral at all locations. If restoration initiatives are going to substantively improve the condition and recovery of degraded reef fish communities, restoration efforts need to be planned, designed, and monitored based on fish‐specific habitat requirements and locally specific community dynamics.     

An analysis of fish‐habitat associations on disturbed coral reefs: chaetodontid fishes in New Caledonia

A concordance analysis was used to study the simultaneous influence of several environmental data sets on chaetodontid (butterflyfish) distributions. This multivariate and multitable method enabled the correlation of three types of benthic characteristics (mineral substratum, coverage of structural species and large echinoderms) with butterflyfish abundances in two bays of the urban centre of Nouméa (New Caledonia). The first concordance axis was related to a gradient in the coverage of branching corals. This disturbance gradient compared damaged reef areas dominated by long‐spined sea urchins to areas with an extensive coverage of branching corals. The abundance of corallivorous chaetodontids was related to this gradient, supporting the view of corals as a food and shelter source for these fishes. The second concordance axis was interpreted as a gradient of heterogeneity in the coverage of benthic life‐forms. The abundance of omnivorous chaetodontids was related to this gradient. Thus, the concordance axes defined two key components of habitat structure that were related to the entire fish community structure.     

Sensitivity of coral calcification to ocean acidification: a meta‐analysis

To date, meta‐analyses of effects of acidification have focused on the overall strength of evidence for statistically significant responses; however, to anticipate likely consequences of ocean acidification, quantitative estimates of the magnitude of likely responses are also needed. Herein, we use random effects meta‐analysis to produce a systematically integrated measure of the distribution of magnitudes of the response of coral calcification to decreasing Ω_Arag. We also tested whether methodological and biological factors that have been hypothesized to drive variation in response magnitude explain a significant proportion of the among‐study variation. We found that the overall mean response of coral calcification is ~15% per unit decrease in Ω_Arag over the range 2 < Ω_Arag < 4. Among‐study variation is large (standard deviation of 8% per unit decrease in Ω_Arag). Neither differences in carbonate chemistry manipulation method, study duration, irradiance level, nor study species growth rate explained a significant proportion of the among‐study variation. However, studies employing buoyant weighting found significantly smaller decreases in calcification per unit Ω_Arag (~10%), compared with studies using the alkalinity anomaly technique (~25%). These differences may be due to the greater tendency for the former to integrate over light and dark calcification. If the existing body of experimental work is indeed representative of likely responses of corals in nature, our results imply that, under business as usual conditions, declines in coral calcification by end‐of‐century will be ~22%, on average, or ~15% if only studies integrating light and dark calcification are considered. These values are near the low end of published projections, but support the emerging view that variability due to local environmental conditions and species composition is likely to be substantial.     

Positive genetic associations among fitness traits support evolvability of a reef‐building coral under multiple stressors

Climate change threatens organisms in a variety of interactive ways that requires simultaneous adaptation of multiple traits. Predicting evolutionary responses requires an understanding of the potential for interactions among stressors and the genetic variance and covariance among fitness‐related traits that may reinforce or constrain an adaptive response. Here we investigate the capacity of Acropora millepora, a reef‐building coral, to adapt to multiple environmental stressors: rising sea surface temperature, ocean acidification, and increased prevalence of infectious diseases. We measured growth rates (weight gain), coral color (a proxy for Symbiodiniaceae density), and survival, in addition to nine physiological indicators of coral and algal health in 40 coral genets exposed to each of these three stressors singly and combined. Individual stressors resulted in predicted responses (e.g., corals developed lesions after bacterial challenge and bleached under thermal stress). However, corals did not suffer substantially more when all three stressors were combined. Nor were trade‐offs observed between tolerances to different stressors; instead, individuals performing well under one stressor also tended to perform well under every other stressor. An analysis of genetic correlations between traits revealed positive covariances, suggesting that selection to multiple stressors will reinforce rather than constrain the simultaneous evolution of traits related to holobiont health (e.g., weight gain and algal density). These findings support the potential for rapid coral adaptation under climate change and emphasize the importance of accounting for corals’ adaptive capacity when predicting the future of coral reefs.     

Optimizing return‐on‐effort for coral nursery and outplanting practices to aid restoration of the Great Barrier Reef

Coral nursery and outplanting practices have grown in popularity worldwide for targeted restoration of degraded “high value” reef sites, and recovery of threatened taxa. Success of these practices is commonly gauged from coral propagule growth and survival, which fundamentally determines the return‐on‐effort (RRE) critical to the cost‐effectiveness and viability of restoration programs. In many cases, RRE has been optimized from past successes and failures, which therefore presents a major challenge for locations such as the Great Barrier Reef (GBR) where no local history of restoration exists to guide best practice. In establishing the first multi‐taxa coral nursery on the GBR (Opal Reef, February 2018), we constructed a novel scoring criterion from concurrent measurements of growth and survivorship to guide our relative RRE, including nursery propagule numbers (stock density). We initially retrieved RRE scores from a database of global restoration efforts to date (n = 246; 52 studies) to evaluate whether and how success commonly varied among coral taxa. We then retrieved RRE scores for Opal Reef using initial growth and survivorship data for six key coral taxa, to demonstrate that RRE scores were high for all taxa predominantly via high survivorship over winter. Repeated RRE scoring in summer is therefore needed to capture the full dynamic range of success where seasonal factors regulating growth versus survivorship differ. We discuss how RRE scoring can be easily adopted across restoration practices globally to standardize and benchmark success, but also as a tool to aid decision‐making in optimizing future propagation (and outplanting) efforts.     

Population collapse dynamics in Acropora downingi,an Arabian/Persian Gulf ecosystem‐engineering coral,linked to rising temperature

As in the tropical Atlantic, Acropora populations in the southern Persian/Arabian Gulf plummeted within two decades after having been ecosystem engineers on most wave‐exposed reefs since the Pleistocene. Since 1996/1998 live coral cover in the Gulf declined by over 90% in many areas, primarily due to bleaching and diseases caused by rising temperatures. In the formerly dominant table‐coral species A. downingi, population dynamics corresponding to disturbance regimes was quantified in three transition matrices (lower disturbance pre‐1996; moderate disturbance from 1998 to 2010 and 2013 to 2017, disturbed in 1996/1998, 2010/11/12, 2017). Increased disturbance frequency and severity caused progressive reduction in coral size, cover, and population fecundity. Small size‐classes were bolstered more by partial colony mortality than sexual recruitment. Some large corals had a size refuge and resisted die‐back but were also lost with increasing disturbance. Matrix and biophysical larval flow models suggested one metapopulation. Southern, Arabian, populations could be connected to northern, Iranian, populations but this connectivity was lost under assumptions of pelagic larval duration at rising temperatures shortened to a third. Then, the metapopulation disintegrated into isolated populations. Connectivity required to avoid extinctions increased exponentially with disturbance frequency and correlation of disturbances across the metapopulation. Populations became unsustainable at eight disturbances in 15 years, when even highest theoretical recruitment no longer compensated mortality. This lethal disturbance frequency was 3‐fold that of the moderately disturbed monitoring period and 4‐fold of the preceding low‐disturbance period—suggesting ongoing shortening of the disturbance‐free period. Observed population collapse and environmental changes in the Gulf suggest that A. downingi is heading toward at least functional extinction mainly due to increasingly frequent temperature‐induced mortality events, clearly linked to climate change.     

Long‐term salinity tolerance is accompanied by major restructuring of the coral bacterial microbiome

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

Preliminary analysis of bacterial diversity associated with the Porites coral from the Arabian sea

It is widely reported that coral reefs are suffering degradation from a combination of stresses. We have previously reported the use of genomic tools in the study of environmental impact assessment and hypothesize that monitoring the bacterial diversity associated with a coral would indicate changes in its health before visible damage occurs. This study analyzes the bacterial diversity associated with Porites coral collected from two sites in the Arabian Sea using culture independent techniques. Two clone libraries were constructed from the16S rDNA amplicons and selected individual clones were partially sequenced. Retrieved sequences were identified by BLAST analysis and indicate the presence of unidentified bacteria. Diversity index was calculated using Shannon–Wiener index. The bacterial diversity associated with coral sample 1 gives the index of species diversity, H ₁ as 1.6287, divergence from eqiprobability as 45.708% and the evenness of the sample as 54.291. For coral sample 2, the values obtained were, H ₁ as 1.97, divergence from eqiprobability as 15.11% and the evenness of the sample as 84.88. Sequences representing bacteria related to agricultural or industrial pollution and pathogenesis were also found. Coral samples collected near a lagoon area, showed a greater percentage of sequences representing bacteria related to human interventions, indicative of pollution.     

Ecosystem‐based management of coral reefs under climate change

Coral reefs provide food and livelihoods for hundreds of millions of people as well as harbour some of the highest regions of biodiversity in the ocean. However, overexploitation, land‐use change and other local anthropogenic threats to coral reefs have left many degraded. Additionally, coral reefs are faced with the dual emerging threats of ocean warming and acidification due to rising CO₂ emissions, with dire predictions that they will not survive the century. This review evaluates the impacts of climate change on coral reef organisms, communities and ecosystems, focusing on the interactions between climate change factors and local anthropogenic stressors. It then explores the shortcomings of existing management and the move towards ecosystem‐based management and resilience thinking, before highlighting the need for climate change‐ready marine protected areas (MPAs), reduction in local anthropogenic stressors, novel approaches such as human‐assisted evolution and the importance of sustainable socialecological systems. It concludes that designation of climate change‐ready MPAs, integrated with other management strategies involving stakeholders and participation at multiple scales such as marine spatial planning, will be required to maximise coral reef resilience under climate change. However, efforts to reduce carbon emissions are critical if the long‐term efficacy of local management actions is to be maintained and coral reefs are to survive.     

Integrating trait‐based empirical and modeling research to improve ecological restoration

A global ecological restoration agenda has led to ambitious programs in environmental policy to mitigate declines in biodiversity and ecosystem services. Current restoration programs can incompletely return desired ecosystem service levels, while resilience of restored ecosystems to future threats is unknown. It is therefore essential to advance understanding and better utilize knowledge from ecological literature in restoration approaches. We identified an incomplete linkage between global change ecology, ecosystem function research, and restoration ecology. This gap impedes a full understanding of the interactive effects of changing environmental factors on the long‐term provision of ecosystem functions and a quantification of trade‐offs and synergies among multiple services. Approaches that account for the effects of multiple changing factors on the composition of plant traits and their direct and indirect impact on the provision of ecosystem functions and services can close this gap. However, studies on this multilayered relationship are currently missing. We therefore propose an integrated restoration agenda complementing trait‐based empirical studies with simulation modeling. We introduce an ongoing case study to demonstrate how this framework could allow systematic assessment of the impacts of interacting environmental factors on long‐term service provisioning. Our proposed agenda will benefit restoration programs by suggesting plant species compositions with specific traits that maximize the supply of multiple ecosystem services in the long term. Once the suggested compositions have been implemented in actual restoration projects, these assemblages should be monitored to assess whether they are resilient as well as to improve model parameterization. Additionally, the integration of empirical and simulation modeling research can improve global outcomes by raising the awareness of which restoration goals can be achieved, due to the quantification of trade‐offs and synergies among ecosystem services under a wide range of environmental conditions.     

Influence of coral cover and structural complexity on the accuracy of visual surveys of coral‐reef fish communities

Using manipulated patch reefs with combinations of varying live‐coral cover (low, medium and high) and structural complexity (low and high), common community metrics (abundance, diversity, richness and community composition) collected through standard underwater visual census techniques were compared with exhaustive collections using a fish anaesthetic (clove oil). This study showed that reef condition did not influence underwater visual census estimates at a community level, but reef condition can influence the detectability of some small and cryptic species and this may be exacerbated if surveys are conducted on a larger scale.     

Enabling regional management in a changing climate through Bayesian meta‐analysis of a large‐scale disturbance

Aim Quantifying and predicting change in large ecosystems is an important research objective for applied ecologists as human disturbance effects become increasingly evident at regional and global scales. However, studies used to make inferences about large‐scale change are frequently of uneven quality and few in number, having been undertaken to study local, rather than global, change. Our aim is to improve the quality of inferences that can be made in meta‐analyses of large‐scale disturbance by integrating studies of varying quality in a unified modelling framework that is informative for both local and regional management. Innovation Here we improve conventionally structured meta‐analysis methods by including imputation of unknown study variances and the use of Bayesian factor potentials. The approach is a coherent framework for integrating data of varying quality across multiple studies while facilitating belief statements about the uncertainty in parameter estimates and the probable outcome of future events. The approach is applied to a regional meta‐analysis of the effects of loss of coral cover on species richness and the abundance of coral‐dependent fishes in the western Indian Ocean (WIO) before and after a mass bleaching event in 1998. Main conclusions Our Bayesian approach to meta‐analysis provided greater precision of parameter estimates than conventional weighted linear regression meta‐analytical techniques, allowing us to integrate all available data from 66 available study locations in the WIO across multiple scales. The approach thereby: (1) estimated uncertainty in site‐level estimates of change, (2) provided a regional estimate for future change at any given site in the WIO, and (3) provided a probabilistic belief framework for future management of reef resources at both local and regional scales.     

Responses of coral‐associated bacterial communities to heat stress differ with Symbiodinium type on the same coral host

This study compared the effect of heat stress on coral‐associated bacterial communities among juveniles of the coral, Acropora tenuis, hosting different Symbiodinium types. In comparison to a control temperature treatment (28 °C), we documented dramatic changes in bacterial associates on juvenile corals harbouring ITS 1 type D Symbiodinium when placed in a high (32 °C) temperature treatment. In particular, there was a marked increase in the number of retrieved Vibrio affiliated sequences, which coincided with a 44% decline in the photochemical efficiency of the D‐juveniles. Interestingly, these Vibrio sequences affiliated most closely with the coral pathogen, Vibrio coralliilyticus, which has been implicated in some coral disease outbreaks. In contrast, A. tenuis hosting ITS 1 type C1 Symbiodinium did not exhibit major bacterial shifts in the elevated temperature treatment, indicating a more stable bacterial community during thermal stress; concomitantly a decline (10%) in photochemical efficiency was minimal for this group. D juveniles that had been exposed to moderately elevated sea temperatures (30 °C) in the field before being placed in the control temperature treatment displayed a decrease in the number of Vibrio affiliated sequences and bacterial profiles shifted to become more similar to profiles of corals harbouring type C1 Symbiodinium. In combination, these results demonstrate that thermal stress can result in shifts in coral‐associated bacterial communities, which may lead to deteriorating coral health. The lower resilience of A. tenuis to thermal stress when harbouring Symbiodinium D highlights the importance of inter‐kingdom interactions among the coral host, dinoflagellate endosymbiont and bacterial associates for coral health and resilience.     

Spatial and temporal genetic structure of Symbiodinium populations within a common reef‐building coral on the Great Barrier Reef

The dinoflagellate photosymbiont Symbiodinium plays a fundamental role in defining the physiological tolerances of coral holobionts, but little is known about the dynamics of these endosymbiotic populations on coral reefs. Sparse data indicate that Symbiodinium populations show limited spatial connectivity; however, no studies have investigated temporal dynamics for in hospite Symbiodinium populations following significant mortality and recruitment events in coral populations. We investigated the combined influences of spatial isolation and disturbance on the population dynamics of the generalist Symbiodinium type C2 (ITS1 rDNA) hosted by the scleractinian coral Acropora millepora in the central Great Barrier Reef. Using eight microsatellite markers, we genotyped Symbiodinium in a total of 401 coral colonies, which were sampled from seven sites across a 12‐year period including during flood plume–induced coral bleaching. Genetic differentiation of Symbiodinium was greatest within sites, explaining 70–86% of the total genetic variation. An additional 9–27% of variation was explained by significant differentiation of populations among sites separated by 0.4–13 km, which is consistent with low levels of dispersal via water movement and historical disturbance regimes. Sampling year accounted for 6–7% of total genetic variation and was related to significant coral mortality following severe bleaching in 1998 and a cyclone in 2006. Only 3% of the total genetic variation was related to coral bleaching status, reflecting generally small (8%) reductions in allelic diversity within bleached corals. This reduction probably reflected a loss of genotypes in hospite during bleaching, although no site‐wide changes in genetic diversity were observed. Combined, our results indicate the importance of disturbance regimes acting together with limited oceanographic transport to determine the genetic composition of Symbiodinium types within reefs.