Effects of Madagascar marine reserves on juvenile and adult coral abundance, and the implication for population regulation.

Recruitment is a critical component in the dynamics of coral assemblages, and a key question is to determine the degree to which spatial heterogeneity of adults is influenced by pre-vs. post-settlement processes. We analyzed the density of juvenile and adult corals among 18 stations located at three regions around Madagascar, and examined the effects of Marine Protected Areas (MPAs). Our survey did not detect a positive effect of MPAs on juveniles, except for Porites at the study scale. The MPA effect was more pronounced for adults, notably for Acropora, Montipora, Seriatopora, and Porites at the regional scale. For most dominant genera, densities of juveniles and adults were positively correlated at the study scale, and at least at one of the three regions. These outcomes suggest recruitment-limitation relationships for several coral taxa, although differences in post-settlement events may be sufficiently strong to distort the pattern established at settlement for other populations. The modest benefits of MPAs on the density of juvenile corals demonstrated here argue in favor of strengthening conservation measures more specifically focused to protect recruitment processes.

Coral reef structural complexity loss exposes coastlines to waves.

Coral reefs offer natural coastal protection by attenuating incoming waves. Here we combine unique coral disturbance-recovery observations with hydrodynamic models to quantify how structural complexity dissipates incoming wave energy. We find that if the structural complexity of healthy coral reefs conditions is halved, extreme wave run-up heights that occur once in a 100-years will become 50 times more frequent, threatening reef-backed coastal communities with increased waves, erosion, and flooding.

A contemporary baseline of Madagascar's coral assemblages: Reefs with high coral diversity, abundance, and function associated with marine protected areas.

Madagascar is a major hotspot of biodiversity in the Western Indian Ocean, but, as in many other regions, coral reefs surrounding the island confront large-scale disturbances and human-induced local stressors. Conservation actions have been implemented with encouraging results for fisheries, though their benefit on coral assemblages has never been rigorously addressed. In this context, we analyzed the multiscale spatial variation of the composition, generic richness, abundance, life history strategies, and cover of coral assemblages among 18 stations placed at three regions around the island. The potential influences of marine protected areas (MPAs), algal cover, substrate rugosity, herbivorous fish biomass, and geographic location were also analyzed. Our results highlight the marked spatial variability, with variation at either or both regional and local scales for all coral descriptors. The northeast coastal region of Masoala was characterized by the high abundance of coral colonies, most notably of the competitive Acropora and Pocillopora genera and stress-tolerant taxa at several stations. The southwest station of Salary Nord was distinguished by lower abundances, with depauperate populations of competitive taxa. On the northwest coast, Nosy-Be was characterized by higher diversity and abundance as well as by high coral cover (~42-70%) recorded at unfished stations. Results clearly underline the positive effects of MPAs on all but one of the coral descriptors, particularly at Nosy-Be where the highest contrast between fished and unfished stations was observed. Biomass of herbivorous fishes, crustose coralline algae cover, and substrate rugosity were also positively related to several coral descriptors. The occurrence of reefs with high diversity, abundance, and cover of corals, including the competitive Acropora, is a major finding of this study. Our results strongly support the implementation of locally managed marine areas with strong involvement by primary users, particularly to assist in management in countries with reduced logistic and human resources such as Madagascar.

Species and population genomic differentiation in Pocillopora corals (Cnidaria, Hexacorallia).

Correctly delimiting species and populations is a prerequisite for studies of connectivity, adaptation and conservation. Genomic data are particularly useful to test species differentiation for organisms with few informative morphological characters or low discrimination of cytoplasmic markers, as in Scleractinians. Here we applied Restriction site Associated DNA sequencing (RAD-sequencing) to the study of species differentiation and genetic structure in populations of Pocillopora spp. from Oman and French Polynesia, with the objectives to test species hypotheses, and to study the genetic structure among sampling sites within species. We focused here on coral colonies morphologically similar to P. acuta (damicornis type ß). We tested the impact of different filtering strategies on the stability of the results. The main genetic differentiation was observed between samples from Oman and French Polynesia. These samples corresponded to different previously defined primary species hypotheses (PSH), i.e., PSHs 12 and 13 in Oman, and PSH 5 in French Polynesia. In Oman, we did not observe any clear differentiation between the two putative species PSH 12 and 13, nor between sampling sites. In French Polynesia, where a single species hypothesis was studied, there was no differentiation between sites. Our analyses allowed the identification of clonal lineages in Oman and French Polynesia. The impact of clonality on genetic diversity is discussed in light of individual-based simulations.

The war of corals: patterns, drivers and implications of changing coral competitive performances across reef environments.

Amidst global environmental changes, predicting species' responses to future environments is a critical challenge for preserving biodiversity and associated human benefits. We explored the original idea that coral competitive performances, the ability of corals to preempt ecological space on the reef through territorial warfare, serve as indicators of species' ecological niches and environmental windows, and therefore, responses to future environments. Our surveys indicated that coral performances varied with taxonomic identity, size and position along environmental gradients, highlighting complex interplays between life-history, warfare-strategy and niche segregation. Our results forewarn that growing alterations of coastal environments may trigger shifts in coral dominance, with the decline of major reef-building taxa like acroporids, and emphasize the importance of limiting human impacts for coastal resilience. Our empirical approach untangles the complexity of species' battle-like interactions and can help identify winners and losers in various communities caught in the interplay between ecological niches, environmental windows and global changes.

Scaling up calcification, respiration, and photosynthesis rates of six prominent coral taxa.

Coral reefs provide a range of important services to humanity, which are underpinned by community-level ecological processes such as coral calcification. Estimating these processes relies on our knowledge of individual physiological rates and species-specific abundances in the field. For colonial animals such as reef-building corals, abundance is frequently expressed as the relative surface cover of coral colonies, a metric that does not account for demographic parameters such as coral size. This may be problematic because many physiological rates are directly related to organism size, and failure to account for linear scaling patterns may skew estimates of ecosystem functioning. In the present study, we characterize the scaling of three physiological rates - calcification, respiration, and photosynthesis - considering the colony size for six prominent, reef-building coral taxa in Mo'orea, French Polynesia. After a seven-day acclimation period in the laboratory, we quantified coral physiological rates for three hours during daylight (i.e., calcification and gross photosynthesis) and one hour during night light conditions (i.e., dark respiration). Our results indicate that area-specific calcification rates are higher for smaller colonies across all taxa. However, photosynthesis and respiration rates remain constant over the colony-size gradient. Furthermore, we revealed a correlation between the demographic dynamics of coral genera and the ratio between net primary production and calcification rates. Therefore, intraspecific scaling of reef-building coral physiology not only improves our understanding of community-level coral reef functioning but it may also explain species-specific responses to disturbances.

Juvenile corals underpin coral reef carbonate production after disturbance.

Sea-level rise is predicted to cause major damage to tropical coastlines. While coral reefs can act as natural barriers for ocean waves, their protection hinges on the ability of scleractinian corals to produce enough calcium carbonate (CaCO3 ) to keep up with rising sea levels. As a consequence of intensifying disturbances, coral communities are changing rapidly, potentially reducing community-level CaCO3 production. By combining colony-level physiology and long-term monitoring data, we show that reefs recovering from major disturbances can produce 40% more CaCO3 than currently estimated due to the disproportionate contribution of juvenile corals. However, the buffering effect of highly productive juvenile corals is compromised by recruitment failures, which have been more frequently observed after large-scale, repeated bleaching events. While the size structure of corals can bolster a critical ecological function on reefs, climate change impacts on recruitment may undermine this buffering effect, thus further compromising the persistence of reefs and their provision of important ecosystem services.

Quantifying and addressing the prevalence and bias of study designs in the environmental and social sciences.

Building trust in science and evidence-based decision-making depends heavily on the credibility of studies and their findings. Researchers employ many different study designs that vary in their risk of bias to evaluate the true effect of interventions or impacts. Here, we empirically quantify, on a large scale, the prevalence of different study designs and the magnitude of bias in their estimates. Randomised designs and controlled observational designs with pre-intervention sampling were used by just 23% of intervention studies in biodiversity conservation, and 36% of intervention studies in social science. We demonstrate, through pairwise within-study comparisons across 49 environmental datasets, that these types of designs usually give less biased estimates than simpler observational designs. We propose a model-based approach to combine study estimates that may suffer from different levels of study design bias, discuss the implications for evidence synthesis, and how to facilitate the use of more credible study designs.

Diversity, structure and demography of coral assemblages on underwater lava flows of different ages at Reunion Island and implications for ecological succession hypotheses.

Understanding colonization of new habitats and ecological successions is key to ecosystem conservation. However, studies on primary successions are scarce for reef-building corals, due to the rarity of newly formed substratum and the long-term monitoring efforts required for their long life cycle and slow growth rate. We analysed data describing the diversity, structure and demography of coral assemblages on lava flows of different ages and coral reefs at Reunion Island, to evaluate the strength and mechanisms of succession, and its agreement to the theoretical models. No significant differences were observed between the two habitats for most structure and demographic descriptors. In contrast, species richness and composition differentiated coral reefs from lava flows, but were not related to the age of the lava flow. We observed a strong dominance of Pocillopora colonies, which underline the opportunistic nature of this taxa, with life-history traits advantageous to dominance on primary and secondary successional stages. Although some results argue in favor of the tolerance model of succession, the sequences of primary successions as theorized in other ecosystems were difficult to observe, which is likely due to the high frequency and intensity of disturbances at Reunion, that likely distort or set back the expected successional sequences.

Temperature affects the reproductive outputs of coral-eating starfish Acanthaster spp. after adult exposure to near-future ocean warming and acidification.

Outbreaks of the coral-eating crown-of-thorns starfish Acanthaster spp. (COTS) have become to be amongst the most severe threats to coral reefs worldwide. Although most research has focused on COTS early development, it remains unclear how COTS populations will keep pace with changing ocean conditions. Since reproduction is a key process contributing to outbreaks, we investigated the reproductive success of adult COTS acclimated for 3-4 months to different treatment combinations of ambient conditions, ocean warming (+2 °C) and acidification (-0.35 pH). Our results suggest that the optimal breeding season in New Caledonia is concentrated around the end of the calendar year, when water temperature reaches >26 °C. We found negative effects of temperature on egg metrics, fertilisation success, and GSI, conflicting with previously documented effects of temperature on echinoderm reproductive outputs. Fertilisation success dropped drastically (more than threefold) with elevated temperature during the late breeding season. In contrast, we detected no effects of near-future acidification conditions on fertilisation success nor GSI. This is the first time that COTS reproduction is compared among individuals acclimated to different conditions of warming and acidification. Our results highlight the importance of accounting for adult exposure to better understand how COTS reproduction may be impacted in the face of global change.

Citizen Science, a promising tool for detecting and monitoring outbreaks of the crown-of-thorns starfish Acanthaster spp.

Monitoring potentially devastating coral-eating crown-of-thorns starfish (COTS) populations at scales relevant to management is a challenging task. Here, we investigated a citizen science approach to detect COTS outbreaks and prioritize management responses. Between 2014 and 2018, 38 000 COTS were recorded through 641 online observation reports submitted across New Caledonia, Vanuatu and Fiji by private stakeholders (51%), NGOs (22%), business operator (11%), research/government agencies (16%). COTS were observed in multiple areas, including in remote/inhabited reefs where they had never been reported. A three-level classification was developed to discriminate risk areas and propose operational guidelines to streamline management actions. About two-thirds of reports had low abundances (<10 starfish sighted) and could be addressed with low priority. Verification surveys at 65 reef sites confirmed outbreaks in half of the cases, along with high peak densities (7 000 ind.ha-1). Combining professional and non-professional observers increased the detection range (+27%) and the number of COTS detections (+129%). Citizen reports were eventually followed by removal campaigns organized within diverse institutional frameworks. While citizen monitoring has intrinsic limitations, we advocate that it constitutes a complementary and promising approach to support the ongoing management efforts in all countries affected by COTS.

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.

Recent and old duplications in crustaceans "Internal Transcribed Spacer 1″: structural and phylogenetic implications.

Internal Transcribed Spacer structures are important in preserving accessibility to specific enzymes for the maturation of rRNAs. ITS1 sequences reported in the literature in Crustaceans range between 182 and 820 bp and are characterized by the absence of repeats or the presence of only a limited number of microsatellites. Here, we sequenced ITS1 for a range of shrimp families (infraorder Caridea) and show that most taxa have much larger ITS1 sequences. We find a high number of microsatellites in Alpheus hebes and Crangon crangon and we report repeat units in Pandalidae, Palaemonidae and mainly in Alpheidae species. Up to four repeats were found in A. vanderbilti (1915 bp), A. rostratus (1635 bp) and A. lottini (1625 bp). In general, four helices were found in ITS1. Repeat units led to extra hairpins and loops. No conserved positions occurred except in helix 4. Three clades were defined in A. lottini for the first time. We estimated the ITS1 divergence rate for the three clades of A. lottini collected in French Polynesia using existing calibrations of substitution rates. Rates of sequence evolution are largely influenced by repeat units, which likely evolve separately. By comparison with COI marker, we estimated the divergence rate of the whole ITS1 sequence to range from 0.5 to 1.4% Pmy and between 0.12 and 0.5% for the 3' end of ITS1 located outside the repeat units. Given the degree of identity between repeats, we suggest that a duplication event recently occurred in A. floridanus (98% identity) whereas an ancient duplication happened in A. sulcatus (50% identity) early at the origination of the group Alpheidae, approximately 50 mya ago. In conclusion, our results highlight an over representation of shorter ITS1 sequences in public repositories, and underlines the importance to further understand patterns of molecular evolution of this functionally important gene.

Multiscale variability in coral recruitment in the Mascarene Islands: From centimetric to geographical scale.

Coral recruitment refers to the processes allowing maintenance and renewal of coral communities. Recruitment success is therefore indispensable for coral reef recovery after disturbances. Recruitment processes are governed by a variety of factors occurring at all spatial and temporal scales, from centimetres to hundreds of kilometres. In the present context of rising disturbances, it is thus of major importance to better understand the relative importance of different scales in this variation, and when possible, the factors associated with these scales. Multiscale spatio-temporal variability of scleractinian coral recruitment was investigated at two of the Mascarene Islands: Reunion and Rodrigues. Recruitment rates and taxonomic composition were examined during three consecutive six-month periods from regional to micro-local scales (i.e. from hundreds of kilometres to few centimetres) and between two protection levels (no-take zones and general protection zones). Very low recruitment rates were observed. Rodrigues displayed lower recruitment rates than Reunion. Recruit assemblage was dominated by Pocilloporidae (77.9%), followed by Acroporidae (9.9%) and Poritidae (5.2%). No protection effect was identified on coral recruitment, despite differences in recruitment rates among sites within islands. Recruits were patchily distributed within sites but no aggregative effect was detected, i.e. the preferentially colonised tiles were not spatially grouped. Recruits settled mainly on the sides of the tiles, especially at Rodrigues, which could be attributed to the high concentration of suspended matter. The variability of recruitment patterns at various spatial scales emphasises the importance of micro- to macro-local variations of the environment in the dynamics and maintenance of coral populations. High temporal variability was also detected, between seasons and years, which may be related to the early 2016 bleaching event at Rodrigues. The low recruitment rates and the absence of protection effect raise questions about the potential for recovery from disturbances of coral reefs in the Mascarene Islands.

Protists Within Corals: The Hidden Diversity.

Previous observations suggested that microbial communities contribute to coral health and the ecological resilience of coral reefs. However, most studies of coral microbiology focused on prokaryotes and the endosymbiotic algae Symbiodinium. In contrast, knowledge concerning diversity of other protists is still lacking, possibly due to methodological constraints. As most eukaryotic DNA in coral samples was derived from hosts, protist diversity was missed in metagenome analyses. To tackle this issue, we designed blocking primers for Scleractinia sequences amplified with two primer sets that targeted variable loops of the 18S rRNA gene (18SV1V2 and 18SV4). These blocking primers were used on environmental colonies of Pocillopora damicornis sensu lato from two regions with contrasting thermal regimes (Djibouti and New Caledonia). In addition to Symbiodinium clades A/C/D, Licnophora and unidentified coccidia genera were found in many samples. In particular, coccidian sequences formed a robust monophyletic clade with other protists identified in Agaricia, Favia, Montastraea, Mycetophyllia, Porites, and Siderastrea coral colonies. Moreover, Licnophora and coccidians had different distributions between the two geographic regions. A similar pattern was observed between Symbiodinium clades C and A/D. Although we were unable to identify factors responsible for this pattern, nor were we able to confirm that these taxa were closely associated with corals, we believe that these primer sets and the associated blocking primers offer new possibilities to describe the hidden diversity of protists within different coral species.

Recovery of coral assemblages despite acute and recurrent disturbances on a South Central Pacific reef.

Coral reefs are increasingly threatened by various types of disturbances, and their recovery is challenged by accelerating, human-induced environmental changes. Recurrent disturbances reduce the pool of mature adult colonies of reef-building corals and undermine post-disturbance recovery from newly settled recruits. Using a long-term interannual data set, we show that coral assemblages on the reef slope of Moorea, French Polynesia, have maintained a high capacity to recover despite a unique frequency of large-scale disturbances which, since the 1990s, have caused catastrophic declines in coral cover and abundance. In 2014, only four years after one of the most extreme cases of coral decline documented, abundance of juvenile and adult colonies had regained or exceeded pre-disturbance levels, and no phase-shift to macroalgal dominance was recorded. This rapid recovery has been achieved despite constantly low coral recruitment rates, suggesting a high post-disturbance survivorship of recruits. However, taxonomic differences in coral susceptibility to disturbances and contrasting recovery trajectories have resulted in changes in the relative composition of species. In the present context of global coral reef decline, our study establishes a new benchmark for the capacity of certain benthic reef communities to sustain and recover their coral cover from repeated, intense disturbances.

Thermal regime and host clade, rather than geography, drive Symbiodinium and bacterial assemblages in the scleractinian coral Pocillopora damicornis sensu lato.

BACKGROUND: Although the term holobiont has been popularized in corals with the advent of the hologenome theory of evolution, the underlying concepts are still a matter of debate. Indeed, the relative contribution of host and environment and especially thermal regime in shaping the microbial communities should be examined carefully to evaluate the potential role of symbionts for holobiont adaptation in the context of global changes. We used the sessile, long-lived, symbiotic and environmentally sensitive reef-building coral Pocillopora damicornis to address these issues. RESULTS: We sampled Pocillopora damicornis colonies corresponding to two different mitochondrial lineages in different geographic areas displaying different thermal regimes: Djibouti, French Polynesia, New Caledonia, and Taiwan. The community composition of bacteria and the algal endosymbiont Symbiodinium were characterized using high-throughput sequencing of 16S rRNA gene and internal transcribed spacer, ITS2, respectively. Bacterial microbiota was very diverse with high prevalence of Endozoicomonas, Arcobacter, and Acinetobacter in all samples. While Symbiodinium sub-clade C1 was dominant in Taiwan and New Caledonia, D1 was dominant in Djibouti and French Polynesia. Moreover, we also identified a high background diversity (i.e., with proportions < 1%) of A1, C3, C15, and G Symbiodinum sub-clades. Using redundancy analyses, we found that the effect of geography was very low for both communities and that host genotypes and temperatures differently influenced Symbiodinium and bacterial microbiota. Indeed, while the constraint of host haplotype was higher than temperatures on bacterial composition, we showed for the first time a strong relationship between the composition of Symbiodinium communities and minimal sea surface temperatures. CONCLUSION: Because Symbiodinium assemblages are more constrained by the thermal regime than bacterial communities, we propose that their contribution to adaptive capacities of the holobiont to temperature changes might be higher than the influence of bacterial microbiota. Moreover, the link between Symbiodinium community composition and minimal temperatures suggests low relative fitness of clade D at lower temperatures. This observation is particularly relevant in the context of climate change, since corals will face increasing temperatures as well as much frequent abnormal cold episodes in some areas of the world.

Ephemeral and Localized Outbreaks of the Coral Predator Acanthaster cf. solaris in the Southwestern Lagoon of New Caledonia.

Mehdi Adjeroud, Mohsen Kayal, Christophe Peignon, Matthieu Juncker, Suzanne C. Mills, Ricardo Beldade, and Pascal Dumas (2018) Outbreaks of the coral predator Acanthaster spp., the crown-of-thorns seastar (COTS), cause major coral declines across the Indo-Pacific. However, the processes surrounding the initiation and propagation of COTS outbreaks are still unclear. We observed COTS outbreak abundances on several mid-shelf and inner-barrier reefs in the southern section of the New Caledonian lagoon, a multi-location initiation event that we expected to precede a broader region-wide disturbance. However, reef monitoring over 3 years revealed the highly localized and ephemeral character of these outbreaks. Outbreaks that were observed at four reef locations at the beginning of the survey simply faded away, without any specific management actions such as culling efforts. We also found no distinct reef biotope on which COTS outbreaks originated, although mid-shelf and inner-shelf barrier reefs seem to be favoured. New Caledonia has been exempted from to widespread regional COTS outbreaks, which is surprising given its proximity to the Australian Great Barrier Reef - a reef complex particularly vulnerable to COTS - and Vanuatu - where large-scale outbreaks were recorded during the same period. The availability of coral prey is probably not a limiting factor for the propagation of COTS outbreaks on New Caledonian reefs, given the high abundance and diversity of coral assemblages. Our findings reveal that localized and ephemeral COTS outbreaks can be naturally contained and do not necessarily result in widespread disturbances.

Bias associated with the detectability of the coral-eating pest crown-of-thorns seastar and implications for reef management.

Outbreaks of the predator crown-of-thorns seastar (COTS) Acanthaster planci cause widespread coral mortality across the Indo-Pacific. Like many marine invertebrates, COTS is a nocturnal species whose cryptic behaviour during the day can affect its detectability, particularly in structurally complex reef habitats that provide many refuges for benthic creatures. We performed extensive day and night surveys of COTS populations in coral reef habitats showing differing levels of structural complexity and COTS abundance. We tested whether estimations of COTS density varied between day and night observations, and if the differences were related to changes in COTS abundance, reef structural complexity and the spatial scale of observation. Estimations of COTS density were on average 27% higher at night than during the day. Differences in COTS detection varied with changing seastar abundance but not reef structural complexity or scale of observation. Underestimation of COTS abundance in daytime was significant for a broad seastar density range, thus potentially affecting most outbreak events. Our study suggests that portions of COTS populations can be undetected during conventional surveys and control campaigns, which are exclusively conducted by day, and significantly affect the trajectory of coral reefs. Accounting for bias in COTS detection can strengthen coral reef management broadly.

Multi-species consumer jams and the fall of guarded corals to crown-of-thorns seastar outbreaks.

Outbreaks of predatory crown-of-thorns seastars (COTS) can devastate coral reef ecosystems, yet some corals possess mutualistic guardian crabs that defend against COTS attacks. However, guarded corals do not always survive COTS outbreaks, with the ecological mechanisms sealing the fate of these corals during COTS infestations remaining unknown. In August 2008 in Moorea (17.539° S, 149.830° W), French Polynesia, an unusually dense multi-species aggregation of predators was observed feeding upon guarded corals following widespread coral decline due to COTS predation. Concurrent assaults from these amplified, mixed-species predator guilds likely overwhelm mutualistic crab defense, ultimately leading to the fall of guarded corals. Our observations indicate that guarded corals can sustain devastating COTS attacks for an extended duration, but eventually concede to intensifying assaults from diverse predators that aggregate in high numbers as alternative prey decays. The fall of guarded corals is therefore suggested to be ultimately driven by an indirect trophic cascade that leads to amplified attacks from diverse starving predators following prey decline, rather than COTS assaults alone.