Mohsen Kayal

Predator crown-of-thorns starfish (Acanthaster planci) outbreak, mass mortality of corals, and cascading effects on reef fish and benthic communities

Outbreaks of the coral-killing seastar Acanthaster planci are intense disturbances that can decimate coral reefs. These events consist of the emergence of large swarms of the predatory seastar that feed on reef-building corals, often leading to widespread devastation of coral populations. While cyclic occurrences of such outbreaks are reported from many tropical reefs throughout the Indo-Pacific, their causes are hotly debated, and the spatio-temporal dynamics of the outbreaks and impacts to reef communities remain unclear. Based on observations of a recent event around the island of Moorea, French Polynesia, we show that Acanthaster outbreaks are methodic, slow-paced, and diffusive biological disturbances. Acanthaster outbreaks on insular reef systems like Mooreas appear to originate from restricted areas confined to the ocean-exposed base of reefs. Elevated Acanthaster densities then progressively spread to adjacent and shallower locations by migrations of seastars in aggregative waves that eventually affect the entire reef system. The directional migration across reefs appears to be a search for prey as reef portions affected by dense seastar aggregations are rapidly depleted of living corals and subsequently left behind. Coral decline on impacted reefs occurs by the sequential consumption of species in the order of Acanthaster feeding preferences. Acanthaster outbreaks thus result in predictable alteration of the coral community structure. The outbreak we report here is among the most intense and devastating ever reported. Using a hierarchical, multi-scale approach, we also show how sessile benthic communities and resident coral-feeding fish assemblages were subsequently affected by the decline of corals. By elucidating the processes involved in an Acanthaster outbreak, our study contributes to comprehending this widespread disturbance and should thus benefit targeted management actions for coral reef ecosystems.

Evolution of Linear Mitochondrial Genomes in Medusozoan Cnidarians

In nearly all animals, mitochondrial DNA (mtDNA) consists of a single circular molecule that encodes several subunits of the protein complexes involved in oxidative phosphorylation as well as part of the machinery for their expression. By contrast, mtDNA in species belonging to Medusozoa (one of the two major lineages in the phylum Cnidaria) comprises one to several linear molecules. Many questions remain on the ubiquity of linear mtDNA in medusozoans and the mechanisms responsible for its evolution, replication, and transcription. To address some of these questions, we determined the sequences of nearly complete linear mtDNA from 24 species representing all four medusozoan classes: Cubozoa, Hydrozoa, Scyphozoa, and Staurozoa. All newly determined medusozoan mitochondrial genomes harbor the 17 genes typical for cnidarians and map as linear molecules with a high degree of gene order conservation relative to the anthozoans. In addition, two open reading frames (ORFs), polB and ORF314, are identified in cubozoan, schyphozoan, staurozoan, and trachyline hydrozoan mtDNA. polB belongs to the B-type DNA polymerase gene family, while the product of ORF314 may act as a terminal protein that binds telomeres. We posit that these two ORFs are remnants of a linear plasmid that invaded the mitochondrial genomes of the last common ancestor of Medusozoa and are responsible for its linearity. Hydroidolinan hydrozoans have lost the two ORFs and instead have duplicated cox1 at each end of their mitochondrial chromosome(s). Fragmentation of mtDNA occurred independently in Cubozoa and Hydridae (Hydrozoa, Hydroidolina). Our broad sampling allows us to reconstruct the evolutionary history of linear mtDNA in medusozoans.

Associational refuges among corals mediate impacts of a crown-of-thorns starfish Acanthaster planci outbreak

Interactions among coral populations can moderate the impact of coral predator outbreaks, enhancing community resilience and recovery. This study used predator-exclusion cages and neighbour removals in a field experiment to test how indirect interactions between populations of three coral taxa, Acropora, Pocillopora, and Porites, influenced their survival during an outbreak of the crown-of-thorns starfish, Acanthaster planci, in Moorea, French Polynesia. High densities of corals enhanced survival by generating associational refuges: physical structures that impeded Acanthaster and protected corals, and by simple density-dependent prey dilution that reduced predation rates. Acanthaster showed feeding preferences, resulting in varying intensities of predation on corals, which (1) influenced the type and strength of the associational refuge among corals and (2) resulted in significant loss of the competitive dominants to the benefit of the competitive inferiors. The result was a set of indirect positive interactions (IPIs) that prevented Acanthaster from eradicating Acropora and may have enhanced Porites, a relatively weak competitor among corals. IPIs probably play a key role in many ecosystems, especially in coral reefs in which corals act as engineer species, to reduce impacts of perturbations and enhance community resilience. This study illustrates the importance of IPIs in community regulation with a new conceptual model.

Understanding Uncertainties in Non-Linear Population Trajectories: A Bayesian Semi-Parametric Hierarchical Approach to Large-Scale Surveys of Coral Cover

Recently, attempts to improve decision making in species management have focussed on uncertainties associated with modelling temporal fluctuations in populations. Reducing model uncertainty is challenging; while larger samples improve estimation of species trajectories and reduce statistical errors, they typically amplify variability in observed trajectories. In particular, traditional modelling approaches aimed at estimating population trajectories usually do not account well for nonlinearities and uncertainties associated with multi-scale observations characteristic of large spatio-temporal surveys. We present a Bayesian semi-parametric hierarchical model for simultaneously quantifying uncertainties associated with model structure and parameters, and scale-specific variability over time. We estimate uncertainty across a four-tiered spatial hierarchy of coral cover from the Great Barrier Reef. Coral variability is well described; however, our results show that, in the absence of additional model specifications, conclusions regarding coral trajectories become highly uncertain when considering multiple reefs, suggesting that management should focus more at the scale of individual reefs. The approach presented facilitates the description and estimation of population trajectories and associated uncertainties when variability cannot be attributed to specific causes and origins. We argue that our model can unlock value contained in large-scale datasets, provide guidance for understanding sources of uncertainty, and support better informed decision making.

Photosynthetic response of Persian Gulf acroporid corals to summer versus winter temperature deviations

With on-going climate change, coral susceptibility to thermal stress constitutes a central concern in reefconservation. In the Persian Gulf, coral reefs are confronted with a high seasonal variability in water temperature, and both hot and cold extremes have been associated with episodes of coral bleaching and mortality. Using physiological performance as a measure of coral health, we investigated the thermal susceptibility of the common acroporid, Acropora downingi, near Hengam Island where the temperature oscillates seasonally in the range 20.2–34.2 °C. In a series of two short-term experiments comparing coral response in summer versus winter conditions, we exposed corals during each season (1) to the corresponding seasonal average and extreme temperature levels in a static thermal environment, and (2) to a progressive temperature deviation from the annual mean toward the corresponding extreme seasonal value and beyond in a dynamic thermal environment. We monitored four indictors of coral physiological performance: net photosynthesis (Pn), dark respiration (R), autotrophic capability (Pn/R), and survival. Corals exposed to warming during summer showed a decrease in net photosynthesis and ultimately died, while corals exposed to cooling during winter were not affected in their photosynthetic performance and survival. Coral autotrophic capability Pn/R was lower at the warmer thermal level within eachseason, and during summer compared to winter. Corals exposed to the maximum temperature of summer displayed Pn/R < 1, inferring that photosynthetic performance could not support basal metabolic needs under this environment. Our results suggest that the autotrophic performance of the Persian Gulf A. downingi is sensitive to the extreme temperatures endured in summer, and therefore its populations may be impacted by future increases in water temperature.

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.

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.

Coral assemblages in Tonga: spatial patterns, replenishment capacities, and implications for conservation strategies.

Coral reefs in Tonga have been confronted by multiple threats of various origins, including large-scale disturbances and human-induced stressors. These reef communities have been poorly studied, and efficient conservation actions are urgently needed. The aim of this study was to: (1) examine the spatial distribution of coral assemblages in the lagoon of Tongatapu; (2) determine the degree to which spatial heterogeneity of adult corals is influenced by recruitment processes; and (3) examine the implications of these results in terms of conservation actions. We recorded a total of 37 adult and 28 juvenile coral genera, a mean density of 11.6 adult and 5.5 juvenile colonies m−2, and a dominance of Montipora, Acropora, and Porites. For seven of the 10 dominant genera, spatial patterns of adults were linked to the short-term recruitment pattern history. Despite a reduced diversity and abundance of adult corals in some areas, the lagoon of Tongatapu retains the potential for replenishment through recruitment of young corals. Consequently, we suggest that conservation actions should focus on reducing factors causing coral mortality and maintain suitable conditions for the establishment and growth of juvenile corals, thus increasing the probability that they will reach maturity and participate to the maintenance of local populations. Rather than establishing a large marine protected area, which will almost certainly suffer from a lack of control and poor enforcement, alternative conservation measures could be successfully implemented through the establishment of several small village-based marine reserves, as has been undertaken in other South Pacific islands with promising results.

Predicting coral community recovery using multi‐species population dynamics models

Predicting whether, how, and to what degree communities recover from disturbance remain major challenges in ecology. To predict recovery of coral communities we applied field survey data of early recovery dynamics to a multi-species integral projection model that captured key demographic processes driving coral population trajectories, notably density-dependent larval recruitment. After testing model predictions against field observations, we updated the model to generate projections of future coral communities. Our results indicated that communities distributed across an island landscape followed different recovery trajectories but would reassemble to pre-disturbed levels of coral abundance, composition, and size, thus demonstrating persistence in the provision of reef habitat and other ecosystem services. Our study indicates that coral community dynamics are predictable when accounting for the interplay between species life-history, environmental conditions, and density-dependence. We provide a quantitative framework for evaluating the ecological processes underlying community trajectory and characteristics important to ecosystem functioning.

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.