Overgrowth and killing of corals by the brown alga Lobophora hederacea (Dictyotales,Phaeophyceae) on healthy reefs in New Caledonia: A new case of the epizoism syndrome

Coral reef degradation is often associated with regime shifts from coral‐ to macroalgal‐dominated reefs. These shifts demonstrate that under certain conditions (e.g. coral mortality, decrease in herbivory, increased nutrients supply) some macroalgae may overgrow corals. The outcome of the competition is dependent on algal aggressiveness and the coral susceptibility. In undisturbed reefs, herbivore grazing is regulating macroalgal cover, thus preventing the latter from overgrowing corals. However, some macroalgae have evolved strategies not only to outcompete corals but also to escape herbivory to some extent, allowing overgrowth of some coral species in undisturbed reefs. Epizoism represents one of those successful strategies, and has been previously documented with red algae, cyanobacteria and Lobophora variegata (Dictyotales, Phaeophyceae). Here we report a new case of epizoism leading to coral mortality, involving a recently described species of Lobophora, L. hederacea, overgrowing the coral Seriatopora caliendrum (Pocilloporidae) in undisturbed reefs in New Caledonia.     

The recovery of coral genetic diversity in the Sunda Strait following the 1883 eruption of Krakatau

Surveys of microsatellite variation show that genetic diversity has largely recovered in two reef-building corals, Pocillopora damicornis and Seriatopora hystrix (Scleractinia: Pocilloporidae), on reefs which were decimated by the eruption of the volcano Krakatau in 1883. Assignment methods and gene flow estimates indicate that the recolonization of Krakatau occurred mainly from the closest upstream reef system, Pulau Seribu, but that larval input from other regions has also occurred. This pattern is clearer in S. hystrix, which is traditionally the more dispersal-limited species. Despite these observed patterns of larval dispersal, self-recruitment appears to now be the most important factor in supplying larvae to coral populations in Krakatau. This suggests that the colonization of devastated reefs can occur quickly through larval dispersal; however, their survival requires local sources of larvae for self-recruitment. This research supports the observation that the recovery of genetic diversity in coral reef animals can occur on the order of decades and centuries rather than millennia. Conservation measures aimed at sustaining coral reef populations in Krakatau and elsewhere should include both the protection of upstream source populations for larval replenishment should disaster occur as well as the protection of large adult colonies to serve as local larval sources.     

Unexpected cryptic species diversity in the widespread coral Seriatopora hystrix masks spatial‐genetic patterns of connectivity

Mounting evidence of cryptic species in a wide range of taxa highlights the need for careful analyses of population genetic data sets to unravel within‐species diversity from potential interspecies relationships. Here, we use microsatellite loci and hierarchical clustering analysis to investigate cryptic diversity in sympatric and allopatric (separated by 450 km) populations of the widespread coral Seriatopora hystrix on the Great Barrier Reef. Structure analyses delimited unique genetic clusters that were confirmed by phylogenetic and extensive population‐level analyses. Each of four sympatric yet distinct genetic clusters detected within S. hystrix demonstrated greater genetic cohesion across regional scales than between genetic clusters within regions (<10 km). Moreover, the magnitude of genetic differentiation between different clusters (>0.620 G”_ST) was similar to the difference between S. hystrix clusters and the congener S. caliendrum (mean G”_ST 0.720). Multiple lines of evidence, including differences in habitat specificity, mitochondrial identity, Symbiodinium associations and morphology, corroborate the nuclear genetic evidence that these distinct clusters constitute different species. Hierarchical clustering analysis combined with more traditional population genetic methods provides a powerful approach for delimiting species and should be regularly applied to ensure that ecological and evolutionary patterns interpreted for single species are not confounded by the presence of cryptic species.     

Variation in the structure of epifaunal invertebrate assemblages among coral hosts

The high biodiversity of coral reefs is attributable to the many invertebrate groups which live in symbiotic relationships with other reef organisms, particularly those which associate with the living coral habitat. However, few studies have examined the diversity and community structure of coral-dwelling invertebrates and how they vary among coral species. This study quantified the species richness and composition of animals associated with four common species of branching corals (Acropora nasuta, A. millepora, Pocillopora damicornis, and Seriatopora hystrix) at Lizard Island in the northern Great Barrier Reef. One hundred and seventy-eight nominal species from 12 different phyla were extracted across 50 replicate colonies of each coral host. A single coral colony, approximately 20 cm in diameter, harbored as many as 73 individuals and 24 species. There were substantial differences in invertebrate species composition among coral hosts of different families as well as genera. Twenty-seven species (15% of all taxa collected) were found on only one of the four different coral species, which may potentially indicate some level of specialization among coral hosts. The distinct assemblages on different coral species, and the presence of potential specialists, suggests invertebrate communities will be sensitive to the differential loss of branching coral species resulting from coral reef degradation.     

Revisiting the connectivity puzzle of the common coral Pocillopora damicornis

Understanding levels of connectivity among scleractinian coral populations over a range of temporal and spatial scales is vital for managing tropical coral reef ecosystems. Here, we use multilocus microsatellite genotypes to assess the spatial genetic structure of two molecular operational taxonomic units (MOTUs, types α and β) of the widespread coral Pocillopora damicornis on the Great Barrier Reef (GBR) and infer the extent of connectivity on spatial scales spanning from local habitat types to latitudinal sectors of the GBR. We found high genetic similarities over large spatial scales spanning > 1000 km from the northern to the southern GBR, but also strong genetic differentiation at local scales in both MOTUs. The presence of a considerable number of first‐generation migrants within the populations sampled (12% and 27% for types α and β, respectively) suggests that genetic differentiation over small spatial scales is probably a consequence of stochastic recruitment from different genetic pools into recently opened up spaces on the reef, for example, following major disturbance events. We explain high genetic similarity among populations over hundreds of kilometres by long competency periods of brooded zooxanthellate larvae and multiple larval release events each year, combined with strong longshore currents typical along the GBR. The lack of genetic evidence for predominantly clonal reproduction in adult populations of P. damicornis, which broods predominantly asexually produced larvae, further undermines the paradigm that brooded larvae settle close to parent colonies shortly after the release.     

Genetic diversity and connectivity in a brooding reef coral at the limit of its distribution

Remote populations are predicted to be vulnerable owing to their isolation from potential source reefs, and usually low population size and associated increased extinction risk. We investigated genetic diversity, population subdivision and connectivity in the brooding reef coral Seriatopora hystrix at the limits of its Eastern Australian (EA) distribution and three sites in the southern Great Barrier Reef (GBR). Over the approximately 1270 km survey range, high levels of population subdivision were detected (global F_ST = 0.224), with the greatest range in pairwise F_ST values observed among the three southernmost locations: Lord Howe Island, Elizabeth Reef and Middleton Reef. Flinders Reef, located between the GBR and the more southerly offshore reefs, was highly isolated and showed the signature of a recent bottleneck. High pairwise F_ST values and the presence of multiple genetic clusters indicate that EA subtropical coral populations have been historically isolated from each other and the GBR. One putative first-generation migrant was detected from the GBR into the EA subtropics. Occasional long-distance dispersal is supported by changes in species composition at these high-latitude reefs and the occurrence of new species records over the past three decades. While subtropical populations exhibited significantly lower allelic richness than their GBR counterparts, genetic diversity was still moderately high. Furthermore, subtropical populations were not inbred and had a considerable number of private alleles. The results suggest that these high-latitude S. hystrix populations are supplemented by infrequent long-distance migrants from the GBR and may have adequate population sizes to maintain viability and resist severe losses of genetic diversity.     

Genetic assignment of recruits reveals short‐ and long‐distance larval dispersal in Pocillopora damicornis on the Great Barrier Reef

Understanding connectivity of coral populations among and within reefs over ecologically significant timescales is essential for developing evidence‐based management strategies, including the design of marineprotected areas. Here, we present the first assessment of contemporary connectivity among populations of two Molecular Operational Taxonomic Units (MOTUs) of the brooding coral Pocillopora damicornis. We used individual‐based genetic assignment methods to identify the proportions of philopatric and migrant larval recruits, settling over 12 months at sites around Lizard Island (northern Great Barrier Reef [GBR]) and over 24 months at sites around the Palms Islands (central GBR). Overall, we found spatially and temporally variable rates of self‐recruitment and dispersal, demonstrating the importance of variation in local physical characteristics in driving dispersal processes. Recruitment patterns and inferred dispersal distances differed between the two P. damicornis MOTUs, with type α recruits exhibiting predominantly philopatric recruitment, while the majority of type β recruits were either migrants from identified putative source populations or assumed migrants based on genetic exclusion from all known populations. While P. damicornis invests much energy into brooding clonal larvae, we found that only 15% and 7% of type α and type β recruits, respectively, were clones of sampled adult colonies or other recruits, challenging the hypothesis that reproduction is predominantly asexual in this species on the GBR. We explain high rates of self‐recruitment and low rates of clonality in these MOTUs by suggesting that locally retained larvae originate predominantly from spawned gametes, while brooded larvae are mainly vagabonds.     

Epidemiology of skeletal eroding band on the Great Barrier Reef and the role of injury in the initiation of this widespread coral disease

Skeletal eroding band (SEB), which manifests as dense aggregations of the ciliate Halofolliculina corallasia, was the first coral disease described from the Indo-Pacific. Little is known about its etiology or impact. This study describes the distribution, prevalence and host range of SEB on a 500 km extent of the Great Barrier Reef (GBR), together with in situ rates of progression and infection following experimental injury. SEB occurred on 90–100% of reefs surveyed (n=18) in each of 3 years, demonstrating that SEB is widely distributed and persistent. SEB had the highest prevalence of any disease, affecting approximately 2% of 283,486 scleractinians and hydrocorals surveyed. Its host range was large, affecting 12 families and at least 82 scleractinian species, as well as the hydrocoral, Millepora. Corals in the families Pocilloporidae and Acroporidae were most susceptible, the former being up to five times more susceptible than other families. Progressive tissue loss was recorded on 95% of Acropora muricata colonies monitored (n = 18), with rates of SEB progression averaging ∼2 mm/day. Injury experiments demonstrated that H. corallasia, the putative pathogen of SEB, readily colonised recently exposed coral skeleton in the absence of a vector, but did not colonise intact coral tissue. Invading ciliates failed to form band-like aggregations associated with progressive tissue loss on any of three coral species tested experimentally, suggesting that, while H. corallasia readily colonises recently exposed coral skeleton, it may not be sufficient in itself to cause tissue mortality. Interactions with additional agents or factors, increasing ciliate virulence or lowering disease resistance of coral hosts may be required before halofolliculinid infections become associated with tissue loss.     

Temporal clustering of tropical cyclones on the Great Barrier Reef and its ecological importance

Tropical cyclones have been a major cause of reef coral decline during recent decades, including on the Great Barrier Reef (GBR). While cyclones are a natural element of the disturbance regime of coral reefs, the role of temporal clustering has previously been overlooked. Here, we examine the consequences of different types of cyclone temporal distributions (clustered, stochastic or regular) on reef ecosystems. We subdivided the GBR into 14 adjoining regions, each spanning roughly 300 km, and quantified both the rate and clustering of cyclones using dispersion statistics. To interpret the consequences of such cyclone variability for coral reef health, we used a model of observed coral population dynamics. Results showed that clustering occurs on the margins of the cyclone belt, being strongest in the southern reefs and the far northern GBR, which also has the lowest cyclone rate. In the central GBR, where rates were greatest, cyclones had a relatively regular temporal pattern. Modelled dynamics of the dominant coral genus, Acropora, suggest that the long-term average cover might be more than 13 % greater (in absolute cover units) under a clustered cyclone regime compared to stochastic or regular regimes. Thus, not only does cyclone clustering vary significantly along the GBR but such clustering is predicted to have a marked, and management-relevant, impact on the status of coral populations. Additionally, we use our regional clustering and rate results to sample from a library of over 7000 synthetic cyclone tracks for the GBR. This allowed us to provide robust reef-scale maps of annual cyclone frequency and cyclone impacts on Acropora. We conclude that assessments of coral reef vulnerability need to account for both spatial and temporal cyclone distributions.

     

Coral reef restoration in the Eastern Tropical Pacific: feasibility of the coral nursery approach

Due to the worldwide degradation of coral reefs, the active restoration of these ecosystems has received considerable attention in recent decades. This study investigated (1) the feasibility of using coral nurseries for restoration projects, (2) the minimum size required for a Pocillopora damicornis (Pocilloporidae) coral fragment to survive and grow in a nursery, and (3) the optimal transplant size of a fragment when transplanted to a degraded reef at Gorgona Island (Colombian Pacific). For this investigation, 230 fragments were transplanted directly to El Remanso reef, and another 150 fragments were maintained in in situ nurseries. Every 2 months, the length, weight, and survival of the fragments were recorded. After growing for 134 days in the nurseries, the 52 surviving fragments were transplanted to El Remanso reef, and after 5 months, the same variables were measured. Among the nursery‐reared fragments, the largest (4 to <8 cm) had the highest survival and growth rates, whereas among the directly transplanted fragments, the smallest fragments (<2 cm) had the highest survival and growth rates. However, the nursery‐reared fragments acquired greater structural complexity (arborescent morphology), and they were all alive 156 days after transplantation and presented a maximum linear growth rate of over 2 cm, which was higher than that of the directly transplanted fragments. Apparently, the arborescent morphology acquired during the nursery period provides advantages to the colonies that favor greater success when transplanted. Therefore, nursery‐reared fragments of P. damicornis between 2 and 4 cm are the most appropriate for use in restoration projects.     

Morphological differences among three species of newly settled pocilloporid coral recruits

 Investigation of the life history of corals is hampered by an inability to identify early recruits. In this study, the pattern of formation and morphology of the juvenile skeletons of three laboratory-reared pocilloporids, Seriatopora hystrix, Stylophora pistillata and Pocillopora damicornis, were compared to determine whether they could be reliably distinguished. The pattern of skeleton formation, including the origin and structure of the septa, columella and corallite wall was similar in all species. Following the completion of the primary corallite wall after 4–5 days, these species could be identified by differences in the diameter of the primary corallite. The mean diameter (±SE) of each species differed markedly: S. hystrix 400 ± 2.7 μm, range 325–450 μm; S. pistillata 505 ± 3.5 μm, range 400–550 μm; P. damicornis 697 ± 7.5 μm, range 492–885 μm. Values for the primary corallite diameter overlapped in only 3% of samples, demonstrating the potential utility of this feature as a tool for classifying recruits obtained from the field. Accepted: 4 January 2000     

Coral growth with thermal stress and ocean acidification: lessons from the eastern tropical Pacific

The rapid growth of scleractinian corals is responsible for the persistence of coral reefs through time. Coral growth rates have declined over the past 30 years in the western Pacific, Indian, and North Atlantic Oceans. The spatial scale of this decline has led researchers to suggest that a global phenomenon like ocean acidification may be responsible. A multi-species inventory of coral growth from Pacific Panamá confirms that declines have occurred in some, but not all species. Linear extension declined significantly in the most important reef builder of the eastern tropical Pacific, Pocillopora damicornis, by nearly one-third from 1974 to 2006. The rate of decline in skeletal extension for P. damicornis from Pacific Panamá (0.9% year⁻¹) was nearly identical to massive Porites in the Indo-Pacific over the past 20–30 years (0.89–1.23% year⁻¹). The branching pocilloporid corals have shown an increased tolerance to recurrent thermal stress events in Panamá, but appear to be susceptible to acidification. In contrast, the massive pavonid corals have shown less tolerance to thermal stress, but may be less sensitive to acidification. These differing sensitivities will be a fundamental determinant of eastern tropical Pacific coral reef community structure with accelerating climate change that has implications for the future of reef communities worldwide.     

Low genetic structuring among <Emphasis Type="Italic">Pericharax heteroraphis</Emphasis> (Porifera: Calcarea) populations from the Great Barrier Reef (Australia), revealed by analysis of nrDNA and nuclear intron sequences

A new nuclear marker system for sponges, the second intron of the nuclear ATP synthetase beta subunit gene (ATPSbeta-iII), was analysed together with nuclear ribosomal DNA (nrDNA) internal transcribed spacer (ITS) sequences aiming to uncover phylogeographic patterns of the coral reef sponge Pericharax heteroraphis in the south-west Pacific, focussing on the Great Barrier Reef (GBR). Variation among ITS sequences was low (<1.1% p-distance), in contrast to ATPSbeta-iII (<8.3% p-distance). Single-Stranded Conformation Polymorphism (SSCP) analysis proved to be an effective tool for phasing ATPSbeta-iII alleles of 292 bp length. Although sample sizes were limited for most populations and these results await corroboration by an extended sampling regime, a past population subdivision with subsequent range expansion was indicated by a ‘dumb-bell’ shaped statistical parsimony network of GBR ATPSbeta-iII alleles. Although no clear phylogeographic break was discovered on the GBR, the northern GBR was genetically differentiated from the central/southern GBR and Queensland Plateau, based on significant pairwise F _st values (0.137–0.275 and p ≤ 0.05) of pooled regional populations. The ATPSbeta-iII used in this study outperformed the frequently employed nrDNA ITS and might also turn out to be useful for phylogeographic studies of other coral reef taxa. Electronic supplementary material The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

Three lines of evidence to link outbreaks of the crown-of-thorns seastar Acanthaster planci to the release of larval food limitation

Population outbreaks of the coral-eating crown-of-thorns seastar, Acanthaster planci, continue to kill more coral on Indo-Pacific coral reefs than other disturbances, but the causes of these outbreaks have not been resolved. In this study, we combine (1) results from laboratory experiments where larvae were reared on natural phytoplankton, (2) large-scale and long-term field data of river floods, chlorophyll concentrations and A. planci outbreaks on the Great Barrier Reef (GBR), and (3) results from A. planci—coral population model simulations that investigated the relationship between the frequency of outbreaks and larval food availability. The experiments show that the odds of A. planci larvae completing development increases ~8-fold with every doubling of chlorophyll concentrations up to 3 μg l⁻¹. Field data and the population model show that river floods and regional differences in phytoplankton availability are strongly related to spatial and temporal patterns in A. planci outbreaks on the GBR. The model also shows that, given plausible historic increases in river nutrient loads over the last 200 years, the frequency of A. planci outbreaks on the GBR has likely increased from one in 50–80 years to one every 15 years, and that current coral cover of reefs in the central GBR may be 30–40% of its potential value. This study adds new and strong empirical support to the hypothesis that primary A. planci outbreaks are predominantly controlled by phytoplankton availability.     

Reef coral survival and mortality at low temperatures in the Arabian Gulf: new species-specific lower temperature limits

A series of cold fronts passing over the western Arabian Gulf from December 1988 to March 1989 produced the longest period of sustained low water temperatures ever recorded in a coral reef area. Sea water temperatures recorded on two reefs during this period provide new estimates of lower thermal limits for reef coral survival. Severe mortality of the corals Acropora pharaonis and Platygyra daedalea occurred at the northern site where minimum temperatures fell below 11.5°C on four consecutive days and mean daily temperatures were 13°C or less for more than 30 days. However, Porites compressa, the principal reef-former in this area, and various faviid corals initially showed only sub-lethal effects and appeared normal after six months. Corals were not damaged at the southern site, where minimum water temperature fell below 12.5°C for two consecutive days, but mean temperatures were 14°C or less for only 5 non-consecutive days.     

Seasonal and local spatial patterns in the upper thermal limits of corals on the inshore Central Great Barrier Reef

 Experimental studies of the upper thermal limits of corals from Orpheus Island, an inshore reef in the central Great Barrier Reef, show that Acropora formosa has a 5-day 50%-bleaching threshold of between 31 and 32 °C in summer, only 2 to 3 °C higher than local mean summer temperatures (29 °C). Summer bleaching thresholds for Pocillopora damicornis and A. elseyi were 1 °C higher (between 32 and 33 °C). The winter bleaching threshold of Pocillopora damicornis was 1 °C lower than its summer threshold, indicating that seasonal acclimatisation may take place. This seasonal difference raises the possibility that at least some corals may be capable of short-term thermal acclimatisation. Neither P. damicornis nor A. elseyi showed habitat-specific (reef flat versus reef slope) differences in bleaching thresholds. Further, colonies of P. damicornis collected from sites 3 km apart also showed no difference in bleaching threshold despite populations of this species responding differently at these two sites during a natural bleaching event. The bleaching thresholds determined in this study are best considered as the maximum tolerable temperatures for local populations of these species because they were determined in the absence of additional stressors (e.g. high light) which often co-occur during natural bleaching events. We consider the 5-day 50% bleaching thresholds determined in these experiments to be fair indicators of upper thermal limits, because >50% of a sample population died when allowed to recover in situ. We found a delay of up to a month in the bleaching response of corals following thermal stress, a result that has implications for identifying the timing of stressful conditions in natural bleaching events. Accepted: 26 May 1999     

Influence of water flow on skeletal isotopic composition in the coral Pocillopora damicornis

Fragments of branching Pocillopora damicornis coral colonies were grown in experimental flumes under two water flow regimes. Colony size and buoyant weight increased most rapidly in the fast-flow regime. Branch tips from the upper and outer parts of the colonies showed the lowest and most consistent skeletal oxygen isotope ratios. Flow regime had little influence on the lowest oxygen isotope ratios, which were at least 3.5‰ lighter than the calculated oxygen isotopic equilibrium. These “kinetic” isotope effects are comparable to those observed in Porites corals. Relatively more branch tips showed extreme ¹⁸O depletions under low-flow conditions, and among small coral colonies. Isotopic variability was greater among branch tips from the lower and inner parts of the colonies and at high flow. Skeletal oxygen and carbon isotope ratios generally showed positive correlations. Despite the particularly large offsets from isotopic equilibrium, the isotopically lightest branches showed the greatest isotopic consistency and therefore would make the best isotopic thermometers. Isotopic variability within the colony may provide an indication of flow regime.     

Fine-scale analysis of genetic structure in the brooding coral Seriatopora hystrix from the Red Sea

The dispersal of gametes and larvae plays a key role in the population dynamics of sessile marine invertebrates. Species with internal fertilisation are often associated with very localised larval dispersal, which may cause small-scale patterns of neutral genetic variation. This study on the brooding coral Seriatopora hystrix from the Red Sea focused on the smallest possible scale: Two S. hystrix stands (~100 colonies each) near Dahab were completely sampled, mapped and analysed at five microsatellite markers. The sexual mode of reproduction, the likely occurrence of selfing and the level of immigration were in agreement with previous studies on this species. Contrary to previous findings, both stands were in Hardy–Weinberg proportions. Also, no evidence for spatially restricted larval dispersal within the sampled areas was found. Differences between this and previous studies on S. hystrix could reflect variation in life history or varying environmental conditions, which opens intriguing questions for future research.     

Restoration of coral populations in light of genetic diversity estimates

Due to the importance of preserving the genetic integrity of populations, strategies to restore damaged coral reefs should attempt to retain the allelic diversity of the disturbed population; however, genetic diversity estimates are not available for most coral populations. To provide a generalized estimate of genetic diversity (in terms of allelic richness) of scleractinian coral populations, the literature was surveyed for studies describing the genetic structure of coral populations using microsatellites. The mean number of alleles per locus across 72 surveyed scleractinian coral populations was 8.27 (±0.75 SE). In addition, population genetic datasets from four species (Acropora palmata, Montastraea cavernosa, Montastraea faveolata and Pocillopora damicornis) were analyzed to assess the minimum number of donor colonies required to retain specific proportions of the genetic diversity of the population. Rarefaction analysis of the population genetic datasets indicated that using 10 donor colonies randomly sampled from the original population would retain >50% of the allelic diversity, while 35 colonies would retain >90% of the original diversity. In general, scleractinian coral populations are genetically diverse and restoration methods utilizing few clonal genotypes to re-populate a reef will diminish the genetic integrity of the population. Coral restoration strategies using 10–35 randomly selected local donor colonies will retain at least 50–90% of the genetic diversity of the original population. Electronic supplementary material  The online version of this article (doi:) contains supplementary material, which is available to authorized users.