Marine heatwaves reveal coral reef zones susceptible to bleaching in the Red Sea

As the Earth's temperature continues to rise, coral bleaching events become more frequent. Some of the most affected reef ecosystems are located in poorly monitored waters, and thus, the extent of the damage is unknown. We propose the use of marine heatwaves (MHWs) as a new approach for detecting coral reef zones susceptible to bleaching, using the Red Sea as a model system. Red Sea corals are exceptionally heat‐resistant, yet bleaching events have increased in frequency. By applying a strict definition of MHWs on >30 year satellite‐derived sea surface temperature observations (1985–2015), we provide an atlas of MHW hotspots over the Red Sea coral reef zones, which includes all MHWs that caused major coral bleaching. We found that: (a) if tuned to a specific set of conditions, MHWs identify all areas where coral bleaching has previously been reported; (b) those conditions extended farther and occurred more often than bleaching was reported; and (c) an emergent pattern of extreme warming events is evident in the northern Red Sea (since 1998), a region until now thought to be a thermal refuge for corals. We argue that bleaching in the Red Sea may be vastly underrepresented. Additionally, although northern Red Sea corals exhibit remarkably high thermal resistance, the rapidly rising incidence of MHWs of high intensity indicates this region may not remain a thermal refuge much longer. As our regionally tuned MHW algorithm was capable of isolating all extreme warming events that have led to documented coral bleaching in the Red Sea, we propose that this approach could be used to reveal bleaching‐prone regions in other data‐limited tropical regions. It may thus prove a highly valuable tool for policymakers to optimize the sustainable management of coastal economic zones.     

A coral reef refuge in the Red Sea

The stability and persistence of coral reefs in the decades to come is uncertain due to global warming and repeated bleaching events that will lead to reduced resilience of these ecological and socio‐economically important ecosystems. Identifying key refugia is potentially important for future conservation actions. We suggest that the Gulf of Aqaba (GoA) (Red Sea) may serve as a reef refugium due to a unique suite of environmental conditions. Our hypothesis is based on experimental detection of an exceptionally high bleaching threshold of northern Red Sea corals and on the potential dispersal of coral planulae larvae through a selective thermal barrier estimated using an ocean model. We propose that millennia of natural selection in the form of a thermal barrier at the southernmost end of the Red Sea have selected coral genotypes that are less susceptible to thermal stress in the northern Red Sea, delaying bleaching events in the GoA by at least a century.     

Thermal refugia against coral bleaching throughout the northern Red Sea

Tropical reefs have been impacted by thermal anomalies caused by global warming that induced coral bleaching and mortality events globally. However, there have only been very few recordings of bleaching within the Red Sea despite covering a latitudinal range of 15° and consequently it has been considered a region that is less sensitive to thermal anomalies. We therefore examined historical patterns of sea surface temperature (SST) and associated anomalies (1982–2012) and compared warming trends with a unique compilation of corresponding coral bleaching records from throughout the region. These data indicated that the northern Red Sea has not experienced mass bleaching despite intensive Degree Heating Weeks (DHW) of >15°C‐weeks. Severe bleaching was restricted to the central and southern Red Sea where DHWs have been more frequent, but far less intense (DHWs <4°C‐weeks). A similar pattern was observed during the 2015–2016 El Niño event during which time corals in the northern Red Sea did not bleach despite high thermal stress (i.e. DHWs >8°C‐weeks), and bleaching was restricted to the central and southern Red Sea despite the lower thermal stress (DHWs < 8°C‐weeks). Heat stress assays carried out in the northern (Hurghada) and central (Thuwal) Red Sea on four key reef‐building species confirmed different regional thermal susceptibility, and that central Red Sea corals are more sensitive to thermal anomalies as compared to those from the north. Together, our data demonstrate that corals in the northern Red Sea have a much higher heat tolerance than their prevailing temperature regime would suggest. In contrast, corals from the central Red Sea are close to their thermal limits, which closely match the maximum annual water temperatures. The northern Red Sea harbours reef‐building corals that live well below their bleaching thresholds and thus we propose that the region represents a thermal refuge of global importance.     

Genetic population structure of the lionfish Pterois miles (Scorpaenidae, Pteroinae) in the Gulf of Aqaba and northern Red Sea

The aim of this study is to reveal gene flow between populations of the coral reef dwelling lionfish Pterois miles in the Gulf of Aqaba and northern Red Sea. Due to the fjord-like hydrography and topology of the Gulf of Aqaba, isolation of populations might be possible. Analysis of 5' mitochondrial control region sequences from 94 P. miles specimens detected 32 polymorphic sites, yielding 38 haplotypes. Sequence divergence among different haplotypes ranged from 0.6% to 9.9% and genetic diversity was high (h=0.85, pi=1.9%). AMOVA indicates panmixia between the Gulf of Aqaba and northern Red Sea, but analysis of migration pattern shows an almost unidirectional migration originating from the Red Sea.     

The status of coral reef ecology research in the Red Sea

The Red Sea has long been recognized as a region of high biodiversity and endemism. Despite this diversity and early history of scientific work, our understanding of the ecology of coral reefs in the Red Sea has lagged behind that of other large coral reef systems. We carried out a quantitative assessment of ISI-listed research published from the Red Sea in eight specific topics (apex predators, connectivity, coral bleaching, coral reproductive biology, herbivory, marine protected areas, non-coral invertebrates and reef-associated bacteria) and compared the amount of research conducted in the Red Sea to that from Australia’s Great Barrier Reef (GBR) and the Caribbean. On average, for these eight topics, the Red Sea had 1/6th the amount of research compared to the GBR and about 1/8th the amount of the Caribbean. Further, more than 50 % of the published research from the Red Sea originated from the Gulf of Aqaba, a small area (<2 % of the area of the Red Sea) in the far northern Red Sea. We summarize the general state of knowledge in these eight topics and highlight the areas of future research priorities for the Red Sea region. Notably, data that could inform science-based management approaches are badly lacking in most Red Sea countries. The Red Sea, as a geologically “young” sea located in one of the warmest regions of the world, has the potential to provide insight into pressing topics such as speciation processes as well as the capacity of reef systems and organisms to adapt to global climate change. As one of the world’s most biodiverse coral reef regions, the Red Sea may yet have a significant role to play in our understanding of coral reef ecology at a global scale.     

Population genomic response to geographic gradients by widespread and endemic fishes of the Arabian Peninsula

Genetic structure within marine species may be driven by local adaptation to their environment, or alternatively by historical processes, such as geographic isolation. The gulfs and seas bordering the Arabian Peninsula offer an ideal setting to examine connectivity patterns in coral reef fishes with respect to environmental gradients and vicariance. The Red Sea is characterized by a unique marine fauna, historical periods of desiccation and isolation, as well as environmental gradients in salinity, temperature, and primary productivity that vary both by latitude and by season. The adjacent Arabian Sea is characterized by a sharper environmental gradient, ranging from extensive coral cover and warm temperatures in the southwest, to sparse coral cover, cooler temperatures, and seasonal upwelling in the northeast. Reef fish, however, are not confined to these seas, with some Red Sea fishes extending varying distances into the northern Arabian Sea, while their pelagic larvae are presumably capable of much greater dispersal. These species must therefore cope with a diversity of conditions that invoke the possibility of steep clines in natural selection. Here, we test for genetic structure in two widespread reef fish species (a butterflyfish and surgeonfish) and eight range‐restricted butterflyfishes across the Red Sea and Arabian Sea using genome‐wide single nucleotide polymorphisms. We performed multiple matrix regression with randomization analyses on genetic distances for all species, as well as reconstructed scenarios for population subdivision in the species with signatures of isolation. We found that (a) widespread species displayed more genetic subdivision than regional endemics and (b) this genetic structure was not correlated with contemporary environmental parameters but instead may reflect historical events. We propose that the endemic species may be adapted to a diversity of local conditions, but the widespread species are instead subject to ecological filtering where different combinations of genotypes persist under divergent ecological regimes.     

Recruitment of coral reef fishes along a cross-shelf gradient in the Red Sea peaks outside the hottest season

Knowledge on the early life history, ecology, and biology of marine species is crucial for future projections of the resilience of coral reef ecosystems and for adequate management strategies. A fundamental component of population dynamics is the recruitment of new individuals, and in some marine populations, this may be a limiting factor. Recruitment peaks of coral reef fishes commonly occur during the warmer months of the year in many subtropical and temperate locations worldwide. In the Red Sea, very little is known about the influence of temperature on reproductive patterns of coral reef fishes and studies on recruitment are missing. The Red Sea is one of the hottest and most isolated tropical seas in the world. We hypothesized that sea surface temperatures (SSTs) during the Red Sea’s hottest season may exceed the optimum for successful recruitment of some coral reef fishes, which therefore has to occur during other, cooler seasons, unlike recruitment among coral reef ecosystems around the world. We identified taxa among fish recruits by matching mitochondrial DNA sequences (using COI, commonly known as “barcoding”) and assessed potential biological and environmental drivers of recruitment. We studied three reefs located along a cross-shelf gradient for 12 consecutive months in the central Red Sea to capture seasonal changes in biotic and abiotic parameters along this gradient. Our results indicated that recruitment peaks did not occur during the hottest SSTs for most taxa, especially at the hottest inshore and mid-shelf reefs, and identified fish recruitment to be mainly and strongly correlated with the biomass of planktonic invertebrates. Moreover, temporal patterns of fish recruitment differed within and among taxonomic families among the reefs.

     

The determinants of species richness of a relatively young coral-reef ichthyofauna

Aim Unique topographic features left the Red Sea and its north‐eastern extension into the Gulf of Aqaba practically devoid of coral‐reef‐based organisms during the last glacial maximum. The current ichthyofauna in these two ‘regions’ thus represents the product of relatively recent colonization by species found in the Arabian Sea, which adjoins the Red Sea at its southern tip. We used this system to test why some marine species seemingly fail to extend their geographic range, thereby generating spatial heterogeneity in biodiversity. Location The Arabian Sea, Red Sea, and the Gulf of Aqaba. Methods A list of coral‐reef‐associated fish species, belonging to the 10 most speciose families, was compiled for each region using published sources. The data were analysed (major axis regression, randomization tests) for taxonomic and body‐size‐dependent biases in colonization probabilities. A simple probabilistic model was used to examine the potential contribution of local (within‐region) extinctions to determining species composition in the Red Sea. Results Of the 462 reef‐associated species that inhabit the Arabian Sea, 69% have crossed successfully into the Red Sea; of these, 55% have crossed into the Gulf of Aqaba. A species’ probability of being found in either ‘target’ was independent of presumed innate differences, i.e. ecological correlates of taxonomic affiliation and body size. Similarly, local extinctions were found unlikely to have been of consequence over the past several thousand years. Main conclusions Present‐day differences in the species richness of reef‐associated fish species among the Arabian Sea, Red Sea and Gulf of Aqaba appear to be the product of external, non‐selective constraints on colonization. The random nature of the colonization process is suggestive of ecological redundancy among coral‐reef fish species. Importantly, the study places a time frame on the processes that determine spatial patterns of biodiversity in reef fish.     

Genetic population structure of the endemic fourline wrasse (Larabicus quadrilineatus) suggests limited larval dispersal distances in the Red Sea

The connectivity among marine populations is determined by the dispersal capabilities of adults as well as their eggs and larvae. Dispersal distances and directions have a profound effect on gene flow and genetic differentiation within species. Genetic homogeneity over large areas is a common feature of coral reef fishes and can reflect high dispersal capability resulting in high levels of gene flow. If fish larvae return to their parental reef, gene flow would be restricted and genetic differentiation could occur. Larabicus quadrilineatus (Labridae) is considered as an endemic fish species of the Red Sea and Gulf of Aden. The juveniles of this species are cleaner fish that feed on ectoparasites of other fishes. Here, we investigated the genetic population structure and gene flow in L. quadrilineatus among five locations in the Red Sea to infer connectivity among them. To estimate genetic diversity, we analysed 369 bp of 237 mitochondrial DNA control region sequences. Haplotype and nucleotide diversities were higher in the southern than in the northern Red Sea. Analysis of molecular variance (amova) detected the highest significant genetic variation between northern and central/southern populations (Phi(CT) = 0.01; P < 0.001). Migration analysis revealed a several fold higher northward than southward migration, which could be explained by oceanographic conditions and spawning season. Even though the Phi(ST) value of 0.01 is rather low and implies a long larval dispersal distance, estimates based on the isolation-by-distance model show a very low mean larval dispersal distance (0.44-5.1 km) compared to other studies. In order to enable a sustainable ornamental fishery on the fourline wrasse, the results of this study suggest that populations in the northern and southern Red Sea should be managed separately as two different stocks. The rather low larval dispersal distance of about 5 km needs to be considered in the design of marine protected areas to enable connectivity and self-seeding.     

Food selection of a corallivorous butterflyfish Chaetodon austriacus in the Red Sea, with particular emphasis on size and fish symbionts of corals

The exquisite butterflyfish Chaetodon austriacus feeds mainly on Acropora , Pocillopora , Montipora and Stylophora in the northern Red Sea. Large colonies of Acropora are preferred over smaller colonies and other coral genera, whereas avoidance is indicated for corals that are occupied by certain coral-associated gobiid fishes of the genus Gobiodon . It is suggested that, apart from coral identity, colony size and potential repellent effects of particular coral symbionts are both important sources of variation in the food selectivity of corallivorous chaetodotids.     

Near-bottom depletion of zooplankton over coral reefs: III: vertical gradient of predation pressure

Many diurnal planktivorous fish in coral reefs efficiently consume zooplankton drifting in the overlying water column. Our survey, carried out at two coral reefs in the Red Sea, showed that most of the diurnal planktivorous fish foraged near the bottom, close to the shelters from piscivores. The planktivorous fish were order of magnitude more abundant near (<1.5 m) the bottom than higher in the water column. The predation pressure exerted by these fish was assessed by measuring the consumption of brine shrimps tethered at different heights above the bottom on a vertical line which was pulled over the reef. Below 1.5 m above bottom, the shrimps survival probability sharply decreased toward the bottom. Higher in the water column, survivorship was nearly 100% with little vertical variation. Our results indicate that near-bottom depletion of zooplankton in coral reefs is likely due to intense predation at that boundary layer. Risk of predation by piscivorous fish apparently restricts planktivorous fish to forage near the bottom, with a distribution pattern greatly deviating from ideal-free distribution.     

Community structure and biogeography of shore fishes in the Gulf of Aqaba,Red Sea

Shore fish community structure off the Jordanian Red Sea coast was determined on fringing coral reefs and in a seagrass-dominated bay at 6 m and 12 m depths. A total of 198 fish species belonging to 121 genera and 43 families was recorded. Labridae and Pomacentridae dominated the ichthyofauna in terms of species richness and Pomacentridae were most abundant. Neither diversity nor species richness was correlated to depth. The abundance of fishes was higher at the deep reef slope, due to schooling planktivorous fishes. At 12 m depth abundance of fishes at the seagrass-dominated site was higher than on the coral reefs. Multivariate analysis demonstrated a strong influence on the fish assemblages by depth and benthic habitat. Fish species richness was positively correlated with hard substrate cover and habitat diversity. Abundance of corallivores was positively linked with live hard coral cover. The assemblages of fishes were different on the shallow reef slope, deep reef slope and seagrass meadows. An analysis of the fish fauna showed that the Gulf of Aqaba harbours a higher species richness than previously reported. The comparison with fish communities on other reefs around the Arabian Peninsula and Indian Ocean supported the recognition of an Arabian subprovince within the Indian Ocean. The affinity of the Arabian Gulf ichthyofauna to the Red Sea is not clear. Received in revised form: 2 November 2001 Electronic Publication     

First record of the paedomorphic fish Schindleria (Gobioidei, Schindleriidae) from the Red Sea

A male specimen of the paedomorphic fish Schindleria sp. was collected by plankton net, in February 2005, from a reef lagoon from Hurghada on the Egyptian coast of the northern Red Sea. This is the first record of the Schindleriidae in the Red Sea.     

Quantitative Analyse von Korallengemeinschaften des Sanganeb-Atolls (mittleres Rotes Meer). II. Vergleich mit einem Riffareal bei Aqaba (nördliches Rotes Meer) am Nordrande des indopazifischen Riffgürtels

Quantitative studies of coral communities in the central and northern Red Sea were designed for comparison of the community structure in both areas. The central Red Sea provides reef-building Scleractinia and reef-inhabiting Alcyonaria with optimal temperature conditions, whereas the north tip of the Gulf of Aqaba (29°30 N) represents the northernmost outpost of coral reefs in the Indian Ocean. It is generally assumed that coral diversity decreases towards the margins of the global reef-belt. In the Red Sea, generic diversity of hermatypic Scleractinia slightly decreases from the central to the northern part (51 : 48 genera); but cnidarian species abundance (species number per 25 m² area) was found to increase from 62 to 98 species and the Shannon-Wiener diversity index increased from 2.58 to 3.67 with regard to colony number. The mean colony size was 189 cm² at Sanganeb-Atoll, but only 52 cm² at Aqaba. The mean numbers of colonies were inversely related: 662 per 25 m² at Sanganeb-Atoll and 2028 at Aqaba. Uninhabited parts of the studied areas amounted to 47 % at Sanganeb-Atoll and to 56 % at Aqaba. The community structure of the studied areas indicates that occasional perturbations prevent the progress of the community towards a low-diversity equilibrium state. Since severe hydrodynamic damage is extremely rare in 10 m depth, major disturbances may occur by sedimentation, by the interference of grazers (e. g.Diadema setosum) and due to overgrowth by space-competitors (mainly soft corals). These events are to be regarded as throwbacks in the process of monopolization of the area by well adapted species. Recovery from such perturbations (i.e. recolonization of dead areas) obviously takes place at different velocities in the northern and central Red Sea, for the mean water temperature at Aqaba is 5 °C lower than in the central Red Sea. Hence the process of taking over a given space by a few species proceeds further in the central Red Sea than at its northern end. The increase in diversity per area towards high latitudes is comparable to that with depth. It is concluded from the great number of species at Aqaba that these reefs mark the northernmost outpost of the Indian Ocean only geographically but not ecophysiologically; they would occur at even higher latitudes, if the Gulf of Aqaba extended farther north.     

Vertical zonation of coral reef fishes in the Sudanese Red Sea

The vertical zonation of 38 species of fish inhabiting coral reefs in the Sudanese Red Sea is described. A marked degree of vertical zonation of the fishes is shown to exist. The usefulness of a depth oriented survey method for studying reef fish is discussed in relation to these results.General relationships between vertical zonation and species diversity are noted.     

Copper enrichment reduces thermal tolerance of the highly resistant Red Sea coral Stylophora pistillata

Coral Reefs - Corals in the Gulf of Aqaba (GoA) in the northern Red Sea show high thermal tolerance. The GoA has therefore been suggested as a coral reef refuge from climate change. However, as a...     

Coral frameworks revisited–reefs and coral carpets in the northern Red Sea

 Coral communities were investigated in the northern Red Sea, in the Gulfs of Suez and Aqaba, for their framework building potential. Five types of coral frameworks were differentiated: Acropora reef framework, Porites reef framework, Porites carpet, faviid carpet, and Stylophora carpet. Two non-framework community types were found: the Stylophora-Acropora community, and soft coral communities. Reef frameworks show a clear ecological zonation along depth and hydrodynamic exposure gradients, with clear indicator communities for each zone. By definition, coral carpets build a framework but lack distinct zonation patterns since they grow only in areas without pronounced gradients. In the northern Red Sea they show a gradual change with depth from Porites to faviid dominance. A Stylophora carpet is restricted to shallow water in the northern Gulf of Suez. Although growth rates of carpets may be somewhat less than those of reefs, the carbonate accumulation is considered to be higher in carpet areas due to their significantly higher areal extension. In addition, reefs and carpets have different sediment retention characteristics – the carpet retains, the reef exports. The in situ fossilization potential of coral carpets is expected to be higher than that of reef frameworks. Accepted: 25 May 1999     

Spatial distribution of fifty ornamental fish species on coral reefs in the Red Sea and Gulf of Aden

The spatial distribution of 50 ornamental fish species from shallow water habitats on coral reefs were investigated using visual census techniques, between latitudes 11−29°N in the Red Sea, in Jordan, Egypt, Saudi Arabia, and Yemen, and in the adjacent Gulf of Aden in Djibouti. One hundred eighteen transects (each 100×5 m) were examined in 29 sites (3−8 sites per country). A total of 522,523 fish individuals were counted during this survey, with mean abundance of 4428.2 ± 87.26 individual per 500 m² transect. In terms of relative abundance (RA), the most abundant species were Blue green damselfish, Chromis viridis (RA=54.4%),followed bySea goldie, Pseudanthias squamipinnis (RA= 34.7), Whitetail dascyllus, Dascyllus aruanus (RA= 2.6%), Marginate dascyllus, Dascyllus marginatus (RA= 2.0),Red Sea eightline flasher Paracheilinus octotaenia (RA=1.0),andKlunzinger’s wrasse, Thalassoma rueppellii (0.7%). The highest number of species (S) per 500 m² transect was found on reefs at the latitude 20° in Saudi Arabia (S=21.8), and the lowest number of species was found at the latitude 15° in Djibouti (S=11.11). The highest mean abundance (8565.8) was found on reefs at latitude 20° in Saudi Arabia and the lowest mean abundance (230) was found on reefs at latitude 22°, also in Saudi Arabia. Whereas, the highest Shannon-Wiener Diversity Index was found in reefs at the latitude 22° (H`=2.4) and the lowest was found in reefs at the latitude 20° (H`=0.6). This study revealed marked differences in the structure of ornamental fish assemblages with latitudinal distribution. The data support the presence of two major biogeographic groups of fishes in the Red Sea and Gulf of Aden: the southern Red Sea and Gulf of Aden group and the group in the northern and central Red Sea. Strong correlations were found between live coral cover and the number of fish species, abundance and Shannon-Wiener Diversity indices, and the strength of these correlations varied among the reefs. A conclusion was done that environmental differences among the reefs and the habitats investigated were important components of abundance variations and species diversity of ornamental fish along latitudinal gradients in the Red Sea and the Gulf of Aden.     

Lactococcus garvieae in wild Red Sea wrasse Coris aygula (Labridae)

Lactococcus garvieae infection in wild wrasse Coris aygula is reported, and the serological and molecular characteristics of the isolate are described. This is the first evidence of the presence of this pathogen in the Red Sea, and it follows the recent diagnosis of Mycobacterium marinum and Streptococcus iniae in wild fish from the same region. Whether all 3 pathogens are strains endemic to the Red Sea, or recent introductions into the region, remains to be determined, but their appearance over a period of a few years in wild fish populations in the northern Red Sea is consistent with an emerging trend affecting marine organisms on a global level in areas subjected to intense anthropogenic impacts.     

Mycobacteriosis in wild rabbitfish Siganus rivulatus associated with cage farming in the Gulf of Eilat, Red Sea

Infection patterns of Mycobacterium marinum were studied over a period of 3 yr in wild rabbitfish Siganus nivulatus populations associated with commercial mariculture cages and inhabiting various sites along the Israeli Red Sea coastline. Mycobacteriosis was first recorded from the Red Sea in 1990 in farmed sea bass Dicentrarchus labrax and is absent from records of studies on parasites and diseases of wild rabbitfish carried out in the 1970s and 1980s. A sharp increase in the prevalence of the disease in cultured and wild fish in the region has occurred since. A total of 1142 rabbitfish were examined over a 3 yr period from inside mariculture net cages, from the cage surroundings and from several sites along the coast. Histological sections of spleens were examined for presence of granulomatous lesions. Overall prevalence levels of 50% were recorded in the rabbitfish sampled inside the net cages and 39% at the cages' close surroundings, 21% at a sandy beach site 1.2 km westwards, 35% at Eilat harbour 3 km to the south and 42% at a coral reef site about 10 km south of the cages. In addition, 147 fish belonging to 18 native Red Sea species were sampled from 2 sites, the net cage farm perimeter and the coral reef area, and examined for similar lesions. None of those from the coral reef were infected with Mycobacterium; however, 9 of 14 species collected from the cage surroundings were infected. An increase in prevalence of mycobacteriosis in the mariculture farm area was noted from 1995 to 1997. At the same time, a significant increase in prevalence was also apparent at the coral reef sampling site. Two M. marinum isolates from rabbitfish captured at Eilat harbour and the coral reef site were shown by 16S rDNA sequencing analysis to be identical to isolates from rabbitfish trapped inside the mariculture cages as well as isolates from locally cultured sea bass D. labrax. The implications of spreading of M. marinum infection in wild fish populations in the Gulf of Eilat are discussed.