Susceptibility of central Red Sea corals during a major bleaching event

A major coral bleaching event occurred in the central Red Sea near Thuwal, Saudi Arabia, in the summer of 2010, when the region experienced up to 10–11 degree heating weeks. We documented the susceptibility of various coral taxa to bleaching at eight reefs during the peak of this thermal stress. Oculinids and agaricids were most susceptible to bleaching, with up to 100 and 80 % of colonies of these families, respectively, bleaching at some reefs. In contrast, some families, such as mussids, pocilloporids, and pectinids showed low levels of bleaching (<20 % on average). We resurveyed the reefs 7 months later to estimate subsequent mortality. Mortality was highly variable among taxa, with some taxa showing evidence of full recovery and some (e.g., acroporids) apparently suffering nearly complete mortality. The unequal mortality among families resulted in significant change in community composition following the bleaching. Significant factors in the likelihood of coral bleaching during this event were depth of the reef and distance of the reef from shore. Shallow reefs and inshore reefs had a higher prevalence of bleaching. This bleaching event shows that Red Sea reefs are subject to the same increasing pressures that reefs face worldwide. This study provides a quantitative, genus-level assessment of the vulnerability of various coral groups from within the Red Sea to bleaching and estimates subsequent mortality. As such, it can provide valuable insights into the future for reef communities in the Red Sea.     

Morphology and molecules reveal two new species of Porites (Scleractinia,Poritidae) from the Red Sea and the Gulf of Aden

Two new reef coral species, Porites farasani sp. nov. and Porites hadramauti sp. nov. (Scleractinia, Poritidae), are described from the Red Sea and the Gulf of Aden. Porites farasani sp. nov. only occurs in the Farasan Islands in the southern Red Sea, while P. hadramauti sp. nov. has been collected in the Yemen Hadramaut region in the Gulf of Aden. Both species presented striking in situ differences with respect to other Porites species, and were characterized by small encrusting colonies and unusual polyp colouration. In order to test the genetic distinctiveness of P. farasani sp. nov. and P. hadramauti sp. nov. between each other and with respect to other representatives in the genus Porites, we investigated their evolutionary relationships with eight other morphological species of Porites occurring in the Red Sea and in the Gulf of Aden. Two DNA loci, the mitochondrial putative control region and the nuclear ribosomal ITS region, were sequenced, and three species delimitation approaches based on barcoding threshold (Automated Barcoding Gap Discovery) and coalescence theory (Poisson-Tree process, Generalized Mixed Yule Coalescent) were applied. Phylogenetic and species delimitation analyses were overall concordant, resolving P. farasani sp. nov. and P. hadramauti sp. nov. as two divergent but closely related lineages. Of the other morphologically defined Porites species, three were genetically differentiated (P. rus, P. columnaris and P. fontanesii), but five were genetically indistinguishable. The discovery of two regional endemics confirms the importance of the Red Sea and the Gulf of Aden as regions of high biodiversity and suggests the need for an integration of genome-wide molecular data with the re-evaluation of skeletal structures in the systematics of Porites.     

Environmental gradients predict the genetic population structure of a coral reef fish in the Red Sea

The relatively recent fields of terrestrial landscape and marine seascape genetics seek to identify the influence of biophysical habitat features on the spatial genetic structure of populations or individuals. Over the last few years, there has been accumulating evidence for the effect of environmental heterogeneity on patterns of gene flow and connectivity in marine systems. Here, we investigate the population genetic patterns of an anemonefish, Amphiprion bicinctus, along the Saudi Arabian coast of the Red Sea. We collected nearly one thousand samples from 19 locations, spanning approximately 1500 km, and genotyped them at 38 microsatellite loci. Patterns of gene flow appeared to follow a stepping‐stone model along the northern and central Red Sea, which was disrupted by a distinct genetic break at a latitude of approximately 19°N. The Red Sea is characterized by pronounced environmental gradients along its axis, roughly separating the northern and central from the southern basin. Using mean chlorophyll‐a concentrations as a proxy for this gradient, we ran tests of isolation by distance (IBD, R² = 0.52) and isolation by environment (IBE, R² = 0.64), as well as combined models using partial Mantel tests and multiple matrix regression with randomization (MMRR). We found that genetic structure across our sampling sites may be best explained by a combined model of IBD and IBE (Mantel: R² = 0.71, MMRR: R² = 0.86). Our results highlight the potential key role of environmental patchiness in shaping patterns of gene flow in species with pelagic larval dispersal. We support growing calls for the integration of biophysical habitat characteristics into future studies of population genetic structure.     

Pachyseris inattesa sp. n. (Cnidaria,Anthozoa, Scleractinia): a new reef coral species from the Red Sea and its phylogenetic relationships

A new scleractinian coral species, Pachyseris inattesa sp. n., is described from the Red Sea. Despite a superficial resemblance with some species in the agariciid genus Leptoseris with which it has been previously confused, P. inattesa sp. n. has micro-morphological characters typical of the genus Pachyseris. This genus, once part of the Agariciidae, is comprised of five extant species and is widely distributed throughout the tropical Indo-Pacific. It is currently incertae sedis as a result of recent molecular analysis and appears to be closely related to the Euphylliidae. A molecular phylogenetic reconstruction including P. inattesa sp. n., the genus type species P. rugosa, and P. speciosa, all present in the Red Sea, was performed using the mitochondrial intergenic spacer between COI and 16S-rRNA. The results confirm that P. inattesa sp. n. is a monophyletic lineage closely related to the other Pachyseris species examined.     

Movement Patterns of Juvenile Whale Sharks Tagged at an Aggregation Site in the Red Sea

Conservation efforts aimed at the whale shark, Rhincodon typus, remain limited by a lack of basic information on most aspects of its ecology, including global population structure, population sizes and movement patterns. Here we report on the movements of 47 Red Sea whale sharks fitted with three types of satellite transmitting tags from 2009–2011. Most of these sharks were tagged at a single aggregation site near Al-Lith, on the central coast of the Saudi Arabian Red Sea. Individuals encountered at this site were all juveniles based on size estimates ranging from 2.5–7 m total length with a sex ratio of approximately 1∶1. All other known aggregation sites for juvenile whale sharks are dominated by males. Results from tagging efforts showed that most individuals remained in the southern Red Sea and that some sharks returned to the same location in subsequent years. Diving data were recorded by 37 tags, revealing frequent deep dives to at least 500 m and as deep as 1360 m. The unique temperature-depth profiles of the Red Sea confirmed that several whale sharks moved out of the Red Sea while tagged. The wide-ranging horizontal movements of these individuals highlight the need for multinational, cooperative efforts to conserve R. typus populations in the Red Sea and Indian Ocean.     

Seascape genetics along environmental gradients in the Arabian Peninsula: insights from ddRAD sequencing of anemonefishes

Understanding the processes that shape patterns of genetic structure across space is a central aim of landscape genetics. However, it remains unclear how geographical features and environmental variables shape gene flow, particularly for marine species in large complex seascapes. Here, we evaluated the genomic composition of the two‐band anemonefish Amphiprion bicinctus across its entire geographical range in the Red Sea and Gulf of Aden, as well as its close relative, Amphiprion omanensis endemic to the southern coast of Oman. Both the Red Sea and the Arabian Sea are complex and environmentally heterogeneous marine systems that provide an ideal scenario to address these questions. Our findings confirm the presence of two genetic clusters previously reported for A. bicinctus in the Red Sea. Genetic structure analyses suggest a complex seascape configuration, with evidence of both isolation by distance (IBD) and isolation by environment (IBE). In addition to IBD and IBE, genetic structure among sites was best explained when two barriers to gene flow were also accounted for. One of these coincides with a strong oligotrophic–eutrophic gradient at around 16–20?N in the Red Sea. The other agrees with a historical bathymetric barrier at the straight of Bab al Mandab. Finally, these data support the presence of interspecific hybrids at an intermediate suture zone at Socotra and indicate complex patterns of genomic admixture in the Gulf of Aden with evidence of introgression between species. Our findings highlight the power of recent genomic approaches to resolve subtle patterns of gene flow in marine seascapes.     

Exploring seascape genetics and kinship in the reef sponge Stylissa carteri in the Red Sea

A main goal of population geneticists is to study patterns of gene flow to gain a better understanding of the population structure in a given organism. To date most efforts have been focused on studying gene flow at either broad scales to identify barriers to gene flow and isolation by distance or at fine spatial scales in order to gain inferences regarding reproduction and local dispersal. Few studies have measured connectivity at multiple spatial scales and have utilized novel tools to test the influence of both environment and geography on shaping gene flow in an organism. Here a seascape genetics approach was used to gain insight regarding geographic and ecological barriers to gene flow of a common reef sponge, Stylissa carteri in the Red Sea. Furthermore, a small‐scale (<1 km) analysis was also conducted to infer reproductive potential in this organism. At the broad scale, we found that sponge connectivity is not structured by geography alone, but rather, genetic isolation in the southern Red Sea correlates strongly with environmental heterogeneity. At the scale of a 50‐m transect, spatial autocorrelation analyses and estimates of full‐siblings revealed that there is no deviation from random mating. However, at slightly larger scales (100–200 m) encompassing multiple transects at a given site, a greater proportion of full‐siblings was found within sites versus among sites in a given location suggesting that mating and/or dispersal are constrained to some extent at this spatial scale. This study adds to the growing body of literature suggesting that environmental and ecological variables play a major role in the genetic structure of marine invertebrate populations.     

Strong habitat and weak genetic effects shape the lifetime reproductive success in a wild clownfish population

The relative contributions of environmental, maternal and additive genetic factors to the Lifetime reproductive success (LRS) determine whether species can adapt to rapid environmental change. Yet to date, studies quantifying LRS across multiple generations in marine species in the wild are non‐existent. Here we used 10‐year pedigrees resolved for a wild orange clownfish population from Kimbe Island (PNG) and a quantitative genetic linear mixed model approach to quantify the additive genetic, maternal and environmental contributions to variation in LRS for the self‐recruiting portion of the population. We found that the habitat of the breeder, including the anemone species and geographic location, made the greatest contribution to LRS. There were low to negligible contributions of genetic and maternal factors equating with low heritability and evolvability. Our findings imply that our population will be susceptible to short‐term, small‐scale changes in habitat structure and may have limited capacity to adapt to these changes.     

Distinct patterns of hybridization across a suture zone in a coral reef fish (Dascyllus trimaculatus)

Hybrid zones are natural laboratories for investigating the dynamics of gene flow, reproductive isolation, and speciation. A predominant marine hybrid (or suture) zone encompasses Christmas Island (CHR) and Cocos (Keeling) Islands (CKE), where 15 different instances of interbreeding between closely related species from Indian and Pacific Oceans have been documented. Here, we report a case of hybridization between genetically differentiated Pacific and Indian Ocean lineages of the three‐spot dascyllus, Dascyllus trimaculatus (Rüppell, 1829). Field observations indicate there are subtle color differences between Pacific and Indian Ocean lineages. Most importantly, population densities of color morphs and genetic analyses (mitochondrial DNA and SNPs obtained via RADSeq) suggest that the pattern of hybridization within the suture zone is not homogeneous. At CHR, both color morphs were present, mitochondrial haplotypes of both lineages were observed, and SNP analyses revealed both pure and hybrid genotypes. Meanwhile, in CKE, the Indian Ocean color morphs were prevalent, only Indian Ocean mitochondrial haplotypes were observed, and SNP analysis showed hybrid individuals with a large proportion (~80%) of their genotypes assigning to the Indian Ocean lineage. We conclude that CHR populations are currently receiving an influx of individuals from both ocean basins, with a greater influence from the Pacific Ocean. In contrast, geographically isolated CKE populations appear to be self‐recruiting and with more influx of individuals from the Indian Ocean. Our research highlights how patterns of hybridization can be different at scales of hundreds of kilometers, due to geographic isolation and the history of interbreeding between lineages.     

Management under uncertainty: guide-lines for incorporating connectivity into the protection of coral reefs

The global decline in coral reefs demands urgent management strategies to protect resilience. Protecting ecological connectivity, within and among reefs, and between reefs and other ecosystems is critical to resilience. However, connectivity science is not yet able to clearly identify the specific measures for effective protection of connectivity. This article aims to provide a set of principles or practical guidelines that can be applied currently to protect connectivity. These ‘rules of thumb’ are based on current knowledge and expert opinion, and on the philosophy that, given the urgency, it is better to act with incomplete knowledge than to wait for detailed understanding that may come too late. The principles, many of which are not unique to connectivity, include: (1) allow margins of error in extent and nature of protection, as insurance against unforeseen or incompletely understood threats or critical processes; (2) spread risks among areas; (3) aim for networks of protected areas which are: (a) comprehensive and spread—protect all biotypes, habitats and processes, etc., to capture as many possible connections, known and unknown; (b) adequate—maximise extent of protection for each habitat type, and for the entire region; (c) representative—maximise likelihood of protecting the full range of processes and spatial requirements; (d) replicated—multiple examples of biotypes or processes enhances risk spreading; (4) protect entire biological units where possible (e.g. whole reefs), including buffers around core areas. Otherwise, choose bigger rather than smaller areas; (5) provide for connectivity at a wide range of dispersal distances (within and between patches), emphasising distances <20–30 km; and (6) use a portfolio of approaches, including but not limited to MPAs. Three case studies illustrating the application of these principles to coral reef management in the Bohol Sea (Philippines), the Great Barrier Reef (Australia) and Kimbe Bay (Papua New Guinea) are described.