Responses of the coral reef cryptobiome to environmental gradients in the Red Sea.

An essential component of the coral reef animal diversity is the species hidden in crevices within the reef matrix, referred to as the cryptobiome. These organisms play an important role in nutrient cycling and provide an abundant food source for higher trophic levels, yet they have been largely overlooked. Here, we analyzed the distribution patterns of the mobile cryptobiome (>2000 µm) along the latitudinal gradient of the Saudi Arabian coast of the Red Sea. Analysis was conducted based on 54 Autonomous Reef Monitoring Structures. We retrieved a total of 5273 organisms, from which 2583 DNA sequences from the mitochondrially encoded cytochrome c oxidase I were generated through sanger sequencing. We found that the cryptobiome community is variable over short geographical distances within the basin. Regression tree models identified sea surface temperature (SST), percentage cover of hard coral and turf algae as determinant for the number of operational taxonomic units present per Autonomous Reef Monitoring Structures (ARMS). Our results also show that the community structure of the cryptobiome is associated with the energy available (measured as photosynthetic active radiation), sea surface temperature, and nearby reef habitat characteristics (namely hard corals, turf and macroalgae). Given that temperature and reef benthic characteristics affect the cryptobiome, current scenarios of intensive climate change are likely to modify this fundamental biological component of coral reef functioning. However, the trajectory of change is unknow and can be site specific, as for example, diversity is expected to increase above SST of 28.5°C, and with decreasing hard coral and turf cover. This study provides a baseline of the cryptobenthic community prior to major coastal developments in the Red Sea to be used for future biodiversity studies and monitoring projects. It can also contribute to better understand patterns of reef biodiversity in a period where Marine Protected Areas are being discussed in the region.

Probiotics reshape the coral microbiome in situ without detectable off-target effects in the surrounding environment.

Beneficial microorganisms for corals (BMCs), or probiotics, can enhance coral resilience against stressors in laboratory trials. However, the ability of probiotics to restructure the coral microbiome in situ is yet to be determined. As a first step to elucidate this, we inoculated putative probiotic bacteria (pBMCs) on healthy colonies of Pocillopora verrucosa in situ in the Red Sea, three times per week, during 3 months. pBMCs significantly influenced the coral microbiome, while bacteria of the surrounding seawater and sediment remained unchanged. The inoculated genera Halomonas, Pseudoalteromonas, and Bacillus were significantly enriched in probiotic-treated corals. Furthermore, the probiotic treatment also correlated with an increase in other beneficial groups (e.g., Ruegeria and Limosilactobacillus), and a decrease in potential coral pathogens, such as Vibrio. As all corals (treated and non-treated) remained healthy throughout the experiment, we could not track health improvements or protection against stress. Our data indicate that healthy, and therefore stable, coral microbiomes can be restructured in situ, although repeated and continuous inoculations may be required in these cases. Further, our study provides supporting evidence that, at the studied scale, pBMCs have no detectable off-target effects on the surrounding microbiomes of seawater and sediment near inoculated corals.

Management and research efforts are failing dolphins, porpoises, and other toothed whales.

Despite being subject to intensive research and public interest many populations of dolphins, porpoises, and other toothed whales (small cetaceans) continue to decline, and several species are on the verge of extinction. We examine small cetacean status, human activities driving extinction risk, and whether research efforts are addressing priority threats. We estimate that 22% of small cetaceans are threatened with extinction, with little signs of improvement in nearly thirty years. Fisheries and coastal habitat degradation are the main predictors of extinction risk. Contrary to popular belief, we show that the causal impact of small-scale fisheries on extinction risk is greater than from large-scale fisheries. Fisheries management strength had little influence on extinction risk, suggesting that the implementation of existing measures have been largely ineffective. Alarmingly, we find research efforts for priority threats to be vastly underrepresented and so a major shift in research focus is required. Small cetaceans are among the lower hanging fruits of marine conservation; continued failure to halt their decline bodes poorly for tackling marine biodiversity loss and avoiding an Anthropocene mass extinction.

Low diversity and abundance of predatory fishes in a peripheral coral reef ecosystem.

Semi-enclosed seas are often associated with elevated local threats and distinct biogeographic patterns among marine fishes, but our understanding of how fish assemblage dynamics vary in relation to relatively small semi-enclosed seas (e.g., the Gulf of Aqaba) remains limited. Baited remote underwater video surveys (n = 111) were conducted across ~300 km of coral reef habitats in the Gulf of Aqaba and the northern Red Sea. A total of 55 predatory fish species were detected, with less than half of all species (n = 23) observed in both basins. Relative abundance patterns between the Gulf of Aqaba and the northern Red Sea were variable among taxa, but nearly twice as many predatory fish were observed per unit of effort in the northern Red Sea. In general, assemblages in both basins were dominated by three taxa (Epinephelinae, Carangidae, and Lethrinidae). Large-bodied and threatened species were recorded at very low abundances. Multivariate analysis revealed distinct assemblage structuring of coral reef predators between the Gulf of Aqaba and the northern Red Sea. Most of the species driving these differences were recorded in both basins, but occurred at varying levels of abundance. Environmental factors were largely unsuccessful in explaining variation in assemblage structuring. These findings indicate that biological assemblages in the Gulf of Aqaba are more distinct than previously reported and that reef fish assemblage structuring can occur even within a relatively small semi-enclosed sea. Despite inter-basin assemblage structuring, the overall low abundance of vulnerable fish species is suggestive of overexploitation in both the Gulf of Aqaba and the northern Red Sea of Saudi Arabia. As the region surveyed is currently undergoing large-scale coastal development, the results presented herein aim to guide spatial management and recovery plans for these coral reef systems in relation to this development.

Linking vertical movements of large pelagic predators with distribution patterns of biomass in the open ocean.

Many predator species make regular excursions from near-surface waters to the twilight (200 to 1,000 m) and midnight (1,000 to 3,000 m) zones of the deep pelagic ocean. While the occurrence of significant vertical movements into the deep ocean has evolved independently across taxonomic groups, the functional role(s) and ecological significance of these movements remain poorly understood. Here, we integrate results from satellite tagging efforts with model predictions of deep prey layers in the North Atlantic Ocean to determine whether prey distributions are correlated with vertical habitat use across 12 species of predators. Using 3D movement data for 344 individuals who traversed nearly 1.5 million km of pelagic ocean in [Formula: see text]42,000 d, we found that nearly every tagged predator frequented the twilight zone and many made regular trips to the midnight zone. Using a predictive model, we found clear alignment of predator depth use with the expected location of deep pelagic prey for at least half of the predator species. We compared high-resolution predator data with shipboard acoustics and selected representative matches that highlight the opportunities and challenges in the analysis and synthesis of these data. While not all observed behavior was consistent with estimated prey availability at depth, our results suggest that deep pelagic biomass likely has high ecological value for a suite of commercially important predators in the open ocean. Careful consideration of the disruption to ecosystem services provided by pelagic food webs is needed before the potential costs and benefits of proceeding with extractive activities in the deep ocean can be evaluated.

Hurdles and opportunities in implementing marine biosecurity systems in data-poor regions.

Managing marine nonindigenous species (mNIS) is challenging, because marine environments are highly connected, allowing the dispersal of species across large spatial scales, including geopolitical borders. Cross-border inconsistencies in biosecurity management can promote the spread of mNIS across geopolitical borders, and incursions often go unnoticed or unreported. Collaborative surveillance programs can enhance the early detection of mNIS, when response may still be possible, and can foster capacity building around a common threat. Regional or international databases curated for mNIS can inform local monitoring programs and can foster real-time information exchange on mNIS of concern. When combined, local species reference libraries, publicly available mNIS databases, and predictive modeling can facilitate the development of biosecurity programs in regions lacking baseline data. Biosecurity programs should be practical, feasible, cost-effective, mainly focused on prevention and early detection, and be built on the collaboration and coordination of government, nongovernment organizations, stakeholders, and local citizens for a rapid response.

Inter-nesting, migration, and foraging behaviors of green turtles (Chelonia mydas) in the central-southern Red Sea.

Sea turtles are migratory with nesting and foraging areas in distinct and often widely separated habitats. Telemetry has been a vital tool for tracking sea turtle migrations between these areas, but tagging efforts are often focused on only a few large rookeries in a given region. For instance, turtle tagging in the Red Sea has been focused in the north of the basin. We tagged five green turtles (Chelonia mydas) at a nesting site in the central-southern Red Sea and tracked them for 72-243 days. During the inter-nesting period, the turtles showed high site-fidelity, with a maximum home range of 161 km2. After the nesting season, the turtles migrated up to 1100 km to five distinct foraging locations in three countries (Saudi Arabia, Sudan, and Eritrea). Movements within foraging habitats were more wide-ranging compared to inter-nesting movements, with home ranges varying between 1.19 and 931 km2. The tracking data revealed that the creation of a relatively small marine reserve could protect the critical inter-nesting habitat in the Farasan Banks. The results also highlight the need for multinational collaboration to protect migratory corridors and foraging sites of this endangered species.

Widespread diversity deficits of coral reef sharks and rays.

A global survey of coral reefs reveals that overfishing is driving resident shark species toward extinction, causing diversity deficits in reef elasmobranch (shark and ray) assemblages. Our species-level analysis revealed global declines of 60 to 73% for five common resident reef shark species and that individual shark species were not detected at 34 to 47% of surveyed reefs. As reefs become more shark-depleted, rays begin to dominate assemblages. Shark-dominated assemblages persist in wealthy nations with strong governance and in highly protected areas, whereas poverty, weak governance, and a lack of shark management are associated with depauperate assemblages mainly composed of rays. Without action to address these diversity deficits, loss of ecological function and ecosystem services will increasingly affect human communities.

A Preliminary Report of Plastic Ingestion by Hawksbill and Green Turtles in the Saudi Arabian Red Sea.

(1) Background: Plastic pollution is a major environmental concern confronting marine animals. Sea turtles are considered a bio-indicator of plastic pollution, but there is little information regarding plastic ingestion by turtles in the Red Sea. With large-scale development projects being built along the Saudi Arabian coast, it is important to have a baseline for plastic ingestion before construction is complete. (2) Methods: Ten deceased sea turtles (four hawksbill and six green turtles) were collected along the Saudi Arabian coastline. Necropsies were conducted, and the entire gastrointestinal tracts were extracted and the contents were passed through a 1 mm mesh sieve. (3) Results: We found that 40% of the turtles in this study had ingested plastics. Thread-like plastics were the most common plastic category, and multi-colored was the most prevalent color category. (4) Conclusions: Monitoring of the plastic ingestion by marine megafauna should be conducted as a long-term assessment of the developments' impacts. Additionally, conservation efforts should be focused on removing plastics (namely ghost nests and fishing lines) from the reefs and reducing the amount of plastic entering the sea.

First record of Boulenger's anthias Sacura boulengeri (Heemstra 1973) in the Red Sea.

In November 2020, we observed several individuals and collected one juvenile of an unidentified anthiadine fish (Serranidae) between depths of 250 and 307 m near vertical walls of rocky reefs in the northern Red Sea. Further morphological and molecular analyses revealed that the collected specimen matches Sacura boulengeri, a species previously reported only from the Gulf of Oman to India.

Interaction effects of crude oil and nutrient exposure on settlement of coral reef benthos.

Anthropogenic stressors increasingly cause ecosystem-level changes to sensitive marine habitats such as coral reefs. Intensification of coastal development and shipping traffic can increase nutrient and oil pollution on coral reefs, yet these two stressors have not been studied in conjunction. Here, we simulate a disturbance scenario exposing carbonate settlement tiles to nutrient and oil pollution in a full-factorial design with four treatments: control, nutrients, oil, and combination to examine community structure and net primary productivity (NPP) of pioneer communities throughout 28 weeks. Compared to the control treatment oil pollution decreased overall settlement and NPP, while nutrients increased turf algae and NPP. However, the combination of these two stressors resulted in similar community composition and NPP as the control. These results indicate that pioneer communities may experience shifts due to nutrient enrichment, and/or oil pollution. However, the timing and duration of an event will influence recovery trajectories requiring further study.

Coral bleaching due to cold stress on a central Red Sea reef flat.

Ocean warming is leading to more frequent coral bleaching events. However, cold stress can also induce bleaching in corals. Here, we report observations of a boreal winter bleaching event in January 2020 in the central Red Sea, mainly within a population of the branching coral Stylophora pistillata on an offshore reef flat. Sea surface temperatures (SSTs) rarely fall below 24°C in this region, but data loggers deployed on several nearby reef flats recorded overnight seawater temperatures as low as 18°C just 3 days before the observations. The low temperatures coincided with an extremely low tide and cool air temperatures, likely resulting in the aerial exposure of the corals during the night time low-tide event. The risk of aerial exposure is rare in winter months, as the Red Sea exhibits seasonal fluctuations in sea level with winter values typically 0.3-0.4 m higher than in summer. These observations are notable for a region typically characterized as a high-temperature sea, and highlight the need for long-term monitoring programs as this rare event may have gone unnoticed.

Demographic histories shape population genomics of the common coral grouper (Plectropomus leopardus).

Many coral reef fishes display remarkable genetic and phenotypic variation across their geographic ranges. Understanding how historical and contemporary processes have shaped these patterns remains a focal question in evolutionary biology since they reveal how diversity is generated and how it may respond to future environmental change. Here, we compare the population genomics and demographic histories of a commercially and ecologically important coral reef fish, the common coral grouper (Plectropomus leopardus [Lacépède 1802]), across two adjoining regions (the Great Barrier Reef; GBR, and the Coral Sea, Australia) spanning approximately 14 degrees of latitude and 9 degrees of longitude. We analysed 4548 single nucleotide polymorphism (SNP) markers across 11 sites and show that genetic connectivity between regions is low, despite their relative proximity (~100 km) and an absence of any obvious geographic barrier. Inferred demographic histories using 10,479 markers suggest that the Coral Sea population was founded by a small number of GBR individuals and that divergence occurred ~190 kya under a model of isolation with asymmetric migration. We detected population expansions in both regions, but estimates of contemporary effective population sizes were approximately 50% smaller in Coral Sea sites, which also had lower genetic diversity. Our results suggest that P. leopardus in the Coral Sea have experienced a long period of isolation that precedes the recent glacial period (~10-120 kya) and may be vulnerable to localized disturbances due to their relative reliance on local larval replenishment. While it is difficult to determine the underlying events that led to the divergence of the Coral Sea and GBR lineages, we show that even geographically proximate populations of a widely dispersed coral reef fish can have vastly different evolutionary histories.

A multi-method characterization of Elasmobranch & Cheloniidae communities of the north-eastern Red Sea and Gulf of Aqaba.

The Red Sea is particularly biodiverse, hosting high levels of endemism and numerous populations whose extinction risk is heightened by their relative isolation. Elasmobranchs and sea turtles have likely suffered recent declines in this region, although data on their distribution and biology are severely lacking, especially on the eastern side of the basin in Saudi Arabian waters. Here, we present sightings of elasmobranchs and sea turtles across the north-eastern Red Sea and Gulf of Aqaba collected through a combination of survey methods. Over 455 survey hours, we recorded 407 sightings belonging to 26 elasmobranch species and two sea turtle species, more than 75% of which are of conservation concern. We identified 4 species of rays and 9 species of sharks not previously recorded in Saudi Arabia and report a range extension for the pink whipray (Himantura fai) and the round ribbontail ray (Taeniurops meyeni) into the Gulf of Aqaba. High density of sightings of conservation significance, including green and hawksbill sea turtles and halavi guitarfish were recorded in bay systems along the eastern Gulf of Aqaba and the Saudi Arabian coastline bordering the north-eastern Red Sea, and many carcharhinid species were encountered at offshore seamounts in the region. Our findings provide new insights into the distribution patterns of megafaunal assemblages over smaller spatial scales in the region, and facilitate future research and conservation efforts, amidst ongoing, large-scale coastal developments in the north-eastern Red Sea and Gulf of Aqaba.

Size structure of the coral Stylophora pistillata across reef flat zones in the central Red Sea.

Demographic analyses offer insight into the state of a population. Here, we surveyed different reef flat zones (exposed, midreef and sheltered) of six reefs over a cross-shelf gradient to characterize the population structure of Stylophora pistillata, a coral species which dominates reef flats in the central Red Sea. Phototransects were conducted at each reef flat zone, and the density of S. pistillata, the planar area of each colony, and the occurrence of partial mortality were calculated using the program ImageJ. Each colony was also assigned a color morph (yellow, purple or mixed colors). Density and mean size were extremely variable, both among reef flat zones and reefs, but overall, both metrics were lower on the midshelf reefs. The yellow color morph accounted for nearly 90% of colonies surveyed and dominated most reef flats assessed, with the exception of one site where 81% of colonies were purple morphs. There were no spatial trends in the percentage of colonies suffering partial mortality, but overall there is a positive correlation with size class and proportion of colonies with partial mortality. Despite few trends emerging from assessing individual parameters, a PERMANOVA analysis revealed differences among reef flat zones in most of the reefs, highlighting the importance of multivariate analysis. The data presented here serve as a baseline for monitoring and may identify possible future demographic changes to this important coral species in a region increasingly affected by bleaching events.

An assessment of heavy metals in green sea turtle (Chelonia mydas) hatchlings from Saudi Arabia's largest rookery, Ras Baridi.

Background: Anthropogenic sources can lead to the accumulation of heavy metals in marine organisms through ingestion, absorption, or inhalation. For sea turtle embryos, heavy metals can be absorbed into the egg from the incubation environment or be maternally transferred to the offspring causing neurological, reproductive, and developmental problems. Here, we report heavy metal concentrations in green turtle hatchlings from the largest rookery on the Red Sea, Ras Baridi. Methods: Deceased hatchlings were collected from two beaches near a cement factory at Ras Baridi, from which heavy metal concentrations (chromium (Cr), manganese (Mn), iron (Fe), cobalt (Co), nickel (Ni), copper (Cu), zinc (Zn), arsenic (As), selenium (Se), cadmium (Cd), and lead (Pb)) were measured from the liver, muscle, and residual yolk of the hatchlings. Results: Although based on a small sample of hatchlings, the data presented here provides the first measurements of heavy metals from sea turtles in the Red Sea and highlights the link between human activity and its impact on the ecology of sea turtles. In general, the heavy metal concentrations of heavy metals were not significantly different between the beach next to the cement factory and the beach downwind from the factory. However, the concentrations of heavy metals were significantly different between sampled tissues (liver, muscle, and residual yolk). Discussion: This study provides insight into current heavy metal levels in green turtle hatchlings, which can be used as bio-indicators for environmental contaminants as coastal development increases in the Red Sea. Moreover, we found a lack of standardized methodology to evaluate heavy metals in hatchling sea turtles. Future efforts should work toward creating comparable techniques for long-term heavy metal monitoring, as this is a useful determinant of anthropogenic pollution.

Newly described nesting sites of the green sea turtle (Chelonia mydas) and the hawksbill sea turtle (Eretmochelys imbricata) in the central Red Sea.

Background: There is relatively little published information about sea turtle nesting distribution and seasonality in the Saudi Arabian Red Sea. Upcoming large-scale developments occurring along the Saudi Arabian Red Sea coast could negatively affect many sea turtle nesting beaches with potential impacts on the survival of local populations. Methods: In 2019, two coastal beaches and three near-shore islands were surveyed for turtle nesting in the central Red Sea. We recorded all emergences, examined beach morphology, and collected sand samples to determine grain size, moisture content and colour. Results: Sea turtle nesting was found at all surveyed sites, though emergence counts were often low. The limited occurrence of nesting at several previously undocumented sites suggests that nesting activity may be widespread, but sparsely distributed, in the central Red Sea region. In addition, nesting at novel sites appeared to favour the seaward side of islands, a pattern that was not observed in previously documented areas. The substrate of most surveyed sites was composed of calcium carbonate with Ras Baridi as the only exception; it was composed of dark quartz-rich sediment. This study highlights several important sea turtle rookeries while also demonstrating that low levels of nesting occur throughout the region, although inter-annual nesting patterns still need to be determined. Future developments should be steered away from key nesting areas and the seaward bias in marginal rookeries should be taken into account where possible.

Acanthopagrus oconnorae, a new species of seabream (Sparidae) from the Red Sea.

A new species of sparid fish, Acanthopagrus oconnorae, is described based on 11 specimens collected in the shallow (0-1 m depth) mangrove-adjacent sandflats of Thuwal, Saudi Arabia. The new species is distinguished from its congeners by the following combination of characters: second anal-fin spine 12.8%-16.6% of standard length (SL); 3½ scale rows between the fifth dorsal-fin spine and lateral line; suborbital width 5.7%-6.7% of SL; eyes positioned at the anterior edge of the head, often forming a weakly convex break in an otherwise gently curved head profile, when viewed laterally; caudal fin light yellow with black posterior margin (approximately half of fin); anal fin dusky grey, with posterior one-fifth of the fin light yellow; black streaks on inter-radial membranes of anal fin absent. The most similar species to A. oconnorae is Acanthopagrus vagus, which differs by the presence of a w-shaped anterior edge of the scaled predorsal area, a more acute snout and black streaks on the inter-radial membranes of the anal fin. Phylogenetic placement and species delimitation of A. oconnorae are discussed based on COI, CytB and 16S sequences. It is hypothesized that ecology and behaviour explain how this species avoided detection despite its likely occurrence in coastal areas of the Red Sea with historically high fishing pressure.

Global collision-risk hotspots of marine traffic and the world's largest fish, the whale shark.

Marine traffic is increasing globally yet collisions with endangered megafauna such as whales, sea turtles, and planktivorous sharks go largely undetected or unreported. Collisions leading to mortality can have population-level consequences for endangered species. Hence, identifying simultaneous space use of megafauna and shipping throughout ranges may reveal as-yet-unknown spatial targets requiring conservation. However, global studies tracking megafauna and shipping occurrences are lacking. Here we combine satellite-tracked movements of the whale shark, Rhincodon typus, and vessel activity to show that 92% of sharks' horizontal space use and nearly 50% of vertical space use overlap with persistent large vessel (>300 gross tons) traffic. Collision-risk estimates correlated with reported whale shark mortality from ship strikes, indicating higher mortality in areas with greatest overlap. Hotspots of potential collision risk were evident in all major oceans, predominantly from overlap with cargo and tanker vessels, and were concentrated in gulf regions, where dense traffic co-occurred with seasonal shark movements. Nearly a third of whale shark hotspots overlapped with the highest collision-risk areas, with the last known locations of tracked sharks coinciding with busier shipping routes more often than expected. Depth-recording tags provided evidence for sinking, likely dead, whale sharks, suggesting substantial "cryptic" lethal ship strikes are possible, which could explain why whale shark population declines continue despite international protection and low fishing-induced mortality. Mitigation measures to reduce ship-strike risk should be considered to conserve this species and other ocean giants that are likely experiencing similar impacts from growing global vessel traffic.

Potential effects of heavy metal pollution from a cement factory near Saudi Arabia's largest green turtle rookery.

Sand samples were collected from four beaches near a cement factory in Ras Baridi, north of Yanbu, which hosts the largest green turtle rookery in Saudi Arabia. Heavy metal concentrations (Cd, Pb, Fe, Cr, Ni, Se, Sb, As, and Cu) were measured at three different depths. For most elements, there were no significant differences in concentrations among depths; however, significant differences were found among the nesting beaches in Ras Baridi, which were likely influenced by the wind direction from the factory. Fe, Cr, Cu, and Ni had elevated contamination factor values, suggesting that the nesting beaches downwind and adjacent to the cement factory contained moderately contaminated sand. Given the possibility of heavy metals being absorbed through eggshells, there is a potential risk of heavy metal contamination in clutches laid in Ras Baridi. The rising threat to the local ecology in Saudi Arabia due to recent coastal developments for tourism projects highlights the importance of monitoring heavy metal concentrations over time.