### Recent Submissions

• #### High summer temperatures amplify functional differences between coral- and algae-dominated reef communities

(Ecology, Wiley, 2020-10-17) [Article]
Shifts from coral to algal dominance are expected to increase in tropical coral reefs as a result of anthropogenic disturbances. The consequences for key ecosystem functions such as primary productivity, calcification, and nutrient recycling are poorly understood, particularly under changing environmental conditions. We used a novel in situ incubation approach to compare functions of coral- and algae-dominated communities in the central Red Sea bi-monthly over an entire year. In situ gross and net community primary productivity, calcification, dissolved organic carbon fluxes, dissolved inorganic nitrogen fluxes, and their respective activation energies were quantified to describe the effects of seasonal changes. Overall, coral-dominated communities exhibited 30% lower net productivity and 10 times higher calcification than algae-dominated communities. Estimated activation energies indicated a higher thermal sensitivity of coral-dominated communities. In these communities, net productivity and calcification were negatively correlated with temperature (>40% and >65% reduction, respectively, with +5°C increase from winter to summer), while carbon losses via respiration and dissolved organic carbon release were more than doubled at higher temperatures. In contrast, algae-dominated communities doubled net productivity in summer, while calcification and dissolved organic carbon fluxes were unaffected. These results suggest pronounced changes in community functioning associated with phase shifts. Algae-dominated communities may outcompete coral-dominated communities due to their higher productivity and carbon retention to support fast biomass accumulation while compromising the formation of important reef framework structures. Higher temperatures likely amplify these functional differences, indicating a high vulnerability of ecosystem functions of coral-dominated communities to temperatures even below coral bleaching thresholds. Our results suggest that ocean warming may not only cause but also amplify coral-algal phase shifts in coral reefs.
• #### Total alkalinity production in a mangrove ecosystem reveals an overlooked Blue Carbon component

(Limnology and Oceanography Letters, Wiley, 2020-10-16) [Article]
Mangroves have the capacity to sequester organic carbon (Corg) in their sediments permanently. However, the carbon budget of mangroves is also affected by the total alkalinity (TA) budget. Principally, TA emitted from carbonate sediment dissolution is a perennial sink of atmospheric CO2. The assessment of the TA budget of mangrove carbonate sediments in the Red Sea revealed a large TA emission of 403 ± 17 mmol m−2 d−1, independent of light, seasons, or the presence of pneumatophores, compared to −36 ± 10 mmol m−2 d−1 in lagoon sediment. We estimate the TA emission from carbonate dissolution in Red Sea mangroves supported a CO2 uptake of 345 ± 15 gC m−2 yr−1, 23-fold the Corg burial rate of 15 gC m−2 yr−1. The focus on Corg burial in sediments may substantially underestimate the role of mangroves in CO2 removal. Quantifying the role of mangroves in climate change mitigation requires carbonate dissolution to be included in assessments.
• #### Organic carbon export and loss rates in the Red Sea

(Global Biogeochemical Cycles, American Geophysical Union (AGU), 2020-10-14) [Article]
The export and fate of organic carbon in the mesopelagic zone are still poorly understood and quantified due to lack of observations. We exploited data from a BGC-Argo float that was deployed in the Red Sea to study how a warm and hypoxic environment can affect the fate of the organic carbon in the ocean’s interior. We observed that only 10% of the particulate organic carbon (POC) exported survived at depth due to remineralization processes in the upper mesopelagic zone. We also found that POC exported was rapidly degraded in a first stage and slowly in a second one, which may be dependent on the palatability of the organic matter. We observed that AOU-based loss rates (a proxy of the remineralization of total organic matter) were significantly higher than the POC-based loss rates, likely because changes in AOU are mainly attributed to changes in dissolved organic carbon. Finally, we showed that POC- and AOU-based loss rates could be expressed as a function of temperature and oxygen concentration. These findings advance our understanding of the biological carbon pump and mesopelagic ecosystem.
• #### Evolution and biogeography of the Zanclea-Scleractinia symbiosis

(Coral Reefs, Springer Science and Business Media LLC, 2020-10-12) [Article]
Abstract Scleractinian corals provide habitats for a broad variety of cryptofauna, which in turn may contribute to the overall functioning of coral symbiomes. Among these invertebrates, hydrozoans belonging to the genus Zanclea represent an increasingly known and ecologically important group of coral symbionts. In this study, we analysed 321 Zanclea colonies associated with 31 coral genera collected from 11 localities across the Indo-Pacific and Caribbean regions, and used a multi-disciplinary approach to shed light on the evolution and biogeography of the group. Overall, we found high genetic diversity of hydrozoans that spans nine clades corresponding to cryptic or pseudo-cryptic species. All but two clades are associated with one or two coral genera belonging to the Complex clade, whereas the remaining ones are generalists associated with both Complex and Robust corals. Despite the observed specificity patterns, no congruence between Zanclea and coral phylogenies was observed, suggesting a lack of coevolutionary events. Most Zanclea clades have a wide distribution across the Indo-Pacific, including a generalist group extending also into the Caribbean, while two host-specific clades are possibly found exclusively in the Red Sea, confirming the importance of this peripheral region as an endemicity hotspot. Ancestral state reconstruction suggests that the most recent common ancestor of all extant coral-associated Zanclea was a specialist species with a perisarc, occurring in what is now known as the Indo-Pacific. Ultimately, a mixture of geography- and host-related diversification processes is likely responsible for the observed enigmatic phylogenetic structure of coral-associated Zanclea.
• #### Optimising sample sizes for animal distribution analysis using tracking data

(Methods in Ecology and Evolution, Wiley, 2020-10-09) [Article]
1. Knowledge of the spatial distribution of populations is fundamental to management plans for any species. When tracking data are used to describe distributions, it is sometimes assumed that the reported locations of individuals delineate the spatial extent of areas used by the target population. 2. Here, we examine existing approaches to validate this assumption, highlight caveats, and propose a new method for a more informative assessment of the number of tracked animals (i.e. sample size) necessary to identify distribution patterns. We show how this assessment can be achieved by considering the heterogeneous use of habitats by a target species using the probabilistic property of a utilisation distribution. Our methods are compiled in the R package SDLfilter. 3. We illustrate and compare the protocols underlying existing and new methods using conceptual models and demonstrate an application of our approach using a large satellite tracking data-set of flatback turtles, Natator depressus, tagged with accurate Fastloc-GPS tags (n = 69). 4. Our approach has applicability for the post-hoc validation of sample sizes required for the robust estimation of distribution patterns across a wide range of taxa, populations and life history stages of animals.
• #### Wolves in sheep’s clothing: three new cases of aggressive mimicry in Red Sea coral reef fishes

(Journal of Natural History, Informa UK Limited, 2020-09-30) [Article]
Here we document three cases of mimicry in coral reef fishes not previously reported in the literature involving two groupers (Epinephelus leucogrammicus and Plectropomus marisrubri) and a soapfish (Diploprion drachi) as mimics, and two wrasses (Larabicus quadrilineatus and Cheilinus quinquecinctus) and a blenny (Meiacanthus nigrolineatus) as models. All three cases are of aggressive mimicry, with a predatory species mimicking a harmless one, and in one of the cases, the mimicry is also Müllerian, where both the predator and harmless species are unpalatable.
• #### A connectivity portfolio effect stabilizes marine reserve performance

(Proceedings of the National Academy of Sciences, Proceedings of the National Academy of Sciences, 2020-09-29) [Article]
Well-managed and enforced no-take marine reserves generate important larval subsidies to neighboring habitats and thereby contribute to the long-term sustainability of fisheries. However, larval dispersal patterns are variable, which leads to temporal fluctuations in the contribution of a single reserve to the replenishment of local populations. Identifying management strategies that mitigate the uncertainty in larval supply will help ensure the stability of recruitment dynamics and minimize the volatility in fishery catches. Here, we use genetic parentage analysis to show extreme variability in both the dispersal patterns and recruitment contribution of four individual marine reserves across six discrete recruitment cohorts for coral grouper (Plectropomus maculatus) on the Great Barrier Reef. Together, however, the asynchronous contributions from multiple reserves create temporal stability in recruitment via a connectivity portfolio effect. This dampening effect reduces the variability in larval supply from individual reserves by a factor of 1.8, which effectively halves the uncertainty in the recruitment contribution of individual reserves. Thus, not only does the network of four marine reserves generate valuable larval subsidies to neighboring habitats, the aggregate effect of individual reserves mitigates temporal fluctuations in dispersal patterns and the replenishment of local populations. Our results indicate that small networks of marine reserves yield previously unrecognized stabilizing benefits that ensure a consistent larval supply to replenish exploited fish stocks.
• #### Haloferax profundi sp. nov. and Haloferax marisrubri sp. nov., Isolated from the Discovery Deep Brine-Seawater Interface in the Red Sea

(Microorganisms, MDPI AG, 2020-09-28) [Article]
Two extremely halophilic archaeal strains, designated SB29T and SB3T, were isolated from the brine-seawater interface of Discovery Deep in the Red Sea. Cells of both strains were pleomorphic (irregular polyhedrals, ovals, and rods) and stained Gram-negative; colonies were pigmented pink. The sequence similarity of the 16S rRNA gene of strain SB29T with that of its most closely related validly described species (Hfx. sulfurifontis DSM 16227T) and that of strain SB3T with its closest validly described relative (Hfx. denitrificans ATCC 35960T) was 98.1% and 98.6%, respectively. The incomplete draft genomes of SB29T and SB3T are 3,871,125 bp and 3,904,985 bp in size, respectively, and their DNA G + C contents are 60.75% and 65.64%, respectively. The highest ANI values between the genomes of SB29T and SB3T and the most closely related genomes in GenBank were determined as 82.6% (Hfx. sulfurifontis ATCC BAA-897T, GenBank accession no. GCA_000337835.1) and 92.6% (Haloferax denitrificans ATCC 35960T, GenBank accession no. GCA_000337795.1), respectively. These data indicate that the two new isolates cannot be classified into any recognized species of the genus Haloferax, and, therefore, two novel species of the genus Haloferax are proposed: Haloferax profundi sp. nov. (type strain SB29T = JCM 19567T = CGMCC 1.14960T) and Haloferax marisrubri sp. nov. (type strain SB3T = JCM 19566T = CGMCC 1.14958T).
• #### Discovery of deep-water coral frameworks in the northern Red Sea waters of Saudi Arabia

(Scientific Reports, Springer Science and Business Media LLC, 2020-09-18) [Article]
Abstract This paper reports a deep-water coral framework (a single colonial bush or a larger bioconstruction of coral covering the sea bottom), formed entirely by the scleractinian coral Eguchipsammia fistula (Alcock, 1902) (Dendrophylliidae), in the northern Red Sea waters of Saudi Arabia at a depth of about 640 m. The framework consists of mostly live corals with a total area of about 10 m$^{2}$ and the length of the individual coral branches range from 12 to 30 cm. Although E. fistula is ubiquitous, this discovery is the second record of a framework formed by this species and the first discovery of a large living reef in the Red Sea. The results of the genetic study indicate the potential existence of a genetic variation of E. fistula in the Red Sea. This discovery implies that the Red Sea has favorable habitats for framework-forming DWC species and highlights the need for conducting more systematic surveys for understanding their distribution, abundance, and ecology.
• #### Stimulated Raman microspectroscopy as a new method to classify microfibers from environmental samples

(Environmental Pollution, Elsevier BV, 2020-09-16) [Article]
Capsule: We present Stimulated Raman Microscopy as a new method to reliably classify environmental microfibers. The majority of analyzed microfibers were of natural origin.
• #### Temperature transcends partner specificity in the symbiosis establishment of a cnidarian

(The ISME Journal, Springer Science and Business Media LLC, 2020-09-15) [Article]
Abstract Coral reef research has predominantly focused on the effect of temperature on the breakdown of coral-dinoflagellate symbioses. However, less is known about how increasing temperature affects the establishment of new coral-dinoflagellate associations. Inter-partner specificity and environment-dependent colonization are two constraints proposed to limit the acquisition of more heat tolerant symbionts. Here, we investigated the symbiotic dynamics of various photosymbionts in different host genotypes under “optimal” and elevated temperature conditions. To do this, we inoculated symbiont-free polyps of the sea anemone Exaiptasia pallida originating from Hawaii (H2), North Carolina (CC7), and the Red Sea (RS) with the same mixture of native symbiont strains (Breviolum minutum, Symbiodinium linucheae, S. microadriaticum, and a Breviolum type from the Red Sea) at 25 and 32 °C, and assessed their ITS2 composition, colonization rates, and PSII photochemical efficiency (Fv/Fm). Symbiont communities across thermal conditions differed significantly for all hosts, suggesting that temperature rather than partner specificity had a stronger effect on symbiosis establishment. Overall, we detected higher abundances of more heat resistant Symbiodiniaceae types in the 32 °C treatments. Our data further showed that PSII photophysiology under elevated temperature improved with thermal pre-exposure (i.e., higher Fv/Fm), yet, this effect depended on host genotype and was influenced by active feeding as photochemical efficiency dropped in response to food deprivation. These findings highlight the role of temperature and partner fidelity in the establishment and performance of symbiosis and demonstrate the importance of heterotrophy for symbiotic cnidarians to endure and recover from stress.
• #### The World Coral Conservatory: A Noah's ark for corals to support survival of reef ecosystems

(PLOS Biology, Public Library of Science (PLoS), 2020-09-14) [Article]
Global change causes widespread decline of coral reefs. In order to counter the anticipated disappearance of coral reefs by the end of this century, many initiatives are emerging, including creation of marine protected areas (MPAs), reef restoration projects, and assisted evolution initiatives. Such efforts, although critically important, are locally constrained. We propose to build a “Noah’s Ark” biological repository for corals that taps into the network of the world’s public aquaria and coral reef scientists. Public aquaria will serve not only as a reservoir for the purpose of conservation, restoration, and research of reef-building corals but also as a laboratory for the implementation of operations for the selection of stress-resilient and resistant genotypes. The proposed project will provide a global dimension to coral reef education and protection as a result of the involvement of a network of public and private aquaria.
• #### Rapid Evolution of Plastic-degrading Enzymes Prevalent in the Global Ocean

(Cold Spring Harbor Laboratory, 2020-09-09) [Preprint]
Estimates of marine plastic stocks, a major threat to marine life, are far lower than expected from exponentially-increasing litter inputs, suggesting important loss factors. These may involve microbial degradation, as the plastic-degrading polyethylene terephthalate enzyme (PETase) has been reported in marine microbial communities. An assessment of 416 metagenomes of planktonic communities across the global ocean identifies 68 oceanic PETase variants (oPETase) that evolved from ancestral enzymes degrading polycyclic aromatic hydrocarbons. Nearly 20 oPETases have predicted efficiencies comparable to those of laboratory-optimized PETases, suggesting strong selective pressures directing the evolution of these enzymes. We found oPETases in 90.1% of samples across all oceans and depths, particularly abundant at 1,000 m depth, with a strong dominance of Pseudomonadales containing putative highly-efficient oPETase variants in the dark ocean. Enzymatic degradation may be removing plastic from the marine environment while providing a carbon source for bathypelagic microbial communities.
• #### Does color matter? Molecular and ecological divergence in four sympatric color morphs of a coral reef fish

(Ecology and Evolution, Wiley, 2020-09-04) [Article]
Non-sex-linked color polymorphism is common in animals and can be maintained in populations via balancing selection or, when under diversifying selection, can promote divergence. Despite their potential importance in ecological interactions and the evolution of biodiversity, their function and the mechanisms by which these polymorphisms are maintained are still poorly understood. Here, we combine field observations with life history and molecular data to compare four sympatric color morphs of the coral reef fish Paracirrhites forsteri (family Cirrhitidae) in the central Red Sea. Our findings verify that the color morphs are not sex-limited, inhabit the same reefs, and do not show clear signs of avoidance or aggression among them. A barcoding approach based on 1,276 bp of mitochondrial DNA could not differentiate the color morphs. However, when 36,769 SNPs were considered, we found low but significant population structure. Focusing on 1,121 FST outliers, we recovered distinct population clusters that corresponded to shifts in allele frequencies with each color morph harboring unique alleles. Genetic divergence at these outlier loci is accompanied by differences in growth and marginal variation in microhabitat preference. Together, life history and molecular analysis suggest subtle divergence between the color morphs in this population, the causes for which remain elusive.
• #### Potential feminization of Red Sea turtle hatchlings as indicated by in situ sand temperature profiles

(Conservation Science and Practice, Wiley, 2020-09-04) [Article]
Climate change poses a serious threat to species that demonstrate temperature-dependent sex determination, including marine turtles. Increased temperatures can result in highly female-skewed sex ratios and decreased hatching success. The pivotal temperature that delineates hatchling sex ratios is commonly considered to be 29.2°C, but whether this threshold applies to turtles in the Red Sea region has not been tested in situ. For all species of marine turtles, there is a supposed thermal range of 25–33°C in which egg incubation is successful, with prolonged temperatures above 33°C resulting in morphological abnormalities and hatchling mortality. Sand temperature data were collected from May–September 2018 from the average nesting depth of hawksbill (Eretmochelys imbricata) and green turtles (Chelonia mydas) at five study sites. We calculated the expected sex ratio based on a maximum likelihood model. The sand temperature profile at four of the sites exceeded the pivotal temperature (29.2°C) throughout the study duration, which suggests feminization of turtles could be occurring; however, the pivotal temperature in this region still needs to be empirically confirmed. The percentage of days with sand temperature exceeding the maximum thermal threshold between June 3, and September 16, 2018, was site-specific rather than determined by latitudinal temperature gradients, and ranged between 0 and 100% of days. Maximum temperature recordings were as high as 36.0 and 35.3°C at 30 and 50 cm depth, respectively. Nesting sites in the Red Sea region could already be exceeding the thermal limits and may be particularly vulnerable to rising temperatures. Sites with lower sand temperatures, such as Small Gobal Island, may represent priority areas for conservation efforts. Alternatively, local adaptation may be a reality under extremely warm conditions, thus, further research into the thermal tolerance of hatchlings in the region could provide insight on how they might adapt to future climate change.
• #### Perceptions of Marine Environmental Issues by Saudi Citizens

(Frontiers in Marine Science, Frontiers Media SA, 2020-09-03) [Article]
We depend on the sea, economically, social well-being, and for the quality of our lives, yet direct and indirect human activities have affected the marine environment, causing many problems such as overfishing and pollution at the local scale and ocean warming and acidification at the global one. Hence, addressing the cumulative effects of these activities is required to conserve the marine environment for our current and future generations. Social commitment and support for these actions depend, however, on awareness and requires, therefore, an understanding of citizens’ awareness and perceptions on these issues. We assessed the awareness and the perceptions of Saudi citizens on ocean issues through an online questionnaire about environmental issues globally and in the country. The survey was completed by 1,524 Saudi citizens 18 years old and above, with different geographic distributions, gender, and educational status. The participants identified climate change within the top three global problems, with variable level of information and trust on different sources of environmental information. Littering, sewage pollution, and chemical pollution were identified as the top three major marine issues in Saudi Arabia, with the respondents demanding an immediate action through imposing fines to polluters and more regulatory constraints to activities that act as sources of pollution as well as supporting research in science and technologies to address these environmental issues.
• #### Intentional partial beaching in a coral reef fish: a newly recorded hunting behaviour for titan triggerfish, Balistoides viridescens.

(Journal of fish biology, Wiley, 2020-09-01) [Article]
Coral reef fishes use a multitude of diverse feeding behaviours to increase their ability to successfully capture a wide range of prey. Here, we report a novel hunting behaviour in a coral reef fish, the titan triggerfish, Balistoides viridescens, where an individual was seen partially beaching itself while attempting to catch a Red Sea ghost crab, Ocypode saratan. This is the first report of this behaviour in the order Tetraodontiformes, and represents an astonishing capability for this species to exploit food resources outside their typical assumed ecological niche.
• #### Fate of Plastic Pollution in the Arabian Seas

(2020-09) [Dissertation]