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Recent Submissions

  • Impacts of hypoxic events surpass those of future ocean warming and acidification

    Sampaio, Eduardo; Santos, Catarina; Rosa, Inês C.; Ferreira, Verónica; Pörtner, Hans-Otto; Duarte, Carlos M.; Levin, Lisa A.; Rosa, Rui (Nature Ecology & Evolution, Springer Science and Business Media LLC, 2021-01-11) [Article]
    Over the past decades, three major challenges to marine life have emerged as a consequence of anthropogenic emissions: ocean warming, acidification and oxygen loss. While most experimental research has targeted the first two stressors, the last remains comparatively neglected. Here, we implemented sequential hierarchical mixed-model meta-analyses (721 control–treatment comparisons) to compare the impacts of oxygen conditions associated with the current and continuously intensifying hypoxic events (1–3.5 O2 mg l−1) with those experimentally yielded by ocean warming (+4 °C) and acidification (−0.4 units) conditions on the basis of IPCC projections (RCP 8.5) for 2100. In contrast to warming and acidification, hypoxic events elicited consistent negative effects relative to control biological performance—survival (–33%), abundance (–65%), development (–51%), metabolism (–33%), growth (–24%) and reproduction (–39%)—across the taxonomic groups (mollusks, crustaceans and fish), ontogenetic stages and climate regions studied. Our findings call for a refocus of global change experimental studies, integrating oxygen concentration drivers as a key factor of ocean change. Given potential combined effects, multistressor designs including gradual and extreme changes are further warranted to fully disclose the future impacts of ocean oxygen loss, warming and acidification.
  • The skeletome of the red coral Corallium rubrum indicates an independent evolution of biomineralization process in octocorals

    Le Roy, Nathalie; Ganot, Philippe; Aranda, Manuel; Allemand, Denis; Tambutté, Sylvie (BMC Ecology and Evolution, Springer Science and Business Media LLC, 2021-01-11) [Article]
    Abstract Background The process of calcium carbonate biomineralization has arisen multiple times during metazoan evolution. In the phylum Cnidaria, biomineralization has mostly been studied in the subclass Hexacorallia (i.e. stony corals) in comparison to the subclass Octocorallia (i.e. red corals); the two diverged approximately 600 million years ago. The precious Mediterranean red coral, Corallium rubrum, is an octocorallian species, which produces two distinct high-magnesium calcite biominerals, the axial skeleton and the sclerites. In order to gain insight into the red coral biomineralization process and cnidarian biomineralization evolution, we studied the protein repertoire forming the organic matrix (OM) of its two biominerals. Results We combined High-Resolution Mass Spectrometry and transcriptome analysis to study the OM composition of the axial skeleton and the sclerites. We identified a total of 102 OM proteins, 52 are found in the two red coral biominerals with scleritin being the most abundant protein in each fraction. Contrary to reef building corals, the red coral organic matrix possesses a large number of collagen-like proteins. Agrin-like glycoproteins and proteins with sugar-binding domains are also predominant. Twenty-seven and 23 proteins were uniquely assigned to the axial skeleton and the sclerites, respectively. The inferred regulatory function of these OM proteins suggests that the difference between the two biominerals is due to the modeling of the matrix network, rather than the presence of specific structural components. At least one OM component could have been horizontally transferred from prokaryotes early during Octocorallia evolution. Conclusion Our results suggest that calcification of the red coral axial skeleton likely represents a secondary calcification of an ancestral gorgonian horny axis. In addition, the comparison with stony coral skeletomes highlighted the low proportion of similar proteins between the biomineral OMs of hexacorallian and octocorallian corals, suggesting an independent acquisition of calcification in anthozoans.
  • Imaging of organic signals in individual fossil diatom frustules with nanoSIMS and Raman spectroscopy

    Akse, Shaun P.; Das, Gobind; Agusti, Susana; Pichevin, Laetitia; Polerecky, Lubos; Middelburg, Jack J. (Marine Chemistry, Elsevier BV, 2021-01) [Article]
    The organic matter occluded in the silica of fossil diatom frustules is thought to be protected from diagenesis and used for paleoceanographic reconstructions. However, the location of the organic matter within the frustule has hitherto not been identified. Here, we combined high spatial resolution imaging by nanoSIMS and Raman micro-spectroscopy to identify where the organic material is retained in cleaned fossil diatom frustules. NanoSIMS imaging revealed that organic signals were present throughout the frustule but in higher concentrations at the pore walls. Raman measurements confirmed the heterogenous presence of organics but could not, because of lower spatial resolution, resolve the spatial patterns observed by nanoSIMS.
  • Imprint of Climate Change on Pan-Arctic Marine Vegetation

    Krause-Jensen, Dorte; Archambault, Philippe; Assis, Jorge; Bartsch, Inka; Bischof, Kai; Filbee-Dexter, Karen; Dunton, Kenneth H.; Maximova, Olga; Ragnarsdóttir, Sunna Björk; Sejr, Mikael K.; Simakova, Uliana; Spiridonov, Vassily; Wegeberg, Susse; Winding, Mie H.S.; Duarte, Carlos M. (Frontiers in Marine Science, Frontiers Media SA, 2020-12-23) [Article]
    The Arctic climate is changing rapidly. The warming and resultant longer open water periods suggest a potential for expansion of marine vegetation along the vast Arctic coastline. We compiled and reviewed the scattered time series on Arctic marine vegetation and explored trends for macroalgae and eelgrass (Zostera marina). We identified a total of 38 sites, distributed between Arctic coastal regions in Alaska, Canada, Greenland, Iceland, Norway/Svalbard, and Russia, having time series extending into the 21st Century. The majority of these exhibited increase in abundance, productivity or species richness, and/or expansion of geographical distribution limits, several time series showed no significant trend. Only four time series displayed a negative trend, largely due to urchin grazing or increased turbidity. Overall, the observations support with medium confidence (i.e., 5–8 in 10 chance of being correct, adopting the IPCC confidence scale) the prediction that macrophytes are expanding in the Arctic. Species distribution modeling was challenged by limited observations and lack of information on substrate, but suggested a current (2000–2017) potential pan-Arctic macroalgal distribution area of 820.000 km2 (145.000 km2 intertidal, 675.000 km2 subtidal), representing an increase of about 30% for subtidal- and 6% for intertidal macroalgae since 1940–1950, and associated polar migration rates averaging 18–23 km decade–1. Adjusting the potential macroalgal distribution area by the fraction of shores represented by cliffs halves the estimate (412,634 km2). Warming and reduced sea ice cover along the Arctic coastlines are expected to stimulate further expansion of marine vegetation from boreal latitudes. The changes likely affect the functioning of coastal Arctic ecosystems because of the vegetation’s roles as habitat, and for carbon and nutrient cycling and storage. We encourage a pan-Arctic science- and management agenda to incorporate marine vegetation into a coherent understanding of Arctic changes by quantifying distribution and status beyond the scattered studies now available to develop sustainable management strategies for these important ecosystems.
  • Patterns, drivers, and ecological implications of upwelling in coral reef habitats of the southern Red Sea

    De Carlo, Thomas Mario; Carvalho, Susana; Gajdzik, Laura; Hardenstine, Royale; Tanabe, Lyndsey K.; Villalobos, Rodrigo; Berumen, Michael L. (Journal of Geophysical Research: Oceans, American Geophysical Union (AGU), 2020-12-22) [Article]
    Coral reef ecosystems are highly sensitive to thermal anomalies, making them vulnerable to ongoing global warming. Yet, a variety of cooling mechanisms, such as upwelling, can offer some respite to certain reefs. The Farasan Banks in the southern Red Sea is home to hundreds of coral reefs covering 16,000 km2 and experiences among the highest water temperatures of any coral-reef region despite exposure to summertime upwelling. We deployed an array of temperature loggers on coral reefs in the Farasan Banks, enabling us to evaluate the skill of satellite-based sea surface temperature (SST) products for capturing patterns of upwelling. Additionally, we used remote sensing products to investigate the physical drivers of upwelling, and to better understand how upwelling modulates summertime heat stress on coral communities. Our results show that various satellite SST products underestimate reef-water temperatures but differ in their ability to capture the spatial and temporal dynamics of upwelling. Monsoon winds from June to September drive the upwelling in the southern Red Sea via Ekman transport of surface waters off the shelf, and this process is ultimately controlled by the southwest Indian monsoon in the Arabian Sea. Further, the timing of the cessation of monsoon winds regulates the maximum water temperatures that are reached in September and October. In addition to describing the patterns and mechanisms of upwelling, we discuss the potential ecological implications of this upwelling system, including modulation of coral bleaching events and effects on biodiversity, sea turtle reproduction, fish pelagic larval duration, and planktivore populations.
  • Contrasting heat stress response patterns of coral holobionts across the Red Sea suggest distinct mechanisms of thermal tolerance

    Voolstra, Christian R.; Valenzuela, Jacob; Turkarslan, Serdar; Cardenas, Anny; Hume, Benjamin; Perna, Gabriela; Buitrago-López, Carol; Rowe, Katherine; Orellana, Monica; Baliga, Nitin; Paranjabe, Sumi; Banc-Prandi, Guilhem; Bellworthy, Jessica; Fine, Maoz; Frias-Torres, Sarah; Barshis, Daniel J. (Research Square, 2020-12-18) [Preprint]
    Abstract Corals from the northern Red Sea, in particular the Gulf of Aqaba (GoA), have exceptionally high bleaching thresholds approaching >5°C above their maximum monthly mean (MMM) temperatures. These elevated thresholds are thought to be due to historical selection, as corals passed through the warmer Southern Red Sea during re-colonization from the Arabian Sea. To test this hypothesis, we determined thermal tolerance thresholds of GoA versus Central Red Sea (CRS) Stylophora pistillata corals using the Coral Bleaching Automated Stress System (CBASS) to run a series of standardized acute thermal stress assays. Relative thermal thresholds of GoA and CRS corals were indeed similar and exceptionally high (~7°C above MMM). However, absolute thermal thresholds of CRS corals were on average 3°C above those of GoA corals. To explore the mechanistic underpinnings, we determined gene expression response and microbiome dynamics of coral holobiont compartments. Transcriptomic responses differed markedly, with a strong response to the thermal stress in GoA corals versus a remarkably muted response in corals from the CRS. This pattern was recapitulated in the algal symbionts that showed site-specific genetic differentiation. Concomitant to this, a subset of coral and algal genes showed temperature-induced expression in GoA corals, while exhibiting fixed high expression, i.e. front-loading, in CRS corals. Bacterial community composition of GoA corals changed dramatically under heat stress, whereas CRS corals displayed consistent assemblages, indicating distinct microbial response patterns. Our work demonstrates distinct patterns underlying thermal tolerance across spatial scales, even for the same species and ocean basin. We interpret the response of GoA corals as that of a resilient population approaching a tipping point in contrast to a pattern of consistently elevated thermal resistance in CRS corals that cannot further attune. Such response differences suggest distinct thermal tolerance mechanisms that affect the response of coral populations to ocean warming.
  • Coral Probiotics: Premise, Promise, Prospects

    Peixoto, Raquel S.; Sweet, Michael; Villela, Helena D.M.; Cardoso, Pedro; Thomas, Torsten; Voolstra, Christian R.; Høj, Lone; Bourne, David G. (Annual Review of Animal Biosciences, Annual Reviews, 2020-12-15) [Article]
    The use of Beneficial Microorganisms for Corals (BMCs) has been proposed recently as a tool for the improvement of coral health, with knowledge in this research topic advancing rapidly. BMCs are defined as consortia of microorganisms that contribute to coral health through mechanisms that include ( a) promoting coral nutrition and growth, ( b) mitigating stress and impacts of toxic compounds, ( c) deterring pathogens, and ( d) benefiting early life-stage development. Here, we review the current proposed BMC approach and outline the studies that have proven its potential to increase coral resilience to stress. We revisit and expand the list of putative beneficial microorganisms associated with corals and their proposed mechanisms that facilitate improved host performance. Further, we discuss the caveats and bottlenecks affecting the efficacy of BMCs and close by focusing on the next steps to facilitate application at larger scales that can improve outcomes for corals and reefs globally. Expected final online publication date for the Annual Review of Animal Biosciences, Volume 9 is February 2021. Please see for revised estimates.
  • KAUST Metagenomic Analysis Platform (KMAP), Enabling Access to Massive Analytics of Re-Annotated Metagenomic Data.

    Alam, Intikhab; Kamau, Allan; Gugi, David; Gojobori, Takashi; Duarte, Carlos M.; Bajic, Vladimir B. (Research Square, 2020-12-14) [Preprint]
    Abstract Exponential rise of metagenomics sequencing is delivering massive functional environmental genomics data. However, this also generates a procedural bottleneck for on-going re-analysis as reference databases grow and methods improve, and analyses need be updated for consistency, which require acceess to increasingly demanding bioinformatic and computational resources. Here, we present the KAUST Metagenomic Analysis Platform (KMAP), a new integrated open web-based tool for the comprehensive exploration of shotgun metagenomic data. We illustrate the capacities KMAP provides through the re-assembly of ~27,000 public metagenomic samples captured in ~450 studies sampled across ~77 diverse habitats, resulting in 36 new habitat-specific gene catalogs, all based on full-length (complete) genes. Extensive taxonomic and gene annotations are stored in Gene Information Tables (GITs), a simple tractable data integration format useful for analysis through command line or for database management. KMAP facilitates the exploration and comparison of microbial GITs across different habitats with over 275 million genes.
  • Exposure to natural ultraviolet B radiation levels has adverse effects on growth, behavior, physiology, and innate immune response in juvenile European seabass (Dicentrarchus labrax)

    Alves, Ricardo; Justo, Micaela S.S.; Laranja, Joseph Leopoldo Q.; Alarcon, Jorge F.; Al-Suwailem, Abdulaziz M.; Agusti, Susana (Aquaculture, Elsevier BV, 2020-12-03) [Article]
    Solar ultraviolet B radiation (UVB) has been underestimated as a stressor in fish species that grow in confined cages, especially in species cultured in oligotrophic waters that receive high levels of UVB. In this context, the present study aims to assess UVB radiation's adverse effects on European seabass (Dicentrarchus labrax), which is a cultured species in the Mediterranean and the Red Sea. Seabass juveniles were exposed for six weeks to four experimental conditions that simulated natural underwater conditions: (1) high dose - UVB-H, 11.86 kJ m−2 d−1; (2) moderate dose - UVB-M, 6.28 kJ m−2 d−1; (3) low dose - UVB-L, 2.55 kJ m−2 d−1; and (4) no UVB exposure as the control. Specimens were collected after 3, 15 (short-term), and 43 (long-term) days and effects of exposure on growth, behavior, physiology, and immune system were investigated. Overall, data showed that short- and long-term exposure to UVB resulted in detrimental effects in European seabass, and some of these effects were cumulative and dose-dependent. High mortality (around 50%) was observed in the seabass juveniles after 3 days of exposure to the highest daily dose (UVB-H). No significant mortality was observed in UVB-M, UVB-L, or control throughout the experiment. Reduction in growth and changes in animal body condition indices were evident in UVB-M exposed fish after 15 and 43 days of exposure. The swimming activity was reduced in the UVB-M treatment, and most of the fish from this treatment tried to avoid the exposure while showing a stationary behavior with slow caudal and dorsal fins movements. A lack of appetite was observed during the experiment, and the reduced total protein, glucose, lactate, and total cholesterol plasmatic levels in UVB exposed fish reflected physiological impairment. Furthermore, several changes in the humoral parameters suggest that an immune system modulation can occur in seabass exposed to the three UVB treatments (UVB-L, UVB-M, UVB-H), and during the different exposure periods (3, 15, and 43 days). Overall, our data provide evidence that, in the case of confinement in cages, European seabass juveniles are sensitive to UVB exposure, especially in oligotrophic waters with high UV radiation incidence such as the Red Sea. Hence, seabass' growth, resistance to pathogens, and survival may be affected by UVB exposure. Further research is recommended to understand how fish growth and survival may be affected by future increases in underwater UVB and when combined with other environmental stressors.
  • Vertical movements of a pelagic thresher shark (Alopias pelagicus): insights into the species’ physiological limitations and trophic ecology in the Red Sea

    Arostegui, MC; Gaube, P; Berumen, Michael L.; DiGiulian, A; Jones, Burton; Røstad, Anders; Braun, CD (Endangered Species Research, Inter-Research Science Center, 2020-12-03) [Article]
    The pelagic thresher shark Alopias pelagicus is an understudied elasmobranch harvested in commercial fisheries of the tropical Indo-Pacific. The species is endangered, overexploited throughout much of its range, and has a decreasing population trend. Relatively little is known about its movement ecology, precluding an informed recovery strategy. Here, we report the first results from an individual pelagic thresher shark outfitted with a pop-up satellite archival transmitting (PSAT) tag to assess its movement with respect to the species’ physiology and trophic ecology. A 19 d deployment in the Red Sea revealed that the shark conducted normal diel vertical migration, spending the majority of the day at 200-300 m in the mesopelagic zone and the majority of the night at 50-150 m in the epipelagic zone, with the extent of these movements seemingly not constrained by temperature. In contrast, the depth distribution of the shark relative to the vertical distribution of oxygen suggested that it was avoiding hypoxic conditions below 300 m even though that is where the daytime peak of acoustic backscattering occurs in the Red Sea. Telemetry data also indicated crepuscular and daytime overlap of the shark’s vertical habitat use with distinct scattering layers of small mesopelagic fishes and nighttime overlap with nearly all mesopelagic organisms in the Red Sea as these similarly undergo nightly ascents into epipelagic waters. We identify potential depths and diel periods in which pelagic thresher sharks may be most susceptible to fishery interactions, but more expansive research efforts are needed to inform effective management.
  • Mesoscale Eddy Dynamics and Scale in the Red Sea

    Campbell, Michael F (2020-12) [Dissertation]
    Advisor: Jones, Burton
    Committee members: Ellis, Joanne; Berumen, Michael L.; Hoteit, Ibrahim; Rainville, Luc
    Recent efforts in understanding the variability inherent in coastal and offshore waters have highlighted the need for higher resolution sampling at finer spatial and temporal resolutions. Gliders are increasingly used in these transitional waters due to their ability to provide these finer resolution data sets in areas where satellite coverage may be poor, ship-based surveys may be impractical, and important processes may occur below the surface. Since no single instrument platform provides coverage across all needed spatial and temporal scales, Ocean Observation systems are using multiple types of instrument platforms for data collection. However, this results in increasingly large volumes of data that need to be processed and analyzed and there is no current “best practice” methodology for combining these instrument platforms. In this study, high resolution glider data, High Frequency Radar (HFR), and satellite-derived data products (MERRA_2 and ARMOR3D NRT Eddy Tracking) were used to quantify: 1) dominant scales of variability of the central Red Sea, 2) determine the minimum sampling frequency required to adequately characterize the central Red Sea, 3) discriminate whether the fine scale persistency of oceanographic variables determined from the glider data are comparable to those identified using HFR and satellite-derived data products, and 4) determine additional descriptive information regarding eddy occurrence and strength in the Red Sea from 2018-2019. Both Integral Time Scale and Characteristic Length Scale analysis show that the persistence time frame from glider data for temperature, salinity, chlorophyll-α, and dissolved oxygen is 2-4 weeks and that these temporal scales match for HFR and MERRA_2 data, matching a similar description of a ”weather-band” level of temporal variability. Additionally, the description of eddy activity in the Red Sea also supports this 2-4-week time frame, with the average duration of cyclonic and anticyclonic eddies from 2018-2019 being 22 and 27 days, respectively. Adoption of scale-based methods across multiple ocean observation areas can help define “best practice” methodologies for combining glider, HFR, and satellite-derived data to better understand the naturally occurring variability and improve resource allocation.
  • Spots and Sequences: Multi-method population assessment of whale sharks in the Red Sea

    Hardenstine, Royale (2020-12) [Dissertation]
    Advisor: Berumen, Michael L.
    Committee members: Gojobori, Takashi; Jones, Burton; Hsu, Hua Hsun
    In 1938 Dr. Eugene Gudger concluded of the Red Sea that "whale sharks must surely abound in this region." Seventy years later, multi-method research began on a whale shark (Rhincodon typus) aggregation at Shib Habil, a reef near Al Lith, Saudi Arabia. However, in 2017 and 2018, a dramatic decline in encounters at this site drew questions about the aggregation's future and overall whale shark population trends in the region. In this dissertation, I describe and discuss the two-year decline in encounters and show that neither remotely sensed sea surface temperature nor chlorophyll-a concentrations were significantly different in seasons with or without sharks. Citizen science-based photo identification was used to characterize the northern Red Sea population, the Red Sea population as a whole, show limited crossover within the basin, and connections with another aggregation in Djibouti. Scarring rates within the Red Sea are compared to recent global studies, and the Red Sea uniquely had no predator bites observed, suggesting boat collisions are likely the leading cause of major scars. Finally, building upon previous genetic work comparing Red Sea and Tanzanian sharks using microsatellites, the mitochondrial control region was sequenced, and two global haplotype networks were produced and compared to each other and previous work. The stability of genetic diversity within the Shib Habil aggregation is compared to declines previously measured in Australia. As tourism develops along the northern Saudi Arabian coast and citizen science increases in the Red Sea, population dynamics within the region could be better understood. The genetic connectivity of Red Sea whale sharks to the Indo-Pacific population exemplifies the need for continued collaborative research beyond local aggregations and multinational conservation measures.
  • Refining patterns of species distributions, genetic diversity, and life history traits in bonefish Albula spp. from the Red Sea.

    Williams, Collin T.; McIvor, Ashlie J; Wallace, Elizabeth M; Jia, Lin Yu; Berumen, Michael L. (Journal of fish biology, Wiley, 2020-12-01) [Article]
    The management of bonefishes Albula spp. has been hindered by unresolved species distributions and a general lack of life history information. We provide the first genetic species identifications of Albula spp. from the northern Indian Ocean. The roundjaw bonefish Albula glossodonta was documented in the Red Sea, and the smallscale bonefish A. oligolepis was identified in the Gulf of Aden with no evidence supporting sympatry. Estimates of genetic differentiation indicate three closely related lineages in A. glossodonta in the Red Sea, Indian Ocean, and Pacific Ocean (Red Sea-Pacific Ocean, F$_{st}$ =0.295; Red Sea-Seychelles, F$_{st}$ =0.193; Pacific Ocean-Seychelles, F$_{st}$ =0.141). Additionally, we provide the first life history information from Albula spp. in the Indian Ocean. Aged-based growth models of A. glossodonta from the Red Sea demonstrated statistically significant differences compared to previously published data from the Pacific Ocean. Spawning activity during winter months was derived from gonadosomatic index values of A. glossodonta from the Red Sea and corresponded with spawning seasonality previously documented for the species in the Pacific Ocean. The results of this study aid in refining biogeographical uncertainties of Albula spp. and illustrate the importance of collecting regional growth information for subsequent management of A. glossodonta. This article is protected by copyright. All rights reserved.
  • Large deep-sea zooplankton biomass mirrors primary production in the global ocean

    Hernández-León, S.; Koppelmann, R.; Fraile-Nuez, E.; Bode, Antonio; Mompeán, C.; Irigoien, X.; Olivar, M. P.; Echevarría, Fidel; Fernández de Puelles, M. L.; González-Gordillo, J. Ignacio; Cózar, A.; Acuña, J. L.; Agusti, Susana; Duarte, Carlos M. (Nature Communications, Springer Science and Business Media LLC, 2020-11-27) [Article]
    AbstractThe biological pump transports organic carbon produced by photosynthesis to the meso- and bathypelagic zones, the latter removing carbon from exchanging with the atmosphere over centennial time scales. Organisms living in both zones are supported by a passive flux of particles, and carbon transported to the deep-sea through vertical zooplankton migrations. Here we report globally-coherent positive relationships between zooplankton biomass in the epi-, meso-, and bathypelagic layers and average net primary production (NPP). We do so based on a global assessment of available deep-sea zooplankton biomass data and large-scale estimates of average NPP. The relationships obtained imply that increased NPP leads to enhanced transference of organic carbon to the deep ocean. Estimated remineralization from respiration rates by deep-sea zooplankton requires a minimum supply of 0.44 Pg C y$^{−1}$ transported into the bathypelagic ocean, comparable to the passive carbon sequestration. We suggest that the global coupling between NPP and bathypelagic zooplankton biomass must be also supported by an active transport mechanism associated to vertical zooplankton migration.
  • Carlgren’s hesitation allayed: redescription and systematics of Heteranthus verruculatus Klunzinger, 1877 (Cnidaria, Actiniaria), with a redefinition of Heteranthidae Carlgren, 1900

    Yap, Nicholas Wei Liang; Quek, Zheng Bin Randolph; Tan, Ria; Nugroho, Dharma Arif; Lee, Jen Nie; Berumen, Michael L.; Tan, Koh Siang; Huang, Danwei (Contributions to Zoology, Brill, 2020-11-27) [Article]
    Species boundaries delineating tropical sea anemones (Cnidaria, Actiniaria) of the zooxanthellate genus, Heteranthus Klunzinger, 1877, are unclear. There are currently two valid Heteranthus species: type species Heteranthus verruculatus Klunzinger, 1877, first reported from Koseir, Egypt, and H. insignis Carlgren, 1943, from Poulo Condore, Vietnam. In describing the latter from a single, poorly preserved specimen, zoologist Oskar Carlgren expressed apprehension with traits he had used to establish this species. Carlgren’s doubts persisted later in writing when he found a similar-looking sea anemone from the Great Barrier Reef. Crucial details to positively identify either species have since remained limited. Here, we re-diagnosed Heteranthus and re-described its type species based on observations of specimens we have obtained from Singapore and Pulau Ambon (Indonesia), and of museum material collected elsewhere across the Indo-West Pacific region (n > 180). Supported by molecular phylogenetic evidence, the family Heteranthidae Carlgren, 1900 was reinstated and re-diagnosed. Heteranthus verruculatus is encountered in the lower intertidal region amongst seagrass, in rocky crevices, or coral rubble. It occurs as solitary individuals or in clonal clusters, well-camouflaged against the substratum. Individuals were observed to frequently propagate by longitudinal fission, resulting in a varied appearance. Type material of H. verruculatus and H. insignis were re-examined and as we found no differences between them, the two were synonymised. We inferred that Carlgren probably misinterpreted cnidae and histological data in defining H. insignis as a distinct species. This revision clarifies the taxonomy and geographic range of H. verruculatus, an Indo-West Pacific species that is found from the Red Sea to subtropical Australia and Hawaii.
  • Century-long records reveal shifting challenges to seagrass recovery

    Krause-Jensen, Dorte; Duarte, Carlos M.; Sand-Jensen, Kaj; Carstensen, Jacob (Global Change Biology, Wiley, 2020-11-25) [Article]
    Global losses over the 20th century placed seagrass ecosystems among the most threatened ecosystems in the world, with eutrophication, and associated deterioration of the submarine light environment identified as the main driver. Growing appreciation of the ecological and societal benefits of healthy seagrass meadows has stimulated efforts to protect and restore them, largely focused on reducing nutrient input to coastal waters. Here we analyze a unique data set spanning 135 years on eelgrass (Zostera marina), the dominant seagrass of the northern hemisphere. We show that meadows in the Western Baltic Sea exhibited major declines relative to historic (1890-1910) reference due to the wasting disease in the 1930s followed by eutrophication peaking in the 1980s, but have only shown modest improvement despite major eutrophication mitigation, halving nitrogen input since the 1980s. Across the past century, we identified generally shallower colonization depths of eelgrass for a given submarine light penetration and, hence, increased apparent light requirements. This suggests that eelgrass recovery is limited by additional stressors. Our study indicates that bottom trawling and intense recent warming (0.5°C per decade, 1985-2018), which impact on deeper and shallower meadows, respectively, suppress eelgrass from fully recovering from eutrophication. Warming is most severe in shallow turbid waters, while clear-water areas offer eelgrass refugia from warming in deeper, cooler waters; but trawling can prevent eelgrass from reaching these refugia. Efforts to reduce nutrient input and thereby improve water clarity have been instrumental in avoiding a catastrophic loss of eelgrass ecosystems. However, local-scale future management must, in addition, reduce bottom trawling to facilitate eelgrass reaching deeper, cooler refugia, and increase resilience toward realized and further warming. Warming needs to be limited by meeting global climate change mitigation goals.
  • Salinity-Conveyed Thermotolerance in the Coral Model Aiptasia Is Accompanied by Distinct Changes of the Bacterial Microbiome

    Randle, Janna L.; Cardenas, Anny; Gegner, Hagen; Ziegler, Maren; Voolstra, Christian R. (Frontiers in Marine Science, Frontiers Media SA, 2020-11-25) [Article]
    Coral bleaching, i.e., the loss of photosynthetic algal endosymbionts, caused by ocean warming is now among the main factors driving global reef decline, making the elucidation of factors that contribute to thermotolerance important. Recent studies implicate high salinity as a contributing factor in cnidarians, potentially explaining the high thermotolerance of corals from the Arabian Seas. Here we characterized bacterial community composition under heat stress at different salinities using the coral model Aiptasia. Exposure of two Aiptasia host-algal symbiont pairings (H2-SSB01 and CC7-SSA01) to ambient (25°C) and heat stress (34°C) temperatures at low (36 PSU), intermediate (39 PSU), and high (42 PSU) salinities showed that bacterial community composition at high salinity was significantly different, concomitant with reduced bleaching susceptibility in H2-SSB01, not observed in CC7-SSA01. Elucidation of bacteria that showed increased relative abundance at high salinity, irrespective of heat stress, revealed candidate taxa that could potentially contribute to the observed increased thermotolerance. We identified 4 (H2-SSB01) and 3 (CC7-SSA01) bacterial taxa belonging to the orders Alteromonadales (1 OTU), Oligoflexales (1 OTU), Rhizobiales (2 OTUs), and Rhodobacterales (2 OTUs), suggesting that only few bacterial taxa are potential contributors to an increase in thermal tolerance at high salinities. These taxa have previously been implicated in nitrogen and DMSP cycling, processes that are considered to affect thermotolerance. Our study demonstrates microbiome restructuring in symbiotic cnidarians under heat stress at different salinities. As such, it underlines how host-associated bacterial communities adapt to prevailing environmental conditions with putative consequences for the environmental stress tolerance of the emergent metaorganism.
  • Source Apportionment and Elemental Composition of Atmospheric Total Suspended Particulates (TSP) Over the Red Sea Coast of Saudi Arabia

    Cusack, Michael; Arrieta, J. M.; Duarte, Carlos M. (Earth Systems and Environment, Springer Science and Business Media LLC, 2020-11-24) [Article]
    AbstractThis work presents a comprehensive study on concentrations and elemental composition of total suspended atmospheric particulates for a semi-urban site on the Red Sea coast, and on-board a research vessel, which collected off-shore samples along the Red Sea. We conducted one of the most extended measurement campaigns of atmospheric particulates ever for the region, with continuous measurements over 27 months. The overall mean concentrations (± st. dev.) of TSP were 125 ± 197 µg m$^{−3}$ for the permanent semi-urban site, and 108 ± 193 µg m$^{−3}$ for the off-shore mobile site. The region is frequently severely impacted by both localised and widespread dust storms, which on occasion, can increase atmospheric particulate concentrations to levels above mg m$^{−3}$ (> 1000 µg m$^{−3}$). Median concentrations were not as variable between seasons, indicating a stable, permanent presence of atmospheric particulates independent of the time of year. The primary chemical elements contributing to particulate mass were Na, Ca, S, Al and Fe. We employed Positive Matrix Factorisation (EPA PMF v5.0.14) to identify different major sources of particulates, which were crustal, marine, fuel oil combustion/secondary sulphate and mixed anthropogenic. The crustal source was characterised by tracers Al, Fe, K, Mg and Sn, and was present to some extent in the other identified sources due to the permanent presence of dust particles in the atmosphere. The fuel oil combustion/secondary sulphate source was identifiable by the almost exclusive presence of S, and to a lesser extent V, emitted from oil combustion as primary emissions and also secondary sulphate formation following the release of S to the atmosphere. A mixed anthropogenic source was characterised by Zn, Ni, Cr, Cu and Pb, emitted from traffic, industry, power generation and water desalination. This study highlights that the natural sources of particulates in this desert region give rise to frequent episodes of extremely poor air quality, and this problem is compounded by significant emissions of anthropogenic pollution, which has an impact across the entire Red Sea basin. Further stringent measures should be adopted to improve air quality across the region and prevent long-term damage to the health of the local population and ecosystems.
  • Composition, uniqueness and connectivity across tropical coastal lagoon habitats in the Red Sea.

    Alsaffar, Zahra Hassan Ali; Curdia, Joao; Irigoien, Xabier; Carvalho, Susana (BMC ecology, Springer Science and Business Media LLC, 2020-11-23) [Article]
    BACKGROUND:Tropical habitats and their associated environmental characteristics play a critical role in shaping macroinvertebrate communities. Assessing patterns of diversity over space and time and investigating the factors that control and generate those patterns is critical for conservation efforts. However, these factors are still poorly understood in sub-tropical and tropical regions. The present study applied a combination of uni- and multivariate techniques to test whether patterns of biodiversity, composition, and structure of macrobenthic assemblages change across different lagoon habitats (two mangrove sites; two seagrass meadows with varying levels of vegetation cover; and an unvegetated subtidal area) and between seasons and years. RESULTS:In total, 4771 invertebrates were identified belonging to 272 operational taxonomic units (OTUs). We observed that macrobenthic lagoon assemblages are diverse, heterogeneous and that the most evident biological pattern was spatial rather than temporal. To investigate whether macrofaunal patterns within the lagoon habitats (mangrove, seagrass, unvegetated area) changed through the time, we analysed each habitat separately. The results showed high seasonal and inter-annual variability in the macrofaunal patterns. However, the seagrass beds that are characterized by variable vegetation cover, through time, showed comparatively higher stability (with the lowest values of inter-annual variability and a high number of resident taxa). These results support the theory that seagrass habitat complexity promotes diversity and density of macrobenthic assemblages. Despite the structural and functional importance of seagrass beds documented in this study, the results also highlighted the small-scale heterogeneity of tropical habitats that may serve as biodiversity repositories. CONCLUSIONS:Comprehensive approaches at the "seascape" level are required for improved ecosystem management and to maintain connectivity patterns amongst habitats. This is particularly true along the Saudi Arabian coast of the Red Sea, which is currently experiencing rapid coastal development. Also, considering the high temporal variability (seasonal and inter-annual) of tropical shallow-water habitats, monitoring and management plans must include temporal scales.
  • Host-association as major driver of microbiome structure and composition in Red Sea seagrass ecosystems

    Garcias-Bonet, Neus; Eguíluz, V. M.; Díaz-Rúa, Rubén; Duarte, Carlos M. (Environmental Microbiology, Wiley, 2020-11-22) [Article]
    The role of the microbiome in sustaining seagrasses has recently been highlighted. However, our understanding of the seagrass microbiome lacks behind that of other organisms. Here, we analyze the endophytic and total bacterial communities of leaves, rhizomes, and roots of six Red Sea seagrass species and their sediments. The structure of seagrass bacterial communities revealed that the 1% most abundant OTUs accounted for 87.9 and 74.8 % of the total numbers of reads in sediment and plant tissue samples, respectively. We found taxonomically distinct bacterial communities in vegetated and bare sediments. Yet, our results suggest that lifestyle (i.e. free-living or host-association) is the main driver of bacterial community composition. Seagrass bacterial communities were tissue- and species-specific and differed from those of surrounding sediments. We identified OTUs belonging to genera related to N and S cycles in roots, and members of Actinobacteria, Bacteroidetes, and Firmicutes phyla as particularly enriched in root endosphere. The finding of highly similar OTUs in well-defined sub-clusters by network analysis suggests the co-occurrence of highly connected key members within Red Sea seagrass bacterial communities. These results provide key information towards the understanding of the role of microorganisms in seagrass ecosystem functioning framed under the seagrass holobiont concept.

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