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Recent Submissions

  • Translational Molecular Ecology in practice: Linking DNA-based methods to actionable marine environmental management

    Aylagas, Eva; Aylagas, Eva; Pochon, Xavier; Zaiko, Anastasija; Keeley, Nigel; Bruce, Kat; Hong, Pei-Ying; Ruiz, Gregory M.; Stein, Eric D.; Theroux, Susanna; Geraldi, Nathan; Ortega, Alejandra; Gajdzik, Laura; Coker, Darren James; Katan, Yasser; Hikmawan, Tyas; Saleem, Ammar; Alamer, Sultan; Jones, Burton; Duarte, Carlos M.; Pearman, John; Carvalho, Susana (Science of The Total Environment, Elsevier BV, 2020-07-12) [Article]
    Molecular-based approaches can provide timely biodiversity assessments, showing an immense potential to facilitate decision-making in marine environmental management. However, the uptake of molecular data into environmental policy remains minimal. Here, we showcase a selection of local to global scale studies applying molecular-based methodologies for environmental management at various stages of implementation. Drawing upon lessons learned from these case-studies, we provide a roadmap to facilitate applications of DNA-based methods to marine policies and to overcome the existing challenges. The main impediment identified is the need for standardized protocols to guarantee data comparison across spatial and temporal scales. Adoption of Translational Molecular Ecology – the sustained collaboration between molecular ecologists and stakeholders, will enhance consensus with regards to the objectives, methods, and outcomes of environmental management projects. Establishing a sustained dialogue among stakeholders is the key to accelerating the adoption of molecular-based approaches for marine monitoring and assessment.
  • Natal philopatry increases relatedness within groups of coral reef cardinalfish

    Rueger, Theresa; Harrison, Hugo B.; Buston, Peter M.; Gardiner, Naomi M.; Berumen, Michael L.; Jones, G. P. (Proceedings of the Royal Society B: Biological Sciences, The Royal Society, 2020-07-08) [Article]
    A central issue in evolutionary ecology is how patterns of dispersal influence patterns of relatedness in populations. In terrestrial organisms, limited dispersal of offspring leads to groups of related individuals. By contrast, for most marine organisms, larval dispersal in open waters is thought to minimize kin associations within populations. However, recent molecular evidence and theoretical approaches have shown that limited dispersal, sibling cohesion and/or differential reproductive success can lead to kin association and elevated relatedness. Here, we tested the hypothesis that limited dispersal explains small-scale patterns of relatedness in the pajama cardinalfish Sphaeramia nematoptera. We used 19 microsatellite markers to assess parentage of 233 juveniles and pairwise relatedness among 527 individuals from 41 groups in Kimbe Bay, Papua New Guinea. Our findings support three predictions of the limited dispersal hypothesis: (i) elevated relatedness within groups, compared with among groups and elevated relatedness within reefs compared with among reefs; (ii) a weak negative correlation of relatedness with distance; (iii) more juveniles than would be expected by chance in the same group and the same reef as their parents. We provide the first example for natal philopatry at the group level causing small-scale patterns of genetic relatedness in a marine fish.
  • Seagrass losses since mid-20th century fuelled CO 2 emissions from soil carbon stocks

    Salinas, Cristian; Duarte, Carlos M.; Lavery, P. S.; Masqué, Pere; Arias-Ortiz, Ariane; Leon, Javier X.; Callaghan, David; Kendrick, G. A.; Serrano, Oscar (Global Change Biology, Wiley, 2020-07-07) [Article]
    Seagrass meadows store globally significant organic carbon (Corg) stocks which, if disturbed, can lead to CO2 emissions, contributing to climate change. Eutrophication and thermal stress continue to be a major cause of seagrass decline worldwide, but the associated CO2 emissions remain poorly understood. This study presents comprehensive estimates of seagrass soil Corg erosion following eutrophication-driven seagrass loss in Cockburn Sound (23 km2 between 1960s and 1990s) and identifies the main drivers. We estimate that shallow seagrass meadows (<5 m depth) had significantly higher Corg stocks in 50 cm thick soils (4.5 ± 0.7 kg Corg/m2) than previously vegetated counterparts (0.5 ± 0.1 kg Corg/m2). In deeper areas (>5 m), however, soil Corg stocks in seagrass and bare but previously vegetated areas were not significantly different (2.6 ± 0.3 and 3.0 ± 0.6 kg Corg/m2, respectively). The soil Corg sequestration capacity prevailed in shallow and deep vegetated areas (55 ± 11 and 21 ± 7 g Corg m−2 year−1, respectively), but was lost in bare areas. We identified that seagrass canopy loss alone does not necessarily drive changes in soil Corg but, when combined with high hydrodynamic energy, significant erosion occurred. Our estimates point at ~0.20 m/s as the critical shear velocity threshold causing soil Corg erosion. We estimate, from field studies and satellite imagery, that soil Corg erosion (within the top 50 cm) following seagrass loss likely resulted in cumulative emissions of 0.06–0.14 Tg CO2-eq over the last 40 years in Cockburn Sound. We estimated that indirect impacts (i.e. eutrophication, thermal stress and light stress) causing the loss of ~161,150 ha of seagrasses in Australia, likely resulted in the release of 11–21 Tg CO2-eq since the 1950s, increasing cumulative CO2 emissions from land-use change in Australia by 1.1%–2.3% per annum. The patterns described serve as a baseline to estimate potential CO2 emissions following disturbance of seagrass meadows.
  • Unfamiliar partnerships limit cnidarian holobiont acclimation to warming

    Herrera Sarrias, Marcela; Klein, Shannon; Schmidt-Roach, Sebastian; Campana, Sara; Cziesielski, Maha Joana; Chen, Jit Ern; Duarte, Carlos M.; Aranda, Manuel (Global Change Biology, Wiley, 2020-07-06) [Article]
    Enhancing the resilience of corals to rising temperatures is now a matter of urgency, leading to growing efforts to explore the use of heat tolerant symbiont species to improve their thermal resilience. The notion that adaptive traits can be retained by transferring the symbionts alone, however, challenges the holobiont concept, a fundamental paradigm in coral research. Holobiont traits are products of a specific community (holobiont) and all its co-evolutionary and local adaptations, which might limit the retention or transference of holobiont traits by exchanging only one partner. Here, we evaluate how interchanging partners affect the short- and long-term performance of holobionts under heat stress using clonal lineages of the cnidarian model system Aiptasia (host and Symbiodiniaceae strains) originating from distinct thermal environments. Our results show that holobionts from more thermally variable environments have higher plasticity to heat stress, but this resilience could not be transferred to other host genotypes through the exchange of symbionts. Importantly, our findings highlight the role of the host in determining holobiont productivity in response to thermal stress and indicate that local adaptations of holobionts will likely limit the efficacy of interchanging unfamiliar compartments to enhance thermal tolerance.
  • High rates of carbon and dinitrogen fixation suggest a critical role of benthic pioneer communities in the energy and nutrient dynamics of coral reefs

    Roth, Florian; Karcher, Denis B.; Rädecker, Nils; Hohn, Sönke; Carvalho, Susana; Thomson, Timothy; Saalmann, Franziska; Voolstra, Christian R.; Kürten, Benjamin; Struck, Ulrich; Jones, Burton; Wild, Christian (Functional Ecology, Wiley, 2020-07-02) [Article]
    1. Following coral mortality in tropical reefs, pioneer communities dominated by filamentous and crustose algae efficiently colonize substrates previously occupied by coral tissue. This phenomenon is particularly common after mass coral mortality following prolonged bleaching events associated with marine heatwaves. 2. Pioneer communities play an important role for the biological succession and reorganization of reefs after disturbance. However, their significance for critical ecosystem functions previously mediated by corals, such as the efficient cycling of carbon (C) and nitrogen (N) within the reef, remains uncertain. 3. We used 96 carbonate tiles to simulate the occurrence of bare substrates after disturbance in a coral reef of the central Red Sea. We measured rates of C and dinitrogen (N2) fixation of pioneer communities on these tiles monthly over an entire year. Coupled with elemental and stable isotope analyses, these measurements provide insights into macronutrient acquisition, export, and the influence of seasonality. 4. Pioneer communities exhibited high rates of C and N2 fixation within 4 – 8 weeks after the introduction of experimental bare substrates. Ranging from 13 to 25 μmol C cm−2 d−1 and 8 to 54 nmol N cm−2 d−1, respectively, C and N2 fixation rates were comparable to reported values for established Red Sea coral reefs. This similarity indicates that pioneer communities may quickly compensate for the loss of benthic productivity by corals. Notably, between 40 and 85% of fixed organic C was exported into the environment, constituting a vital source of energy for the coral reef food web. 5. Our findings suggest that benthic pioneer communities may play a crucial, yet overlooked role in the C and N dynamics of oligotrophic coral reefs by contributing to the input of new C and N after coral mortality. While not substituting other critical ecosystem functions provided by corals (e.g. structural habitat complexity and coastal protection), pioneer communities likely contribute to maintaining coral reef nutrient cycling through the accumulation of biomass and import of macronutrients following coral loss.
  • Cell-by-cell estimation of PAH sorption and subsequent toxicity in marine phytoplankton

    Kottuparambil, Sreejith; Agusti, Susana (Chemosphere, Elsevier BV, 2020-07-01) [Article]
    Polycyclic Aromatic Hydrocarbons (PAHs) have elicited increasing concern due to their ubiquitous occurrence in coastal marine environments and resultant toxicity in organisms. Due to their lipophilic nature, PAHs tend to accumulate in phytoplankton cells and thus subsequently transfer to other compartments of the marine ecosystem. The intrinsic fluorescence properties of PAHs in the ultraviolet (UV)/blue spectral range have recently been exploited to investigate their uptake modes, localization, and aggregation in various biological tissues. Here, we quantitatively evaluate the sorption of two model PAHs (phenanthrene and pyrene) in three marine phytoplankton species (Chaetoceros tenuissimus, Thalassiosira sp. and Proteomonas sp.) using a combined approach of UV excitation flow cytometry and fluorescence microscopy. Over a 48-h exposure to a gradient of PAHs, Thalassiosira sp. showed the highest proportion of PAH-sorbed cells (29% and 97% of total abundance for phenanthrene and pyrene, respectively), which may be attributed to its relatively high total lipid content (33.87 percent dry weight). Moreover, cell-specific pulse amplitude modulation (PAM) microscope fluorometry revealed that PAH sorption significantly reduced the photosynthetic quantum efficiency (Fv/Fm) of individual phytoplankton cells. We describe a rapid and precise hybrid method for the detection of sorption of PAHs on phytoplankton cells. Our results emphasize the ecologically relevant sub-lethal effects of PAHs in phytoplankton at the cellular level, even at concentrations where no growth inhibition was apparent. This work is the first study to address the cell-specific impacts of fluorescent toxicants in a more relevant toxicant-sorbed subpopulation; these cell-specific impacts have to date been unidentified in traditional population-based phytoplankton toxicity assays.
  • 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. (Wiley, 2020-06-28) [Preprint]
    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, offer some respite to certain reefs. The Farasan Banks in the southern Red Sea is home to hundreds of coral reefs covering 16,000 km 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, our study sheds light on the broad 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.
  • Additive impacts of deoxygenation and acidification threaten marine biota.

    Steckbauer, Alexandra; Klein, Shannon; Duarte, Carlos M. (Global change biology, Wiley, 2020-06-26) [Article]
    Deoxygenation in coastal and open-ocean ecosystems rarely exists in isolation but occurs concomitantly with acidification. Here, we first combine meta-data of experimental assessments from across the globe to investigate the potential interactive impacts of deoxygenation and acidification on a broad range of marine taxa. We then characterize the differing degrees of deoxygenation and acidification tested in our dataset using a ratio between the partial pressure of oxygen and carbon dioxide (pO2 /pCO2 ) to assess how biological processes change under an extensive, yet diverse range of pO2 and pCO2 conditions. The dataset comprised 375 experimental comparisons and revealed predominantly additive but variable effects (91.7%-additive, 6.0%-synergistic, 2.3%-antagonistic) of the dual stressors, yielding negative impacts across almost all responses examined. Our data indicates that the pO2 /pCO2 -ratio offers a simplified metric to characterize the extremity of the concurrent stressors and shows that more severe impacts occurred when ratios represented more extreme deoxygenation and acidification conditions. Importantly, our analysis highlights the need to assess the concurrent impacts of deoxygenation and acidification on marine taxa and that assessments considering the impact of O2 depletion alone will likely underestimate the impacts of deoxygenation events and their ecosystem-wide consequences.
  • Giant clams in shallow reefs: UV-resistance mechanisms of Tridacninae in the Red Sea

    Rossbach, Susann; Overmans, Sebastian; Kaidarova, Altynay; Kosel, Jürgen; Agusti, Susana; Duarte, Carlos M. (Coral Reefs, Springer Science and Business Media LLC, 2020-06-22) [Article]
    The photosymbiosis of tropical giant clams (subfamily Tridacninae) with unicellular algae (Symbiodiniaceae) restricts their distribution to the sunlit, shallow waters of the euphotic zone where organisms are additionally exposed to potentially damaging levels of solar UV radiation. Metabolic and physiological responses of Red Sea Tridacna maxima clams, including net calcification and primary production, as well as valvometry (i.e., shell gaping behavior) were assessed when exposed to simulated high radiation levels received at 3 and 5 m underwater. The two levels of radiation included exposure treatments to photosynthetically active radiation (PAR; 400–700 nm) alone and to both, PAR and ultraviolet-B radiation (UV-B;280–315 nm). The valvometry data obtained using flexible magnetic sensors indicated that specimens under PAR ? UV-B exposure significantly reduced the proportion of their exposed mantle area, a potential photo-protective mechanism which, however, reduces the overall amount of PAR received by the algal symbionts. Consequently, specimens under PAR ? UV-B displayed a slight, although non-significant, reduction in primary production rates but no signs of additional oxidative stress, changes in symbiont densities, chlorophyll content, or levels of mycosporine-like amino acids. Net calcification rates of T.maxima were not affected by exposure to UV-B; however, calcification was positively correlated with incident PAR levels. UV-B exposure changes the valvometry, reducing the exposed mantle area which consequently diminishes the available PAR for the photosymbionts. Still, T. maxima maintains high rates of primary production and net calcification, even under high levels of UV-B. This provides experimental support for a recently described, effective UV-defensive mechanism in Tridacninae, in which the photonic cooperation of the associated algal symbionts and giant clam iridocytes is assumed to establish optimal conditions for the photosynthetic performance of the clams’ symbionts.
  • COVID-19 lockdown allows researchers to quantify the effects of human activity on wildlife

    Rutz, Christian; Loretto, Matthias-Claudio; Bates, Amanda E.; Davidson, Sarah C.; Duarte, Carlos M.; Jetz, Walter; Johnson, Mark; Kato, Akiko; Kays, Roland; Mueller, Thomas; Primack, Richard B.; Ropert-Coudert, Yan; Tucker, Marlee A.; Wikelski, Martin; Cagnacci, Francesca (Nature Ecology & Evolution, Springer Science and Business Media LLC, 2020-06-22) [Article]
    We noticed that people started referring to the lockdown period as the ‘Great Pause’, but felt that a more precise term would be helpful. We propose ‘anthropause’ to refer specifcally to a considerable global slowing of modern human activities, notably travel. We are aware that the correct prefx is ‘anthropo-’ (for ‘human’) but opted for the shortened form, which is easier to remember and use, and where the missing ‘po’ is still echoed in the pronunciation of ‘pause’ (pɔːz).
  • Standardized short-term acute heat stress assays resolve historical differences in coral thermotolerance across microhabitat reef sites

    Voolstra, Christian R.; Buitrago-López, Carol; Perna, Gabriela; Cardenas, Anny; Hume, Benjamin; Rädecker, Nils; Barshis, Daniel J. (Global Change Biology, Wiley, 2020-06-22) [Article]
    Coral bleaching is one of the main drivers of reef degradation. Most corals bleach and suffer mortality at just 1–2°C above their maximum monthly mean temperatures, but some species and genotypes resist or recover better than others. Here, we conducted a series of 18-hr short-term acute heat stress assays side-by-side with a 21-day long-term heat stress experiment to assess the ability of both approaches to resolve coral thermotolerance differences reflective of in situ reef temperature thresholds. Using a suite of physiological parameters (photosynthetic efficiency, coral whitening, chlorophyll a , host protein, algal symbiont counts, and algal type association), we assessed bleaching susceptibility of Stylophora pistillata colonies from the windward/exposed and leeward/protected sites of a nearshore coral reef in the central Red Sea, which had previously shown differential mortality during a natural bleaching event. Photosynthetic efficiency was most indicative of the expected higher thermal tolerance in corals from the protected reef site, denoted by an increased retention of dark-adapted maximum quantum yields at higher temperatures. These differences were resolved using both experimental setups, as corroborated by a positive linear relationship, not observed for the other parameters. Notably, short-term acute heat stress assays resolved per-colony (genotype) differences that may have been masked by acclimation effects in the long-term experiment. Using our newly developed portable experimental system termed the Coral Bleaching Automated Stress System (CBASS), we thus highlight the potential of mobile, standardized short-term acute heat stress assays to resolve fine-scale differences in coral thermotolerance. Accordingly, such a system may be suitable for large-scale determination and complement existing approaches to identify resilient genotypes/reefs for downstream experimental examination and prioritization of reef sites for conservation/restoration. Development of such a framework is consistent with the recommendations of the National Academy of Sciences and the Reef Restoration and Adaptation Program committees for new intervention and restoration strategies.
  • Cryptic species and host specificity in the bryozoan-associated hydrozoan Zanclea divergens (Hydrozoa, Zancleidae).

    Maggioni, Davide; Schiavo, Andrea; Ostrovsky, Andrew N; Seveso, Davide; Galli, Paolo; Arrigoni, Roberto; Berumen, Michael L.; Benzoni, Francesca; Montano, Simone (Molecular phylogenetics and evolution, Elsevier BV, 2020-06-21) [Article]
    Zanclea divergens is a tropical hydrozoan living in symbiotic association with bryozoans and currently reported from Papua New Guinea, Indonesia, and Maldives. Here, we used an integrative approach to assess the morpho-molecular diversity of the species across the Indo-Pacific. Phylogenetic and species delimitation analyses based on seven mitochondrial and nuclear loci revealed four well-supported molecular lineages corresponding to cryptic species, and representing a Pacific clade, an Indian clade, and two Red Sea clades. Since the general polyp morphology was almost identical in all samples, the nematocyst capsules were measured and analysed to search for possible fine-scale differences, and their statistical treatment revealed a significant difference in terms of length and width among the clades investigated. All Zanclea divergens specimens were specifically associated with cheilostome bryozoans belonging to the genus Celleporaria. The Pacific and Indian clades were associated with Celleporaria sp. and C. vermiformis, respectively, whereas both Red Sea lineages were associated with C. pigmentaria. Nevertheless, the sequencing of host bryozoans revealed that one of the Red Sea hydrozoan clades is associated with two morphologically undistinguishable, but genetically divergent, bryozoan species. Overall, our results show that Z. divergens is a species complex composed of morphologically cryptic lineages showing partially disjunct distributions and host specificity. The presence of two sympatric lineages living on the same host species reveal complex dynamics of diversification, and future research aimed at understanding their diversification process will likely improve our knowledge on the mechanisms of speciation among currently sympatric cryptic species.
  • Robustness to extinction and plasticity derived from mutualistic bipartite ecological networks.

    Sheykhali, Somaye; Fernández-Gracia, Juan; Traveset, Anna; Ziegler, Maren; Voolstra, Christian R; Duarte, Carlos M.; Eguíluz, Víctor M (Scientific reports, Springer Science and Business Media LLC, 2020-06-20) [Article]
    Understanding the response of ecological networks to perturbations and disruptive events is needed to anticipate the biodiversity loss and extinction cascades. Here, we study how network plasticity reshapes the topology of mutualistic networks in response to species loss. We analyze more than one hundred empirical mutualistic networks and considered random and targeted removal as mechanisms of species extinction. Network plasticity is modeled as either random rewiring, as the most parsimonious approach, or resource affinity-driven rewiring, as a proxy for encoding the phylogenetic similarity and functional redundancy among species. This redundancy should be positively correlated with the robustness of an ecosystem, as functions can be taken by other species once one of them is extinct. We show that effective modularity, i.e. the ability of an ecosystem to adapt or restructure, increases with increasing numbers of extinctions, and with decreasing the replacement probability. Importantly, modularity is mostly affected by the extinction rather than by rewiring mechanisms. These changes in community structure are reflected in the robustness and stability due to their positive correlation with modularity. Resource affinity-driven rewiring offers an increase of modularity, robustness, and stability which could be an evolutionary favored mechanism to prevent a cascade of co-extinctions.
  • Low Symbiodiniaceae diversity in a turbid marginal reef environment

    Smith, E. G.; Gurskaya, A.; Hume, Benjamin; Voolstra, Christian R.; Todd, P. A.; Bauman, Andrew G.; Burt, John A. (Coral Reefs, Springer Science and Business Media LLC, 2020-06-19) [Article]
    The coastal waters of Singapore support coral reefs that are biodiverse but characterized by high turbidity and sedimentation. Here, we used internal transcribed spacer two (ITS2) amplicon sequencing to investigate the Symbiodiniaceae communities associated with this marginal reef system, as turbid reefs may serve as potential refugia from future thermal stress. Using the analytical framework SymPortal, we identified a predominance of Cladocopium among the five coral species studied across six reef sites. Durusdinium was present in comparatively lower abundances and was composed of multiple Durusdinium trenchii strains. In contrast to other marginal environments, the Cladocopium communities exhibited low diversity and lacked the host-specificity of strains reported elsewhere. Nevertheless, we identified a site-specific strain across three species, which was supported by sequencing of the non-coding region of the psbA minicircle (psbAncr). The overall low diversity of the symbiont communities suggests that, although Singapore’s reefs may provide habitat for a diverse coral assemblage, the strong selective pressure exerted by the prevalent turbidity likely limits the diversity of the associated symbiont community.
  • COVID-19 pandemic and associated lockdown as a "Global Human Confinement Experiment" to investigate biodiversity conservation.

    Bates, Amanda E; Primack, Richard B; Moraga, Paula; Duarte, Carlos M. (Biological conservation, Elsevier BV, 2020-06-19) [Article]
    Efforts to curtail the spread of the novel coronavirus (SARS-CoV2) have led to the unprecedented concurrent confinement of nearly two-thirds of the global population. The large human lockdown and its eventual relaxation can be viewed as a Global Human Confinement Experiment. This experiment is a unique opportunity to identify positive and negative effects of human presence and mobility on a range of natural systems, including wildlife, and protected areas, and to study processes regulating biodiversity and ecosystems. We encourage ecologists, environmental scientists, and resource managers to contribute their observations to efforts aiming to build comprehensive global understanding based on multiple data streams, including anecdotal observations, systematic assessments and quantitative monitoring. We argue that the collective power of combining diverse data will transcend the limited value of the individual data sets and produce unexpected insights. We can also consider the confinement experiment as a "stress test" to evaluate the strengths and weaknesses in the adequacy of existing networks to detect human impacts on natural systems. Doing so will provide evidence for the value of the conservation strategies that are presently in place, and create future networks, observatories and policies that are more adept in protecting biological diversity across the world.
  • Iridocytes Mediate Photonic Cooperation Between Giant Clams (Tridacninae) and Their Photosynthetic Symbionts

    Rossbach, Susann; Subedi, Ram Chandra; Ng, Tien Khee; Ooi, Boon S.; Duarte, Carlos M. (Frontiers in Marine Science, Frontiers Media SA, 2020-06-19) [Article]
    Iridocytes, containing multiple stacks of proteinaceous platelets and crystalized guanine, alternating with thin cytoplasm sheets, are specialized cells that act as multilayer nanoreflectors. Convergence evolution led to their arising across a broad range of organisms, including giant clams of the Tridacninae subfamily – the only sessile and photosymbiotic organism, among animals known to possess iridocytes. Through the interference of light with their nanoscale architecture, iridocytes generate “structural colors,” which are reported to serve different purposes, from intra-species communication to camouflage. In giant clams, iridocytes were previously reported to promote a lateral- and forward scattering of photosynthetically productive radiation (PAR) into the clam tissue, as well as the back reflection of non-productive wavelengths. Hence, they are assumed to promote an increased efficiency in the use of available solar energy, while simultaneously preventing photodamage of the algal symbionts. We report the use of guanine crystals within Tridacna maxima giant clam iridocytes as a basis for photonic cooperation between the bivalve host and their photosynthetic symbionts. Our results suggest that, in addition to the previously described scattering processes, iridocytes absorb potentially damaging UV radiation (UVR) and, through successive emission, emit light at longer wavelengths, which is then absorbed by the photosynthetic pigments of the algal symbionts. Consequently, both, host and algal symbionts are sheltered from (potentially) damaging UVR, while the available solar energy within the PAR spectrum increases, thereby potentially enhancing photosynthetic and calcification rates in this large bivalve. Further, our results suggest that this photonic cooperation could be responsible for the broad repertoire of colors that characterizes the highly diverse mantle patterns found in T. maxima.
  • No Place Like Home? High Residency and Predictable Seasonal Movement of Whale Sharks Off Tanzania

    Rohner, Christoph A.; Cochran, Jesse; Cagua, Edgar F.; Prebble, Clare E. M.; Venables, Stephanie K.; Berumen, Michael L.; Kuguru, Baraka L.; Rubens, Jason; Brunnschweiler, Juerg M.; Pierce, Simon J. (Frontiers in Marine Science, Frontiers Media SA, 2020-06-12) [Article]
    Highly mobile marine megafauna species, while widely distributed and frequently threatened, often aggregate in distinct localized habitats. Implementation of local management initiatives within these hotspots is more achievable than developing effective conservation strategies that encompass their entire distributions. Such measures have the potential for disproportionate population-level benefits but rely on a detailed understanding of spatiotemporal habitat use. To that end, we examined the residency and small-scale habitat use of 51 whale sharks (Rhincodon typus) over 5 years at an aggregation site in Tanzania using passive acoustic telemetry. Whale sharks were highly resident within and across years, with a combined maximum residency index of 0.39. Although fewer sharks were detected from March to September, residency was high throughout the year. Ancillary photographic-identification data showed that individual residency persisted before and after tag attachment. Kernel utilization distributions (KUD) and movement networks both revealed the same spatiotemporal pattern of habitat use, with a small core habitat (50% KUD area for all sharks combined = 12.99 km2) that predictably changed on a seasonal basis. Activity spaces did not differ with time of day, sex, or size of the sharks, indicating a population-level pattern driven by prey availability. The small and predictable core habitat area at this site means that site-based management options to reduce shark injuries and mortality from boat strike and fishing gear entanglement can be spatially targeted for maximum effectiveness and compliance by human users.
  • Diatom Modulation of Microbial Consortia Through Use of Two Unique Secondary Metabolites

    Shibl, Ahmed A.; Isaac, Ashley; Ochsenkühn, Michael A.; Cardenas, Anny; Fei, Cong; Behringer, Gregory; Arnoux, Marc; Drou, Nizar; Santos, Miraflor P.; Gunsalus, Kris C.; Voolstra, Christian R.; Amin, Shady A. (Cold Spring Harbor Laboratory, 2020-06-12) [Preprint]
    <jats:p>Unicellular eukaryotic phytoplankton, such as diatoms, rely on microbial communities for survival despite lacking specialized compartments to house microbiomes (e.g., animal gut). Microbial communities have been widely shown to benefit from diatom excretions that accumulate within the microenvironment surrounding phytoplankton cells, known as the phycosphere. However, mechanisms that enable diatoms and other unicellular eukaryotes to nurture specific microbiomes by fostering beneficial bacteria and repelling harmful ones are mostly unknown. We hypothesized that diatom exudates may attune microbial communities and employed an integrated multi-omics approach using the ubiquitous diatom Asterionellopsis glacialis to reveal how it modulates its naturally associated bacteria. We show that A. glacialis reprograms its transcriptional and metabolic profiles in response to bacteria to secrete a suite of central metabolites and two unusual secondary metabolites, rosmarinic acid and azelaic acid. While central metabolites are utilized by potential bacterial symbionts and opportunists alike, rosmarinic acid promotes attachment of beneficial bacteria to the diatom and simultaneously suppresses the attachment of opportunists. Similarly, azelaic acid enhances growth of beneficial bacteria, while simultaneously inhibiting growth of opportunistic ones. We further show that the bacterial response to azelaic acid is widespread in the world's oceans and taxonomically restricted to a handful of bacterial genera. Our results demonstrate the innate ability of an important unicellular eukaryotic group to modulate their microbial consortia, similar to higher eukaryotes, using unique secondary metabolites that regulate bacterial growth and behavior inversely in different bacterial populations.</jats:p>
  • Simultaneous Measurements of Dinitrogen Fixation and Denitrification Associated With Coral Reef Substrates: Advantages and Limitations of a Combined Acetylene Assay

    El-Khaled, Yusuf C.; Roth, Florian; Radecker, Nils; Kharbatia, Najeh M.; Jones, Burton; Voolstra, Christian R.; Wild, Christian (Frontiers in Marine Science, Frontiers Media SA, 2020-06-11) [Article]
    Nitrogen (N) cycling in coral reefs is of key importance for these oligotrophic ecosystems, but knowledge about its pathways is limited. While dinitrogen (N2) fixation is comparably well studied, the counteracting denitrification pathway is under-investigated, mainly because of expensive and relatively complex experimental techniques currently available. Here, we combined two established acetylene-based assays to one single setup to determine N2-fixation and denitrification performed by microbes associated with coral reef substrates/organisms simultaneously. Accumulating target gases (ethylene for N2-fixation, nitrous oxide for denitrification) were measured in gaseous headspace samples via gas chromatography. We measured N2-fixation and denitrification rates of two Red Sea coral reef substrates (filamentous turf algae, coral rubble), and demonstrated, for the first time, the co-occurrence of both N-cycling processes in both substrates. N2-fixation rates were up to eight times higher during the light compared to the dark, whereas denitrification rates during dark incubations were stimulated for turf algae and suppressed for coral rubble compared to light incubations. Our results highlight the importance of both substrates in fixing N, but their role in relieving N is potentially divergent. Absolute N2-fixation rates of the present study correspond with rates reported previously, even though likely underestimated due to an initial lag phase. Denitrification is also presumably underestimated due to incomplete nitrous oxide inhibition and/or substrate limitation. Besides these inherent limitations, we show that a relative comparison of N2-fixation and denitrification activity between functional groups is possible. Thus, our approach facilitates cost-efficient sample processing in studies interested in comparing relative rates of N2-fixation and denitrification.
  • Aqua-Fi: Delivering internet underwater using wireless optical networks

    Shihada, Basem; Amin, Osama; Bainbridge, Christopher; Jardak, Seifallah; Alkhazragi, Omar; Ng, Tien Khee; Ooi, Boon S.; Berumen, Michael L.; Alouini, Mohamed-Slim (IEEE Communications Magazine, Institute of Electrical and Electronics Engineers (IEEE), 2020-06-09) [Article]
    In this article, we demonstrate bringing the Internet to underwater environments by deploying a low power and compact underwater optical wireless system, called Aqua-Fi, to support today's Internet applications. Aqua-Fi uses an LED or laser to support bidirectional wide-range communication services with different requirements, low cost, and simple implementation. LEDs introduce robust short distance solutions with low power requirements. However, laser extends the communication distance and improves the transmission rate at the cost of higher power requirements. Throughout this work, we discuss the proposed Aqua-Fi system architecture, limitations, and solutions to improve data rates and deliver reliable communication links.

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