Expanding ocean protection and peace: a window for science diplomacy in the Gulf.

The ecological state of the Persian or Arabian Gulf (hereafter 'Gulf') is in sharp decline. Calls for comprehensive ecosystem-based management approaches and transboundary conservation have gone largely unanswered, despite mounting marine threats made worse by climate change. The region's long-standing political tensions add additional complexity, especially now as some Gulf countries will soon adopt ambitious goals to protect their marine environments as part of new global environmental commitments. The recent interest in global commitments comes at a time when diplomatic relations among all Gulf countries are improving. There is a window of opportunity for Gulf countries to meet global marine biodiversity conservation commitments, but only if scientists engage in peer-to-peer diplomacy to build trust, share knowledge and strategize marine conservation options across boundaries. The Gulf region needs more ocean diplomacy and coordination; just as critically, it needs actors at its science-policy interface to find better ways of adapting cooperative models to fit its unique marine environment, political context and culture. We propose a practical agenda for scientist-led diplomacy in the short term and lines of research from which to draw (e.g. co-production, knowledge exchange) to better design future science diplomacy practices and processes suited to the Gulf's setting.

Negative effects of a zoanthid competitor limit coral calcification more than ocean acidification.

Ocean acidification (OA) threatens the persistence of reef-building corals and the habitat they provide. While species-specific effects of OA on marine organisms could have cascading effects on ecological interactions like competition, few studies have identified how benthic reef competitors respond to OA. We explored how two common Caribbean competitors, branching Porites and a colonial zoanthid (Zoanthus), respond to the factorial combination of OA and competition. In the laboratory, we exposed corals, zoanthids and interacting corals and zoanthids to ambient (8.01 ± 0.03) and OA (7.68 ± 0.07) conditions for 60 days. The OA treatment had no measured effect on zoanthids or coral calcification but decreased Porites maximum PSII efficiency. Conversely, the competitive interaction significantly decreased Porites calcification but had minimal-to-no countereffects on the zoanthid. Although this interaction was not exacerbated by the 60-day OA exposure, environmental changes that enhance zoanthid performance could add to the dominance of zoanthids over corals. The lack of effects of OA on coral calcification indicates that near-term competitive interactions may have more immediate consequences for some corals than future global change scenarios. Disparate consequences of competition have implications for community structure and should be accounted for when evaluating local coral reef trajectories.

Brilliantia kiribatiensis, a new genus and species of Cladophorales (Chlorophyta) from the remote coral reefs of the Southern Line Islands, Pacific Ocean.

The marine green alga Brilliantia kiribatiensis gen. et sp. nov. is described from samples collected from the coral reefs of the Southern Line Islands, Republic of Kiribati, Pacific Ocean. Phylogenetic analysis of sequences of the large- and small-subunit rDNA and the rDNA internal transcribed spacer region revealed that Brilliantia is a member of the Boodleaceae (Cladophorales), containing the genera Apjohnia, Boodlea, Cladophoropsis, Chamaedoris, Phyllodictyon, and Struvea. Within this clade it formed a distinct lineage, sister to Struvea elegans, but more distantly related to the bona fide Struvea species (including the type S. plumosa). Brilliantia differs from the other genera by having a very simple architecture forming upright, unbranched, single-celled filaments attached to the substratum by a rhizoidal mat. Cell division occurs by segregative cell division only at the onset of reproduction. Based on current sample collection, B. kiribatiensis seems to be largely restricted to the Southern Line Islands, although it was also observed on neighboring islands, including Orona Atoll in the Phoenix Islands of Kiribati, and the Rangiroa and Takapoto Atolls in the Tuamotus of French Polynesia. This discovery highlights the likeliness that there is still much biodiversity yet to be discovered from these remote and pristine reefs of the central Pacific.

Differential susceptibility of reef-building corals to deoxygenation reveals remarkable hypoxia tolerance.

Ocean deoxygenation threatens the persistence of coastal ecosystems worldwide. Despite an increasing awareness that coastal deoxygenation impacts tropical habitats, there remains a paucity of empirical data on the effects of oxygen limitation on reef-building corals. To address this knowledge gap, we conducted laboratory experiments with ecologically important Caribbean corals Acropora cervicornis and Orbicella faveolata. We tested the effects of continuous exposure to conditions ranging from extreme deoxygenation to normoxia (~ 1.0 to 6.25 mg L-1 dissolved oxygen) on coral bleaching, photophysiology, and survival. Coral species demonstrated markedly different temporal resistance to deoxygenation, and within a species there were minimal genotype-specific treatment effects. Acropora cervicornis suffered tissue loss and mortality within a day of exposure to severe deoxygenation (~ 1.0 mg L-1), whereas O. faveolata remained unaffected after 11 days of continuous exposure to 1.0 mg L-1. Intermediate deoxygenation treatments (~ 2.25 mg L-1, ~ 4.25 mg L-1) elicited minimal responses in both species, indicating a low oxygen threshold for coral mortality and coral resilience to oxygen concentrations that are lethal for other marine organisms. These findings demonstrate the potential for variability in species-specific hypoxia thresholds, which has important implications for our ability to predict how coral reefs may be affected as ocean deoxygenation intensifies. With deoxygenation emerging as a critical threat to tropical habitats, there is an urgent need to incorporate deoxygenation into coral reef research, management, and action plans to facilitate better stewardship of coral reefs in an era of rapid environmental change.

Rapid ecosystem-scale consequences of acute deoxygenation on a Caribbean coral reef.

Loss of oxygen in the global ocean is accelerating due to climate change and eutrophication, but how acute deoxygenation events affect tropical marine ecosystems remains poorly understood. Here we integrate analyses of coral reef benthic communities with microbial community sequencing to show how a deoxygenation event rapidly altered benthic community composition and microbial assemblages in a shallow tropical reef ecosystem. Conditions associated with the event precipitated coral bleaching and mass mortality, causing a 50% loss of live coral and a shift in the benthic community that persisted a year later. Conversely, the unique taxonomic and functional profile of hypoxia-associated microbes rapidly reverted to a normoxic assemblage one month after the event. The decoupling of ecological trajectories among these major functional groups following an acute event emphasizes the need to incorporate deoxygenation as an emerging stressor into coral reef research and management plans to combat escalating threats to reef persistence.

Resilience of Tropical Ecosystems to Ocean Deoxygenation.

The impacts of ocean deoxygenation on biodiversity and ecosystem function are well established in temperate regions, and here we illustrate how the study of hypoxia in tropical ecosystems can offer insights of general importance. We first describe how mechanisms of resilience have developed in response to naturally occurring hypoxia across three tropical ecosystems: coral reefs, seagrass beds, and mangrove forests. We then suggest that the vulnerability of these systems to deoxygenation lies in interactions with other stressors that are increasing rapidly in the Anthropocene. Finally, we advocate for the adoption of a broader community- and ecosystem-level perspective that incorporates mutualisms, feedbacks, and mechanisms of self-rescue and recovery to develop a better predictive understanding of the effects of deoxygenation in coastal ecosystems.

Ecophysiology of coral reef primary producers across an upwelling gradient in the tropical central Pacific.

Upwelling is an important source of inorganic nutrients in marine systems, yet little is known about how gradients in upwelling affect primary producers on coral reefs. The Southern Line Islands span a natural gradient of inorganic nutrient concentrations across the equatorial upwelling region in the central Pacific. We used this gradient to test the hypothesis that benthic autotroph ecophysiology is enhanced on nutrient-enriched reefs. We measured metabolism and photophysiology of common benthic taxa, including the algae Porolithon, Avrainvillea, and Halimeda, and the corals Pocillopora and Montipora. We found that temperature (27.2-28.7°C) was inversely related to dissolved inorganic nitrogen (0.46-4.63 µM) and surface chlorophyll a concentrations (0.108-0.147 mg m-3), which increased near the equator. Contrary to our prediction, ecophysiology did not consistently track these patterns in all taxa. Though metabolic rates were generally variable, Porolithon and Avrainvillea photosynthesis was highest at the most productive and equatorial island (northernmost). Porolithon photosynthetic rates also generally increased with proximity to the equator. Photophysiology (maximum quantum yield) increased near the equator and was highest at northern islands in all taxa. Photosynthetic pigments also were variable, but chlorophyll a and carotenoids in Avrainvillea and Montipora were highest at the northern islands. Phycobilin pigments of Porolithon responded most consistently across the upwelling gradient, with higher phycoerythrin concentrations closer to the equator. Our findings demonstrate that the effects of in situ nutrient enrichment on benthic autotrophs may be more complex than laboratory experiments indicate. While upwelling is an important feature in some reef ecosystems, ancillary factors may regulate the associated consequences of nutrient enrichment on benthic reef organisms.

Diel population and functional synchrony of microbial communities on coral reefs.

On coral reefs, microorganisms are essential for recycling nutrients to primary producers through the remineralization of benthic-derived organic matter. Diel investigations of reef processes are required to holistically understand the functional roles of microbial players in these ecosystems. Here we report a metagenomic analysis characterizing microbial communities in the water column overlying 16 remote forereef sites over a diel cycle. Our results show that microbial community composition is more dissimilar between day and night samples collected from the same site than between day or night samples collected across geographically distant reefs. Diel community differentiation is largely driven by the flux of Psychrobacter sp., which is two-orders of magnitude more abundant during the day. Nighttime communities are enriched with species of Roseobacter, Halomonas, and Alteromonas encoding a greater variety of pathways for carbohydrate catabolism, further illustrating temporal patterns of energetic provisioning between different marine microbes. Dynamic diel fluctuations of microbial populations could also support the efficient trophic transfer of energy posited in coral reef food webs.

Ocean acidification causes mortality in the medusa stage of the cubozoan Carybdea xaymacana.

Ocean pH is decreasing due to anthropogenic activities, and the consequences of this acidification on marine fauna and ecosystems are the subject of an increasing number of studies. Yet, the impact of ocean acidification (OA) on several abundant and ecologically important taxa, such as medusozoans, is poorly documented. To date there have been no studies on the effect of post-2050 OA projections on the medusa stage of jellyfish. As medusae represent the reproductive stage of cnidarians, negative impacts on adult jellyfish could severely impact the long-term survival of this group. Using a laboratory experiment, we investigated the effect of 2300 OA projections (i.e. pH of 7.5) on the mortality rate of the medusa-stage of the cubozoan species Carybdea xaymacana, compared to ambient seawater pH conditions (i.e. pH of 8.1). After a 12-h exposure to OA, C. xaymacana medusae suffered higher mortality rates compared to ambient conditions. This study represents the first evidence of the potential lethal effects of post-2050 OA projections on jellyfish. The higher metabolic rates of cubozoans compared to other cnidarians might make box jellyfish more vulnerable to OA. A decrease in the density of cnidarians could lead to harmful ecological events, such as algal blooms.

Gradients in Primary Production Predict Trophic Strategies of Mixotrophic Corals across Spatial Scales.

Mixotrophy is among the most successful nutritional strategies in terrestrial and marine ecosystems. The ability of organisms to supplement primary nutritional modes along continua of autotrophy and heterotrophy fosters trophic flexibility that can sustain metabolic demands under variable or stressful conditions. Symbiotic, reef-building corals are among the most broadly distributed and ecologically important mixotrophs, yet we lack a basic understanding of how they modify their use of autotrophy and heterotrophy across gradients of food availability. Here, we evaluate how one coral species, Pocillopora meandrina, supplements autotrophic nutrition through heterotrophy within an archipelago and test whether this pattern holds across species globally. Using stable isotope analysis (δ13C) and satellite-derived estimates of nearshore primary production (chlorophyll-a, as a proxy for food availability), we show that P. meandrina incorporates a greater proportion of carbon via heterotrophy when more food is available across five central Pacific islands. We then show that this pattern is consistent globally using data from 15 coral species across 16 locations spanning the Caribbean Sea and the Indian and Pacific Oceans. Globally, surface chlorophyll-a explains 77% of the variation in coral heterotrophic nutrition, 86% for one genus across 10 islands, and 94% when controlling for coral taxonomy within archipelagos. These results demonstrate, for the first time, that satellite-derived estimates of nearshore primary production provide a globally relevant proxy for resource availability that can explain variation in coral trophic ecology. Thus, our model provides a pivotal step toward resolving the biophysical couplings between mixotrophic organisms and spatial patterns of resource availability in the coastal oceans.

Nitrogen enrichment offsets direct negative effects of ocean acidification on a reef-building crustose coralline alga.

Ocean acidification (OA) and nutrient enrichment threaten the persistence of near shore ecosystems, yet little is known about their combined effects on marine organisms. Here, we show that a threefold increase in nitrogen concentrations, simulating enrichment due to coastal eutrophication or consumer excretions, offset the direct negative effects of near-future OA on calcification and photophysiology of the reef-building crustose coralline alga, Porolithon onkodes Projected near-future pCO2 levels (approx. 850 µatm) decreased calcification by 30% relative to ambient conditions. Conversely, nitrogen enrichment (nitrate + nitrite and ammonium) increased calcification by 90-130% in ambient and high pCO2 treatments, respectively. pCO2 and nitrogen enrichment interactively affected instantaneous photophysiology, with highest relative electron transport rates under high pCO2 and high nitrogen. Nitrogen enrichment alone increased concentrations of the photosynthetic pigments chlorophyll a, phycocyanin and phycoerythrin by approximately 80-450%, regardless of pCO2 These results demonstrate that nutrient enrichment can mediate direct organismal responses to OA. In natural systems, however, such direct benefits may be counteracted by simultaneous increases in negative indirect effects, such as heightened competition. Experiments exploring the effects of multiple stressors are increasingly becoming important for improving our ability to understand the ramifications of local and global change stressors in near shore ecosystems.

Baseline Assessment of Net Calcium Carbonate Accretion Rates on U.S. Pacific Reefs.

This paper presents a comprehensive quantitative baseline assessment of in situ net calcium carbonate accretion rates (g CaCO3 cm(-2) yr(-1)) of early successional recruitment communities on Calcification Accretion Unit (CAU) plates deployed on coral reefs at 78 discrete sites, across 11 islands in the central and south Pacific Oceans. Accretion rates varied substantially within and between islands, reef zones, levels of wave exposure, and island geomorphology. For forereef sites, mean accretion rates were the highest at Rose Atoll, Jarvis, and Swains Islands, and the lowest at Johnston Atoll and Tutuila. A comparison between reef zones showed higher accretion rates on forereefs compared to lagoon sites; mean accretion rates were also higher on windward than leeward sites but only for a subset of islands. High levels of spatial variability in net carbonate accretion rates reported herein draw attention to the heterogeneity of the community assemblages. Percent cover of key early successional taxa on CAU plates did not reflect that of the mature communities present on surrounding benthos, possibly due to the short deployment period (2 years) of the experimental units. Yet, net CaCO3 accretion rates were positively correlated with crustose coralline algae (CCA) percent cover on the surrounding benthos and on the CAU plates, which on average represented >70% of the accreted material. For foreeefs and lagoon sites combined CaCO3 accretion rates were statistically correlated with total alkalinity and Chlorophyll-a; a GAM analysis indicated that SiOH and Halimeda were the best predictor variables of accretion rates on lagoon sites, and total alkalinity and Chlorophyll-a for forereef sites, demonstrating the utility of CAUs as a tool to monitor changes in reef accretion rates as they relate to ocean acidification. This study underscores the pivotal role CCA play as a key benthic component and supporting actively calcifying reefs; high Mg-calcite exoskeletons makes CCA extremely susceptible changes in ocean water pH, emphasizing the far-reaching threat that ocean acidification poses to the ecological function and persistence of coral reefs worldwide.

Acclimatization of the crustose coralline alga Porolithon onkodes to variable pCO2.

Ocean acidification (OA) has important implications for the persistence of coral reef ecosystems, due to potentially negative effects on biomineralization. Many coral reefs are dynamic with respect to carbonate chemistry, and experience fluctuations in pCO2 that exceed OA projections for the near future. To understand the influence of dynamic pCO2 on an important reef calcifier, we tested the response of the crustose coralline alga Porolithon onkodes to oscillating pCO2. Individuals were exposed to ambient (400 µatm), high (660 µatm), or variable pCO2 (oscillating between 400/660 µatm) treatments for 14 days. To explore the potential for coralline acclimatization, we collected individuals from low and high pCO2 variability sites (upstream and downstream respectively) on a back reef characterized by unidirectional water flow in Moorea, French Polynesia. We quantified the effects of treatment on algal calcification by measuring the change in buoyant weight, and on algal metabolism by conducting sealed incubations to measure rates of photosynthesis and respiration. Net photosynthesis was higher in the ambient treatment than the variable treatment, regardless of habitat origin, and there was no effect on respiration or gross photosynthesis. Exposure to high pCO2 decreased P. onkodes calcification by >70%, regardless of the original habitat. In the variable treatment, corallines from the high variability habitat calcified 42% more than corallines from the low variability habitat. The significance of the original habitat for the coralline calcification response to variable, high pCO2 indicates that individuals existing in dynamic pCO2 habitats may be acclimatized to OA within the scope of in situ variability. These results highlight the importance of accounting for natural pCO2 variability in OA manipulations, and provide insight into the potential for plasticity in habitat and species-specific responses to changing ocean chemistry.

Ocean warming and acidification have complex interactive effects on the dynamics of a marine fungal disease.

Diseases threaten the structure and function of marine ecosystems and are contributing to the global decline of coral reefs. We currently lack an understanding of how climate change stressors, such as ocean acidification (OA) and warming, may simultaneously affect coral reef disease dynamics, particularly diseases threatening key reef-building organisms, for example crustose coralline algae (CCA). Here, we use coralline fungal disease (CFD), a previously described CCA disease from the Pacific, to examine these simultaneous effects using both field observations and experimental manipulations. We identify the associated fungus as belonging to the subphylum Ustilaginomycetes and show linear lesion expansion rates on individual hosts can reach 6.5 mm per day. Further, we demonstrate for the first time, to our knowledge, that ocean-warming events could increase the frequency of CFD outbreaks on coral reefs, but that OA-induced lowering of pH may ameliorate outbreaks by slowing lesion expansion rates on individual hosts. Lowered pH may still reduce overall host survivorship, however, by reducing calcification and facilitating fungal bio-erosion. Such complex, interactive effects between simultaneous extrinsic environmental stressors on disease dynamics are important to consider if we are to accurately predict the response of coral reef communities to future climate change.