Algal Symbionts Research Articles

Stony coral tissue loss disease induces transcriptional signatures of in situ degradation of dysfunctional Symbiodiniaceae

Stony coral tissue loss disease (SCTLD), one of the most pervasive and virulent coral diseases on record, affects over 22 species of reef-building coral and is decimating reefs throughout the Caribbean. To understand how different coral species and their algal symbionts (family Symbiodiniaceae) respond to this disease, we examine the gene expression profiles of colonies of five species of coral from a SCTLD transmission experiment. The included species vary in their purported susceptibilities to SCTLD, and we use this to inform gene expression analyses of both the coral animal and their Symbiodiniaceae. We identify orthologous coral genes exhibiting lineage-specific differences in expression that correlate to disease susceptibility, as well as genes that are differentially expressed in all coral species in response to SCTLD infection. We find that SCTLD infection induces increased expression of rab7, an established marker of in situ degradation of dysfunctional Symbiodiniaceae, in all coral species accompanied by genus-level shifts in Symbiodiniaceae photosystem and metabolism gene expression. Overall, our results indicate that SCTLD infection induces symbiophagy across coral species and that the severity of disease is influenced by Symbiodiniaceae identity.

Caribbean scleractinian corals exhibit highly variable tolerances to acute hypoxia

IntroductionClimate change, and the increase in sea surface temperature, is exacerbating ocean deoxygenation because of the inherent property of seawater to sequester less dissolved gas, such as oxygen, at warmer temperatures. While most coral reef studies focus on the effects of thermal stress and ocean acidification, few studies acknowledge the threat of hypoxia. Hypoxia is traditionally defined as 6.3 kPa (2 mg L-1 O2), however, a universal hypoxia threshold is not useful given the vast range of responses among marine organisms. The range of metabolic responses and tolerances to hypoxia are unknown for Caribbean coral species and their algal symbionts.ObjectiveHere, we quantified the spectrum of acute hypoxia tolerances and the range of metabolic responses of six ecologically and structurally important Caribbean coral species (Acropora cervicornis, Siderastrea radians, Siderastrea siderea, Porites astreoides, Porites porites, and Orbicella faveolata) and their algal symbionts (Symbiodinium, Breviolum, and Durusdinium spp.).MethodsA total of 24 coral fragments (4 individuals per species) were exposed to 10 distinct oxygen concentrations ranging from normoxia (20.38 kPa) to severe hypoxia (3.3 kPa). We used intermittent flow respirometry to measure coral host respiration in the dark and algal symbiont photosynthesis in the light at each oxygen level. We determined a line of best fit for the metabolic rate vs. PO2 data and calculated the critical oxygen partial pressure (PO2 crit), a method that has not been tested on symbiotic species.ResultsCoral species and their algal symbionts measured here displayed a wide range of hypoxia tolerances. For the coral hosts, PO2 crit values differed roughly two-fold ranging from 5.74 kPa to 16.93 kPa, and for the algal symbionts, PO2 crit values differed roughly three-fold ranging from 3.9 kPa to 11.3 kPa.DiscussionThese results should be regarded as a first step to characterizing the metabolic response and acute tolerance of multiple coral hosts and algal symbionts to a wide range of oxygen concentrations. Given that some PO2 crit values were above the generally accepted hypoxia threshold, these results have implications for the community composition of reefs under a rapidly changing climate and can guide purposeful reef restoration.

Adult corals are uniquely more sensitive to manganese than coral early-life stages.

Manganese is an essential element and generally considered to be one of the least toxic metals to aquatic organisms, with chronic effects rarely seen at concentrations below 1000 µg/L. Anthropogenic activities lead to elevated concentrations of manganese in tropical marine waters. Limited data suggests that manganese is more acutely toxic to adult than to early life-stages of scleractinian corals in static renewal tests. However, to enable the inclusion of sufficient sensitive coral data in species sensitivity distributions to derive water quality guideline values (GVs) for manganese, we determined the acute toxicity of manganese to the adult scleractinian coral, Acropora muricata, in flow-through exposures. The 48-h EC50 was 824 µg Mn/L (based on time-weighted average, measured, dissolved manganese). The endpoint was tissue sloughing, a lethal process by which coral tissue detaches from the coral skeleton. Tissue sloughing was unrelated to superoxidase dismutase activity in coral tissue, and occurred in the absence of bleaching, i.e., toxic effects were observed for the coral host, but not for algal symbionts. We confirm that adult scleractinian corals are uniquely sensitive to manganese in acute exposures at concentrations 10 to 340 times lower than those reported to cause acute or chronic toxicity to coral early life stages, challenging the traditional notion that early life stages are more sensitive than mature organisms. This article is protected by copyright. All rights reserved. Environ Toxicol Chem 2023;00:0-0. © 2023 SETAC.

Changes in the microbiome of the sea anemone Exaiptasia diaphana during bleaching from short-term thermal elevation

We examined the response of microbial communities in the model sea anemone Exaiptasia diaphana (Aiptasia) to short-term thermal elevation. Through 16S rRNA gene sequencing, we characterized the microbiomes of symbiotic (with algal symbionts) and aposymbiotic (bleached) anemones under ambient (27°C) and heat-stressed (34°C) conditions for 8-10 days, using both replicated endpoint and non-replicated time-course approaches. Consistent with prior studies, we observed a stable abundance of bacteria from the families Alteromonadaceae and Rhodobacteraceae, though with wide variation among individual anemones. We observed that symbiotic state conferred a larger impact on the microbiome than heat stress, implying the microbiome may play a metabolic role in the maintenance of cnidarian-dinoflagellate symbiosis. In particular, Pelobacter, an anaerobic sulfate reducer that is also a potential nitrogen fixer, was present only in symbiotic anemones, and its abundance decreased with initial exposure to 34°C, but recovered after 7 days. In aposymbiotic anemones, the added heat stress appeared to result in a large increase of rare bacterial taxa, which included potential pathogens such as Vibrio following bleaching. We also observed several archaea, the first reported for this model, but only in the seawater surrounding aposymbiotic Aiptasia, where abundance increased dramatically following heat stress. We further explored the diazotrophic (nitrogen fixation) potential of diverse bacteria associated with symbiotic and aposymbiotic Aiptasia, under both ambient and heat-stressed conditions, using nifH-PCR and qPCR and the acetylene reduction assay (ARA). In contrast to some stony corals, nifH was barely expressed in both anemone types, and under ambient conditions, diazotrophic activity was not detectable via ARA. Thus, although this research contributes to the growing knowledge of the bacterial community associated with a prominent model used in coral-symbiosis research, our results also suggest using caution when making direct comparisons between Aiptasia and different coral species in microbiome studies.

Physiological Characterization of the Coral Holobiont Using a New Micro-Respirometry Tool

Metabolic activity, defined as the sum of organismal processes that involve energy, is of critical importance in understanding the function and evolution of life on earth. Measuring organismal metabolic rates is, therefore, at the center of explaining the physiological states of organisms, their ecological roles, and the impact of environmental change on species within terrestrial and aquatic ecosystems. On coral reefs, measures of metabolism have been used to quantify symbiosis functioning between corals and their obligate algal symbionts (Symbiodiniaceae), as well as assess how environmental stressors, including climate change, will impact coral health. Despite this significance, there is a lack of methods, and therefore data, relating to metabolic rate measurements in coral offspring, likely due to their small size. To address this gap, this study aimed to develop a custom setup for measuring the respiration of small (millimeter size range) marine animal ecologies. This low cost and easy setup should allow for the improved measurement of metabolic rate. This will be essential for applied ecological research utilizing the sexual production of corals for reef restoration.

More than meets the eye: characterizing the cryptic species complex and Symbiodiniaceae communities in the reef-dwelling nudibranch Pteraeolidia ‘semperi’ (Nudibranchia: Aeolidioidea) from Singapore

ABSTRACT The advent of molecular systematics has revolutionized our knowledge of biodiversity, revealing undiscovered cryptic lineages across the tree of life. Correspondingly, an increasing number of nudibranch species complexes have been found and described through integrative taxonomic approaches. Pteraeolidia ‘semperi’ (Nudibranchia: Cladobranchia: Aeolidioidea) presently represents a species complex, possessing ambiguous systematics and an underestimated diversity. Sequencing and phylogenetic reconstructions based on the cytochrome c oxidase subunit I marker from 48 samples of P. ‘semperi’ collected from Singapore's southern waters, as well as morphological analyses including scanning electron microscopy of the radula, suggest that P. ‘semperi’ comprises several distinct cryptic lineages. We further characterized the Symbiodiniaceae communities of P. ‘semperi’ from Singapore using metabarcoding of the internal transcribed spacer 2 gene. Pteraeolidia ‘semperi’ from Singapore was found to predominantly host Cladocopium and Durusdinium symbionts, and was significantly structured by biogeography. This study elucidates the present taxonomic diversity of P. ‘semperi’ in Singapore and contributes to the growing body of work on the diversity of algal symbionts associated with this enigmatic taxon.

Acute hypoxia induces reduction of algal symbiont density and suppression of energy metabolism in the scleractinian coral Pocillopora damicornis

Loss of oxygen in the ocean is accelerating and threatening the coral reef ecosystem. In this study, the impacts of hypoxia on the scleractinian coral Pocillopora damicornis were explored. The algal symbiont density, chlorophyll a + c2 content, energy consumption of corals, as well as energy available and consumption of their symbionts, decreased significantly post hypoxia stress. Meanwhile, the malondialdehyde contents in corals and symbionts, together with the caspase-3 activation level in corals, increased significantly in response to hypoxia stress. Furthermore, it was revealed that activities such as coral cell division and calcification were inhibited under hypoxia. These results collectively suggest that acute hypoxia stress reduces symbiont density and chlorophyll a + c2 content in the coral P. damicornis by elevating intracellular oxidative pressure and apoptotic level, which further suppresses energy metabolism in the symbiotic association and negatively affects a series of activities such as coral cell division and calcification.

The Bacterial Microbiome of the Coral Skeleton Algal Symbiont Ostreobium Shows Preferential Associations and Signatures of Phylosymbiosis.

Ostreobium, the major algal symbiont of the coral skeleton, remains understudied despite extensive research on the coral holobiont. The enclosed nature of the coral skeleton might reduce the dispersal and exposure of residing bacteria to the outside environment, allowing stronger associations with the algae. Here, we describe the bacterial communities associated with cultured strains of 5 Ostreobium clades using 16S rRNA sequencing. We shed light on their likely physical associations by comparative analysis of three datasets generated to capture (1) all algae associated bacteria, (2) enriched tightly attached and potential intracellular bacteria, and (3) bacteria in spent media. Our data showed that while some bacteria may be loosely attached, some tend to be tightly attached or potentially intracellular. Although colonised with diverse bacteria, Ostreobium preferentially associated with 34 bacterial taxa revealing a core microbiome. These bacteria include known nitrogen cyclers, polysaccharide degraders, sulphate reducers, antimicrobial compound producers, methylotrophs, and vitamin B12 producers. By analysing co-occurrence networks of 16S rRNA datasets from Porites lutea and Paragoniastrea australensis skeleton samples, we show that the Ostreobium-bacterial associations present in the cultures are likely to also occur in their natural environment. Finally, our data show significant congruence between the Ostreobium phylogeny and the community composition of its tightly associated microbiome, largely due to the phylosymbiotic signal originating from the core bacterial taxa. This study offers insight into the Ostreobium microbiome and reveals preferential associations that warrant further testing from functional and evolutionary perspectives.

Advancing coral microbiome manipulation to build long-term climate resilience

Coral reefs house one-third of all marine species and are of high cultural and socioeconomic importance. However, coral reefs are under dire threat from climate change and other anthropogenic stressors. Climate change is causing coral bleaching, the breakdown of the symbiosis between the coral host and its algal symbionts, often resulting in coral mortality and the deterioration of these valuable ecosystems. While it is essential to counteract the root causes of climate change, it remains urgent to develop coral restoration and conservation methods that will buy time for coral reefs. The manipulation of the bacterial microbiome that is associated with corals has been suggested as one intervention to improve coral climate resilience. Early coral microbiome-manipulation studies, which are aimed at enhancing bleaching tolerance, have shown promising results, but the inoculated bacteria did generally not persist within the coral microbiome. Here, we highlight the importance of long-term incorporation of bacterial inocula into the microbiome of target corals, as repeated inoculations will be too costly and not feasible on large reef systems like the Great Barrier Reef. Therefore, coral microbiome-manipulation studies need to prioritise approaches that can provide sustained coral climate resilience.

High Heterotrophic Plasticity of Massive Coral Porites pukoensis Contributes to Its Tolerance to Bioaccumulated Microplastics.

Scleractinian corals have been observed to be capable of accumulating microplastics from reef environments; however, the tolerant mechanism is poorly known. Here, we examined the response of Porites pukoensis to microplastic pollution by analyzing algal symbiont density, energetic metabolism, and caspase3 activities (representing the apoptosis level) in the coral-Symbiodiniaceae association. The environments of three fringing reef regions along the south coast of Sanya City, Hainan Province of China, were polluted by microplastics (for example, microplastic concentrations in the seawater ranged from 3.3 to 46.6 particles L-1), resulting in microplastic accumulation in P. pukoensis (0.4-2.4 particles cm-2). The accumulation of microplastics was negatively correlated to algal symbiont density in the corals but not to caspase3 activities in the two symbiotic partners, demonstrating that P. pukoensis could tolerate accumulated microplastics despite the decrease of algal symbiont density. Furthermore, results from the carbon stable isotope and cellular energy allocation assay indicated that P. pukoensis obtained energy availability (mainly as lipid reserves) using the switch between heterotrophy and autotrophy to maintain energy balance and cope with accumulated microplastics. Collectively, P. pukoensis achieved tolerance to microplastic pollution by maintaining energy availability, which was largely attributed to its high heterotrophic plasticity.

Symbiont composition and coral genotype determines massive coral species performance under end-of-century climate scenarios

The recent decline of coral health and substantial loss of coral cover along Florida’s Coral Reef (FCR) results from local stressors such as degraded water quality and disease outbreaks in addition to anthropogenically driven global stressors including ocean warming and acidification. Intervention strategies intended for the restoration of degraded reef habitats need a better understanding of the influence of ocean warming and acidification on coral health to target coral species and individual genotypes that may be more resistant or resilient to such stressors. Here, we examined a suite of physiological traits (coral host and algal symbiont) in response to experimentally elevated water temperatures and pCO2 levels, both separately and in concert, using threatened reef-building corals Pseudodiploria clivosa and Orbicella faveolata reared within a land-based coral nursery. After two months of exposure, responses differed by coral species, where P. clivosa showed declined physiology in response to combined ocean warming and acidification stress and ocean warming alone, whereas O. faveolata showed a positive response under ocean acidification. Responses to temperature could be associated with the algal symbionts harbored, as P. clivosa was dominated by the thermally sensitive Breviolum, and O. faveolata was dominated by the thermally tolerant Durusdinium. Additionally, corals were raised in well-sourced seawater that was naturally high in pCO2, which could have led to corals acclimating to acidified conditions. Of the three P. clivosa genets tested, we determined a top-performing genotype under the combined warming and acidification treatment. O. faveolata, however, displayed high genet variation by treatment and phenotypic trait, making genotype performance rankings challenging to discern. The evidence provided in this study demonstrates that high phenotypic variation in nursery-reared corals contributes to variable warming-acidification responses, suggesting that high-standing genetic variation in nursery-reared corals could support diverse coral restoration population outcomes along FCR.

Increased dominance of heat-tolerant symbionts creates resilient coral reefs in near-term ocean warming

Climate change is radically altering coral reef ecosystems, mainly through increasingly frequent and severe bleaching events. Yet, some reefs have exhibited higher thermal tolerance after bleaching severely the first time. To understand changes in thermal tolerance in the eastern tropical Pacific (ETP), we compiled four decades of temperature, coral cover, coral bleaching, and mortality data, including three mass bleaching events during the 1982 to 1983, 1997 to 1998 and 2015 to 2016 El Niño heatwaves. Higher heat resistance in later bleaching events was detected in the dominant framework-building genus, Pocillopora, while other coral taxa exhibited similar susceptibility across events. Genetic analyses of Pocillopora spp. colonies and their algal symbionts (2014 to 2016) revealed that one of two Pocillopora lineages present in the region (Pocillopora "type 1") increased its association with thermotolerant algal symbionts (Durusdinium glynnii) during the 2015 to 2016 heat stress event. This lineage experienced lower bleaching and mortality compared with Pocillopora "type 3", which did not acquire D. glynnii. Under projected thermal stress, ETP reefs may be able to preserve high coral cover through the 2060s or later, mainly composed of Pocillopora colonies that associate with D. glynnii. However, although the low-diversity, high-cover reefs of the ETP could illustrate a potential functional state for some future reefs, this state may only be temporary unless global greenhouse gas emissions and resultant global warming are curtailed.

Identification of quorum sensing-regulated Vibrio fortis as potential pathogenic bacteria for coral bleaching and the effects on the microbial shift.

Coastal pollution, global warming, ocean acidification, and other reasons lead to the imbalance of the coral reef ecosystem, resulting in the increasingly serious problem of coral degradation. Coral bleaching is often accompanied by structural abnormalities of coral symbiotic microbiota, among which Vibrio is highly concerned. In this study, Vibrio fortis S10-1 (MCCC 1H00104), isolated from sea cucumber, was used for the bacterial infection on coral Seriatopora guttatus and Pocillopora damicornis. The infection of S10-1 led to coral bleaching and a significant reduction of photosynthetic function in coral holobiont, and the pathogenicity of V. fortis was regulated by quorum sensing. Meanwhile, Vibrio infection also caused a shift of coral symbiotic microbial community, with significantly increased abundant Proteobacteria and Actinobacteria and significantly reduced abundant Firmicutes; on genus level, the abundance of Bacillus decreased significantly and the abundance of Rhodococcus, Ralstonia, and Burkholderia-Caballeronia-Paraburkholderia increased significantly; S10-1 infection also significantly impacted the water quality in the micro-ecosystem. In contrast, S10-1 infection showed less effect on the microbial community of the live stone, which reflected that the microbes in the epiphytic environment of the live stone might have a stronger ability of self-regulation; the algal symbionts mainly consisted of Cladocopium sp. and showed no significant effect by the Vibrio infection. This study verified that V. fortis is the primary pathogenic bacterium causing coral bleaching, revealed changes in the microbial community caused by its infection, provided strong evidence for the "bacterial bleaching" hypothesis, and provided an experimental experience for the exploration of the interaction mechanism among microbial communities, especially coral-associated Vibrio in the coral ecosystem, and potential probiotic strategy or QS regulation on further coral disease control.

ForamEcoGEnIE 2.0: incorporating symbiosis and spine traits into a trait-based global planktic foraminiferal model

Abstract. Planktic foraminifera are major marine calcifiers in the modern ocean, regulating the marine inorganic carbon pump, and generating marine fossil archives of past climate change. The foraminifera contain ecogroups with and without spines and algal symbionts, creating functional trait diversity which expands their ecological niches. Here, we incorporate symbiosis and spine traits into the symbiont-barren non-spinose foraminifer functional type in EcoGEnIE to represent all the extant foraminifera species. We calibrated the modelled new traits using Latin hypercube sampling (LHS) and identified the optimal model parameters from an ensemble of 1200 runs compared with global observations from core-top sediment samples, sediment traps, and plankton nets. The model successfully describes the global distribution and seasonal abundance variation of the four major foraminiferal functional groups. The model reproduces the dominance of the symbiont-obligate group in subtropical gyres and of the symbiont-barren types in the productive subpolar oceans. Global annual mean biomass and foraminifer-derived carbon export rate are correctly predicted compared to data, with biomass ranging from 0.001 to 0.010 mmol C m−3 and organic carbon export 0.002–0.031 mmol C m−2 d−1. The model captures the seasonal peak time of biomass and organic carbon export but struggles to reproduce the amplitude of both in productive areas. The sparseness and uneven distribution of observations and the model's limitation in upwelling regions likely contribute to this discrepancy. Our model overcomes the lack of major groups in the previous ForamEcoGEnIE 1.0 version and offers the potential to explore foraminiferal ecology dynamics and its impact on biogeochemistry in modern, future, and paleogeographic environments.

Structure of foliicolous lichen thalli formed by some common lecanoralean taxa in subtropical leaf communities

Numerous distinct clades of lichen-forming fungi have independently specialized as foliicolous colonists of living leaves in the humid tropics and subtropics. Because of technical difficulties, the anatomy of their minute crustose thalli has not been compared in detail. In the present study, we applied SEM-BSE imaging to sectioned blocks of embedded thalli representing six lecanoralean taxa of foliicolous lichen-forming fungi with unicellular green algal partners. We compared our observations with those obtained in a previous study of foliicolous Gomphillaceae (Ostropales), which utilize a similar type of algal partner. The upper surface of the thalli was a mostly continuous layer of mycobiont hyphae of typical diameter, unlike the largely acellular epilayer found previously in the foliicolous Gomphillaceae. Byssoloma leucoblepharum was exceptional in lacking a covering layer altogether. Thalli were essentially unstratified, with algal symbionts not confined to any distinct layer. Whereas the prothallus of foliicolous Gomphillaceae was derived from the overlying epilayer, in the lecanoralean taxa examined here the prothallus was derived from hyphae continuous with either the upper surface of the thallus or the lower surface, or both. This finding suggests that the prothallus of lichen forming fungi may represent structures of developmentally different origins in different taxa.

Climate warming causes photobiont degradation and carbon starvation in a boreal climate sentinel lichen.

The long-term potential for acclimation by lichens to changing climates is poorly known, despite their prominent roles in forested ecosystems. Although often considered "extremophiles," lichens may not readily acclimate to novel climates well beyond historical norms. In a previous study (Smith et al., 2018), Evernia mesomorpha transplants in a whole-ecosystem climate change experiment showed drastic mass loss after 1 yr of warming and drying; however, the causes of this mass loss were not addressed. We examined the causes of this warming-induced mass loss by measuring physiological, functional, and reproductive attributes of lichen transplants. Severe loss of mass and physiological function occurred above +2°C of experimental warming. Loss of algal symbionts ("bleaching") and turnover in algal community compositions increased with temperature and were the clearest impacts of experimental warming. Enhanced CO2 had no significant physiological or symbiont composition effects. The functional loss of algal photobionts led to significant loss of mass and specific thallus mass (STM), which in turn reduced water-holding capacity (WHC). Although algal genotypes remained detectable in thalli exposed to higher stress, within-thallus photobiont communities shifted in composition toward greater diversity. The strong negative impacts of warming and/or lower humidity on Evernia mesomorpha were driven by a loss of photobiont activity. Analogous to the effects of climate change on corals, the balance of symbiont carbon metabolism in lichens is central to their resilience to changing conditions.

A candidate transporter allowing symbiotic dinoflagellates to feed their coral hosts

The symbiotic partnership between corals and dinoflagellate algae is crucial to coral reefs. Corals provide their algal symbionts with shelter, carbon dioxide and nitrogen. In exchange, the symbiotic algae supply their animal hosts with fixed carbon in the form of glucose. But how glucose is transferred from the algal symbiont to the animal host is unknown. We reasoned that a transporter resident in the dinoflagellate cell membrane would facilitate outward transfer of glucose to the surrounding host animal tissue. We identified a candidate transporter in the cnidarian symbiont dinoflagellate Breviolum minutum that belongs to the ubiquitous family of facilitative sugar uniporters known as SWEETs (sugars will eventually be exported transporters). Previous gene expression analyses had shown that BmSWEET1 is upregulated when the algae are living symbiotically in a cnidarian host by comparison to the free-living state [1, 2]. We used immunofluorescence microscopy to localise BmSWEET1 in the dinoflagellate cell membrane. Substrate preference assays in a yeast surrogate transport system showed that BmSWEET1 transports glucose. Quantitative microscopy showed that symbiotic B. minutum cells have significantly more BmSWEET1 protein than free-living cells of the same strain, consistent with export during symbiosis but not during the free-living, planktonic phase. Thus, BmSWEET1 is in the right place, at the right time, and has the right substrate to be the transporter with which symbiotic dinoflagellate algae feed their animal hosts to power coral reefs.

Short-term improvement of heat tolerance in naturally growing Acropora corals in Okinawa.

Mass bleaching and subsequent mortality of reef corals by heat stress has increased globally since the late 20th century, due to global warming. Some experimental studies have reported that corals may increase heat tolerance for short periods, but only a few such studies have monitored naturally-growing colonies. Therefore, we monitored the survival, growth, and bleaching status of Acropora corals in fixed plots by distinguishing individual colonies on a heat-sensitive reef flat in Okinawa, Japan. The level of heat stress, assessed by the modified version of degree heating week duration in July and August, when the seawater temperature was the highest, was minimally but significantly higher in 2017 than in 2016; however, the same colonies exhibited less bleaching and mortality in 2017 than in 2016. Another study conducted at the same site showed that the dominant unicellular endosymbiotic algal species did not change before and after the 2016 bleaching, indicating that shifting and switching of the Symbiodiniaceae community did not contribute to improved heat tolerance. Colonies that suffered from partial mortality in 2016 were completely bleached at higher rates in 2017 than those without partial mortality in 2016. The present results suggest that either genetic or epigenetic changes in coral hosts and/or algal symbionts, or the shifting or switching of microbes other than endosymbionts, may have improved coral holobiont heat tolerance.

Rare species of West Indian aspect in the Holocene of Liverpool Bay and their biogeographic and environmental significance

The Gulf Stream, although not directly responsible for the mild, temperate climate of the British Isles, transports vast quantities of water across the North Atlantic Ocean. An extension of the Caribbean-Loop-Florida current system, this strong current cools and becomes more saline by evaporation as it flows NE across the North Atlantic Ocean. Nevertheless, it is able to transport benthic foraminifera across oceanic distances, the fauna around Bermuda containing many species described from the Caribbean Sea. Examining two cores taken from the shallow middle neritic Holocene Surface Sands Formation of the temperate Liverpool Bay, England, we found rare specimens of eight species recorded also from the neritic of the tropical Caribbean and subtropical Atlantic South Shelf Provinces: Asterigerina carinata, Dyocibicides biserialis, Elphidium discoidale, Nonionoides grateloupii, Quinqueloculina lamarckiana, Reussella atlantica and Sahulia conica. We are confident in our identifications of A. carinata and E. discoidale, but suggest that these names may have been applied to several cryptospecies. Some of these may have been transported on floating phytal debris, A. carinata, which supports algal symbionts, having been recorded at abyssal depths in the eastern North Atlantic. Othersmay have been transported as small propagules (proloculi). Although there may be a constant rain of such specimens into Liverpool Bay, we conclude on the basis of their rarity that the exotic species are unlikely to be able to overwinter there. We suggest, however, that these may have potential as invasive species for Liverpool Bay as climates continue to warm. This is not the earliest instance of transport of exotic species across the North Atlantic. The Late Eocene species Asterocyclina soldadoensis has been recorded from both the southern Caribbean region and offshore Ireland.

TOXICITY OF ZINC OXIDE TO SCLERACTINIAN CORALS AND ZOOXANTHELLAE: A BRIEF REVIEW

In recent years, the safety of sunscreens to coral reefs and the role these products would play in the process of coral bleaching has been a concern. However, the discussion centers almost exclusively on the organic components used as UV filters, with little attention given to inorganic UV filters, such as zinc oxide. Zinc oxide nanoparticles (ZnO-NPs) have been a common ingredient of sunscreen formulations for decades and are being discharged in coral reef environments. Even though there are data supporting that ZnO is toxic to certain species of fish and algae, regulatory agencies do not appear concerned with the possible outcome of the exposure of corals and their algal symbionts to this metal oxide. This review compiles the published work on the toxicity of ZnO and ZnO-NPs to corals and zooxanthellae, which strongly supports the notion that zinc oxide is toxic to both corals and microalgae. In view of this, concern has been raised by the use of the “reef safe” label to promote sunscreens that lack specific organic components, however containing ZnO as the major UV filter.