Fine‐scale structure among mesophotic populations of the great star coral Montastraea cavernosa revealed by SNP genotyping

Mesophotic reefs (30‐150 m) have been proposed as potential refugia that facilitate the recovery of degraded shallow reefs following acute disturbances such as coral bleaching and disease. However, because of the technical difficulty of collecting samples, the connectivity of adjacent mesophotic reefs is relatively unknown compared with shallower counterparts. We used genotyping by sequencing to assess fine‐scale genetic structure of Montastraea cavernosa at two sites at Pulley Ridge, a mesophotic coral reef ecosystem in the Gulf of Mexico, and downstream sites along the Florida Reef Tract. We found differentiation between reefs at Pulley Ridge (~68 m) and corals at downstream upper mesophotic depths in the Dry Tortugas (28–36 m) and shallow reefs in the northern Florida Keys (Key Biscayne, ~5 m). The spatial endpoints of our study were distinct, with the Dry Tortugas as a genetic intermediate. Most striking were differences in population structure among northern and southern sites at Pulley Ridge that were separated by just 12km. Unique patterns of clonality and outlier loci allele frequency support these sites as different populations and suggest that the long‐distance horizontal connectivity typical of shallow‐water corals may not be typical for mesophotic systems in Florida and the Gulf of Mexico. We hypothesize that this may be due to the spawning of buoyant gametes, which commits propagules to the surface, resulting in greater dispersal and lower connectivity than typically found between nearby shallow sites. Differences in population structure over small spatial scales suggest that demographic constraints and/or environmental disturbances may be more variable in space and time on mesophotic reefs compared with their shallow‐water counterparts.     

Population Structure of Montastraea cavernosa on Shallow versus Mesophotic Reefs in Bermuda

Mesophotic coral reef ecosystems remain largely unexplored with only limited information available on taxonomic composition, abundance and distribution. Yet, mesophotic reefs may serve as potential refugia for shallow-water species and thus understanding biodiversity, ecology and connectivity of deep reef communities is integral for resource management and conservation. The Caribbean coral, Montastraea cavernosa, is considered a depth generalist and is commonly found at mesophotic depths. We surveyed abundance and size-frequency of M. cavernosa populations at six shallow (10m) and six upper mesophotic (45m) sites in Bermuda and found population structure was depth dependent. The mean surface area of colonies at mesophotic sites was significantly smaller than at shallow sites, suggesting that growth rates and maximum colony surface area are limited on mesophotic reefs. Colony density was significantly higher at mesophotic sites, however, resulting in equal contributions to overall percent cover. Size-frequency distributions between shallow and mesophotic sites were also significantly different with populations at mesophotic reefs skewed towards smaller individuals. Overall, the results of this study provide valuable baseline data on population structure, which indicate that the mesophotic reefs of Bermuda support an established population of M. cavernosa.     

Modeling vertical coral connectivity and mesophotic refugia

Whether mesophotic reefs will behave as refugia for corals threatened by global climate change and coastal development depends on vertical exchange of larvae between diverse habitats. Here we use a biophysical model of larval dispersal to estimate vertical connectivity of a broadcasting (Orbicella faveolata) and a brooding (Porites astreoides) species of coral in the US Virgin Islands. Modeling predicts subsidy to shallow areas by mesophotic larvae of both species based on local hydrology, adult reproductive characteristics, larval traits, and a wide range of scenarios developed to test depth-sensitive factors, such as fertilization rates and post-settlement survivorship. In extreme model scenarios of reduced fertilization and post-settlement survivorship of mesophotic larvae, 1–10 % local mesophotic subsidy to shallow recruitment is predicted for both species, which are demographically significant. Although direct vertical connectivity is higher for the broadcaster, the brooder demonstrates higher local multigenerational vertical connectivity, which suggests that local P. astreoides populations are more resilient than those of O. faveolata, and corroborates field studies. As shallow habitat degrades, mesophotic–shallow subsidy is predicted to increase for both species. This study is the first of its kind to simulate larval dispersal and settlement between habitats of different depths, and these findings have local, regional, and global implications for predicting and managing coral reef persistence in a changing climate.     

The role of deep reefs in shallow reef recovery: an assessment of vertical connectivity in a brooding coral from west and east Australia

Approximately one quarter of zooxanthellate coral species have a depth distribution from shallow waters (<30 m) down to mesophotic depths of 30-60 m. The deeper populations of such species are less likely to be affected by certain environmental perturbations, including high temperature/high irradiance causing coral bleaching. This has led to the hypothesis that deep populations may serve as refuges and a source of recruits for shallow reef habitats. The extent of vertical connectivity of reef coral species, however, is largely unquantified. Using 10 coral host microsatellite loci and sequences of the host mtDNA putative control region, as well as ribosomal DNA (rDNA) ITS2 sequences of the coral's algal endosymbionts (Symbiodinium), we examine population structure, connectivity and symbiont specificity in the brooding coral Seriatopora hystrix across a depth profile in both northwest (Scott Reef) and northeast Australia (Yonge Reef). Strong genetic structuring over depth was observed in both regions based on the microsatellite loci; however, Yonge Reef exhibited an additional partitioning of mtDNA lineages (associated with specific symbiont ITS2 types), whereas Scott Reef was dominated by a single mtDNA lineage (with no apparent host-symbiont specificity). Evidence for recruitment of larvae of deep water origin into shallow habitats was found at Scott Reef, suggesting that recovery of shallow water habitats may be aided by migration from deep water refuges. Conversely, no migration from the genetically divergent deep slope populations into the shallow habitats was evident at Yonge Reef, making recovery of shallow habitats from deeper waters at this location highly unlikely.     

<Emphasis Type="Italic">Symbiodinium</Emphasis> associations with diseased and healthy scleractinian corals

Despite recent advances in identifying the causative agents of disease in corals and understanding the impact of epizootics on reef communities, little is known regarding the interactions among diseases, corals, and their dinoflagellate endosymbionts (Symbiodinium spp.). Since the genotypes of both corals and their resident Symbiodinium contribute to colony-level phenotypes, such as thermotolerance, symbiont genotypes might also contribute to the resistance or susceptibility of coral colonies to disease. To explore this, Symbiodinium were identified using the internal transcribed spacer-2 region of ribosomal DNA from diseased and healthy tissues within individual coral colonies infected with black band disease (BB), dark spot syndrome (DSS), white plague disease (WP), or yellow blotch disease (YB) in the Florida Keys (USA) and the US Virgin Islands. Most of the diseased colonies sampled contained B1, B5a, or C1 (depending on host species), while apparently healthy colonies of the same coral species frequently hosted these types and/or additional symbiont diversity. No potentially “parasitic” Symbiodinium types, uniquely associated with diseased coral tissue, were detected. Within most individual colonies, the same dominant Symbiodinium type was detected in diseased and visually healthy tissues. These data indicate that specific Symbiodinium types are not correlated with the infected tissues of diseased colonies and that DSS and WP onset do not trigger symbiont shuffling within infected tissues. However, few diseased colonies contained clade D symbionts suggesting a negative correlation between hosting Symbiodinium clade D and disease incidence in scleractinian corals. Understanding the influence of Symbiodinium diversity on colony phenotypes may play a critical role in predicting disease resistance and susceptibility in scleractinian corals.     

Depth-Independent Reproduction in the Reef Coral Porites astreoides from Shallow to Mesophotic Zones

Mesophotic coral ecosystems between 30–150 m may be important refugia habitat for coral reefs and associated benthic communities from climate change and coastal development. However, reduced light at mesophotic depths may present an energetic challenge to the successful reproduction of light-dependent coral organisms, and limit this refugia potential. Here, the relationship of depth and fecundity was investigated in a brooding depth-generalist scleractinian coral, Porites astreoides from 5–37 m in the U.S. Virgin Islands (USVI) using paraffin tissue histology. Despite a trend of increasing planulae production with depth, no significant differences were found in mean peak planulae density between shallow, mid-depth and mesophotic sites. Differential planulae production over depth is thus controlled by P. astreoides coral cover, which peaks at 10 m and ~35 m in the USVI. These results suggest that mesophotic ecosystems are reproductive refuge for P. astreoides in the USVI, and may behave as refugia for P. astreoides metapopulations providing that vertical larval exchanges are viable.     

Symbiont acquisition strategy drives host–symbiont associations in the southern Great Barrier Reef

Coral larvae acquire populations of the symbiotic dinoflagellate Symbiodinium from the external environment (horizontal acquisition) or inherit their symbionts from the parent colony (maternal or vertical acquisition). The effect of the symbiont acquisition strategy on Symbiodinium-host associations has not been fully resolved. Previous studies have provided mixed results, probably due to factors such as low sample replication of Symbiodinium from a single coral host, biogeographic differences in Symbiodinium diversity, and the presence of some apparently host-specific symbiont lineages in coral with either symbiont acquisition strategies. This study set out to assess the effect of the symbiont acquisition strategy by sampling Symbiodinium from 10 coral species (five with a horizontal and five with a vertical symbiont acquisition strategy) across two adjacent reefs in the southern Great Barrier Reef. Symbiodinium diversity was assessed using single-stranded conformational polymorphism of partial nuclear large subunit rDNA and denaturing gradient gel electrophoresis of the internal transcribed spacer 2 region. The Symbiodinium population in hosts with a vertical symbiont acquisition strategy partitioned according to coral species, while hosts with a horizontal symbiont acquisition strategy shared a common symbiont type across the two reef environments. Comparative analysis of existing data from the southern Great Barrier Reef found that the majority of corals with a vertical symbiont acquisition strategy associated with distinct species- or genus-specific Symbiodinium lineages, but some could also associate with symbiont types that were more commonly found in hosts with a horizontal symbiont acquisition strategy.     

Local endemicity and high diversity characterise high-latitude coral–Symbiodinium partnerships

Obligate symbiotic dinoflagellates (Symbiodinium) residing within the tissues of most reef invertebrates are important in determining the tolerance range of their host. Coral communities living at high latitudes experience wide fluctuations in environmental conditions and thus provide an ideal system to gain insights into the range within which the symbiotic relationship can be sustained. Further, understanding whether and how symbiont communities associated with high-latitude coral reefs are different from their tropical counterparts will provide clues to the potential of corals to cope with marginal or changing conditions. However, little is known of the host and symbiont partnerships at high latitudes. Symbiodinium diversity and specificity of high-latitude coral communities were explored using denaturing gradient gel electrophoresis (PCR-DGGE) analysis of the internal transcribed spacer regions (ITS1 and ITS2) of the ribosomal DNA at Lord Howe Island (31°S; Australia), and the Kermadec Islands (29°S; New Zealand). All but one host associated with clade C Symbiodinium, the exception being a soft coral (Capnella sp.) that contained Symbiodinium B1. Besides ‘host-generalist’ Symbiodinium types C1 and C3, approximately 72% of the Symbiodinium identified were novel C types, and zonation of symbionts in relation to environmental parameters such as depth and turbidity was evident in certain host species. The high-latitude Symbiodinium communities showed little overlap and relatively high diversity compared with communities sampled on the tropical Great Barrier Reef. Although host specificity was maintained in certain species, others shared symbionts and this potential reduction of fidelity at high-latitude locations may be the result of locally challenging and highly variable environmental conditions.     

Caribbean mesophotic coral ecosystems are unlikely climate change refugia

Deeper coral reefs experience reduced temperatures and light and are often shielded from localized anthropogenic stressors such as pollution and fishing. The deep reef refugia hypothesis posits that light‐dependent stony coral species at deeper depths are buffered from thermal stress and will avoid bleaching‐related mass mortalities caused by increasing sea surface temperatures under climate change. This hypothesis has not been tested because data collection on deeper coral reefs is difficult. Here we show that deeper (mesophotic) reefs, 30–75 m depth, in the Caribbean are not refugia because they have lower bleaching threshold temperatures than shallow reefs. Over two thermal stress events, mesophotic reef bleaching was driven by a bleaching threshold that declines 0.26 °C every +10 m depth. Thus, the main premise of the deep reef refugia hypothesis that cooler environments are protective is incorrect; any increase in temperatures above the local mean warmest conditions can lead to thermal stress and bleaching. Thus, relatively cooler temperatures can no longer be considered a de facto refugium for corals and it is likely that many deeper coral reefs are as vulnerable to climate change as shallow water reefs.     

Calcification rates of the massive coral Siderastrea siderea and crustose coralline algae along the Florida Keys (USA) outer-reef tract

Coral reefs are degrading on a global scale, and rates of reef-organism calcification are predicted to decline due to ocean warming and acidification. Systematic measurements of calcification over space and time are necessary to detect change resulting from environmental stressors. We established a network of calcification monitoring stations at four managed reefs along the outer Florida Keys Reef Tract (FKRT) from Miami to the Dry Tortugas. Eighty colonies (in two sequential sets of 40) of the reef-building coral, Siderastrea siderea, were transplanted to fixed apparatus that allowed repetitive detachment for buoyant weighing every 6 months. Algal-recruitment tiles were also deployed during each weighing interval to measure net calcification of the crustose coralline algal (CCA) community. Coral-calcification rates were an order of magnitude greater than those of CCA. Rates of coral calcification were seasonal (summer calcification was 53 % greater than winter), and corals in the Dry Tortugas calcified 48 % faster than those at the other three sites. Linear extension rates were also highest in the Dry Tortugas, whereas percent area of the coral skeletons excavated by bioeroding fauna was lowest. The spatial patterns in net coral calcification revealed here correlate well with Holocene reef thickness along the FKRT and, in part, support the “inimical waters hypothesis” proposed by Ginsburg, Hudson, and Shinn almost 50 yrs ago to explain reef development in this region. Due to the homogeneity in coral-calcification rates among the three main Keys sites, we recommend refinement of this hypothesis and suggest that water-quality variables (e.g., carbonate mineral saturation state, dissolved and particulate organic matter, light attenuation) be monitored alongside calcification in future studies. Our results demonstrate that our calcification monitoring network presents a feasible and worthwhile approach to quantifying potential impacts of ocean acidification, warming, and/or deteriorating water quality on the process of calcification.     

Assessing the ‘deep reef refugia’ hypothesis: focus on Caribbean reefs

Coral reefs in shallow-water environments (<30 m) are in decline due to local and global anthropogenic stresses. This has led to renewed interest in the ‘deep reef refugia’ hypothesis (DRRH), which stipulates that deep reef areas (1) are protected or dampened from disturbances that affect shallow reef areas and (2) can provide a viable reproductive source for shallow reef areas following disturbance. Using the Caribbean as an example, the assumptions of this hypothesis were explored by reviewing the literature for scleractinian corals—the reef framework builders on tropical reefs. Although there is evidence to support that deep reefs (>30 m) can escape the direct effects of storm-induced waves and thermal bleaching events, deep reefs are certainly not immune to disturbance. Additionally, the potential of deep reefs to provide propagules for shallow reef areas seems limited to ‘depth-generalist’ coral species, which constitute only ~25% of the total coral biodiversity. Larval connectivity between shallow and deep populations of these species may be further limited due to specific life history traits (e.g., brooding reproductive strategy and vertical symbiont acquisition mode). This review exposes how little is known about deep reefs and coral reproduction over depth. Hence, a series of urgent research priorities are proposed to determine the extent to which deep reefs may act as a refuge in the face of global reef decline.     

Bitten down to size: Fish predation determines growth form of the Caribbean coral reef sponge Mycale laevis

Interactions between organisms add complexity to ecosystem function, particularly on coral reefs. The Caribbean orange icing sponge Mycale laevis is semi-cryptic, often growing under coral colonies or between coral branches. This association is reportedly a mutualism, with the sponge deterring boring sponges from invading the coral skeleton and the coral providing an expanding surface for sponge growth. But is there an alternative explanation for the proximity of sponge and coral? We examined the importance of fish predation on the growth of the sponge. While the semi-cryptic growth form of M. laevis predominates on reefs off the Florida Keys and the Bahamas Islands, M. laevis grows with a non-cryptic, erect morphology off Bocas del Toro, Panama. Surveys revealed that sponge-eating fishes were rare or absent at Bocas del Toro compared to sites in the Florida Keys. Because past studies were inconsistent about the palatability of M. laevis to fish predators, we conducted feeding experiments with sponges from all three sites. Crude organic extracts of M. laevis from all three sites were palatable to generalist fish predators in aquarium assays, and field feeding assays and caging experiments conducted in the Florida Keys confirmed that spongivorous fishes readily ate exposed fragments of M. laevis. Our results suggest that M. laevis is restricted to its semi-cryptic growth form by spongivorous predators, with corals providing a physical refuge from predation. This alternative explanation supports the broader hypothesis that Caribbean reef sponges can be categorized on the basis of chemical defense into defended, palatable, and preferred species, the last of which are restricted to refugia.     

Contrasting abundance and contribution of clonal proliferation to the population structure of the corkscrew sea anemone Bartholomea annulata in the tropical Western Atlantic

Clonal propagation is an important life history trait for many sessile organisms, and often leads to the formation of monoclonal aggregations. In the marine environment, sea anemones have been model species for testing theory regarding the evolution of sex and understanding the contribution of sexual versus asexual reproduction to the population structure in facultatively clonal animals. However, little attention has been paid to tropical actiniarians. The corkscrew anemone Bartholomea annulata is common in tropical marine habitats in the western Atlantic and Caribbean; it forms small aggregations (2–4 anemones) on coral reefs and larger aggregations (>10 anemones) in mangrove habitats. We used field surveys and molecular analyses to investigate patterns of distribution, abundance, and genetic structure of aggregations formed by B. annulata on a reef in the US Virgin Islands and in a unique mangrove habitat in the Florida Keys. Abundance was greatest at the abandoned rock quarry mangrove habitat in the Florida Keys, where anemones formed continuously distributed aggregations carpeting the exposed limestone walls. Genetic diversity assessed via intersimple sequence repeats (ISSRs) and six microsatellite loci revealed that asexual reproduction plays only a minor role in the formation of both small and large anemone aggregations. Specifically, ISSR analyses showed that only ~10% of anemone aggregations were clonal in the US Virgin Islands, while microsatellite genotyping identified clonality in only 1 of 35 aggregations. In the Florida Keys, only four clonal genotypes were recovered within aggregations, but eight clones, representing 33% of the total surveyed population, had individuals in multiple aggregations. Thus, population structure of B. annulata appears to rely primarily on sexual reproduction, although asexual reproduction may play a nontrivial role in some environments. Mechanisms that drive the formation of genotypically diverse aggregations remain unknown, but may include attraction toward conspecifics, shared use of preferred habitats, or the local retention of larvae in partially enclosed habitats.     

Fitness consequences of habitat variability,trophic position,and energy allocation across the depth distribution of a coral-reef fish

Environmental clines such as latitude and depth that limit species’ distributions may be associated with gradients in habitat suitability that can affect the fitness of an organism. With the global loss of shallow-water photosynthetic coral reefs, mesophotic coral ecosystems (~30–150 m) may be buffered from some environmental stressors, thereby serving as refuges for a range of organisms including mobile obligate reef dwellers. Yet habitat suitability may be diminished at the depth boundary of photosynthetic coral reefs. We assessed the suitability of coral-reef habitats across the majority of the depth distribution of a common demersal reef fish (Stegastes partitus) ranging from shallow shelf (SS, <10 m) and deep shelf (DS, 20–30 m) habitats in the Florida Keys to mesophotic depths (MP, 60–70 m) at Pulley Ridge on the west Florida Shelf. Diet, behavior, and potential energetic trade-offs differed across study sites, but did not always have a monotonic relationship with depth, suggesting that some drivers of habitat suitability are decoupled from depth and may be linked with geographic location or the local environment. Feeding and diet composition differed among depths with the highest consumption of annelids, lowest ingestion of appendicularians, and the lowest gut fullness in DS habitats where predator densities were highest and fish exhibited risk-averse behavior that may restrict foraging. Fish in MP environments had a broader diet niche, higher trophic position, and higher muscle C:N ratios compared to shallower environments. High C:N ratios suggest increased tissue lipid content in fish in MP habitats that coincided with higher investment in reproduction based on gonado-somatic index. These results suggest that peripheral MP reefs are suitable habitats for demersal reef fish and may be important refuges for organisms common on declining shallow coral reefs.

     

Location‐Specific Metrics for Rapidly Estimating the Abundance and Condition of the Threatened Coral Acropora cervicornis

We developed a method for quantifying the abundance of the threatened staghorn coral (Acropora cervicornis) and evaluated the accuracy of commonly used methods to assess colony condition. For small‐ to medium‐sized colonies, we show that colony ellipsoid volume estimated from simple colony dimensions serves as a reliable and efficient proxy for the more time‐consuming, conventional measure of colony total linear extension, and that this predictive relationship varies significantly among extant populations in the Caribbean. We also determined that visual estimates of colony partial mortality closely approximate to true values for colonies with <25% mortality, with in situ estimates outperforming estimates from digital images. These results provide coral reef managers and restoration practitioners with guidance for assessing partial mortality and location‐specific regression models to estimate “amount” of staghorn coral in both extant and restored staghorn populations in Belize, the United States Virgin Islands, and the Dry Tortugas National Park, Florida, U.S.A. As staghorn coral monitoring and restoration efforts continue to expand in the Caribbean, these methods for quickly determining staghorn abundance and condition will directly aid resource managers tasked with monitoring wild populations and tracking restoration success over time.     

Evidence for a host role in thermotolerance divergence between populations of the mustard hill coral (Porites astreoides) from different reef environments

Studying the mechanisms that enable coral populations to inhabit spatially varying thermal environments can help evaluate how they will respond in time to the effects of global climate change and elucidate the evolutionary forces that enable or constrain adaptation. Inshore reefs in the Florida Keys experience higher temperatures than offshore reefs for prolonged periods during the summer. We conducted a common garden experiment with heat stress as our selective agent to test for local thermal adaptation in corals from inshore and offshore reefs. We show that inshore corals are more tolerant of a 6‐week temperature stress than offshore corals. Compared with inshore corals, offshore corals in the 31 °C treatment showed significantly elevated bleaching levels concomitant with a tendency towards reduced growth. In addition, dinoflagellate symbionts (Symbiodinium sp.) of offshore corals exhibited reduced photosynthetic efficiency. We did not detect differences in the frequencies of major (>5%) haplotypes comprising Symbiodinium communities hosted by inshore and offshore corals, nor did we observe frequency shifts (‘shuffling’) in response to thermal stress. Instead, coral host populations showed significant genetic divergence between inshore and offshore reefs, suggesting that in Porites astreoides, the coral host might play a prominent role in holobiont thermotolerance. Our results demonstrate that coral populations inhabiting reefs <10‐km apart can exhibit substantial differences in their physiological response to thermal stress, which could impact their population dynamics under climate change.     

The Relative Significance of Host–Habitat,Depth, and Geography on the Ecology,Endemism, and Speciation of Coral Endosymbionts in the Genus Symbiodinium

Dinoflagellates in the genus Symbiodinium are among the most abundant and important group of eukaryotic microbes found in coral reef ecosystems. Recent analyses conducted on various host cnidarians indicated that Symbiodinium assemblages in the Caribbean Sea are genetically and ecologically diverse. In order to further characterize this diversity and identify processes important to its origins, samples from six orders of Cnidaria comprising 45 genera were collected from reef habitats around Barbados (eastern Caribbean) and from the Mesoamerican barrier reef off the coast of Belize (western Caribbean). Fingerprinting of the ribosomal internal transcribed spacer 2 identified 62 genetically different Symbiodinium. Additional analyses of clade B Symbiodinium using microsatellite flanker sequences unequivocally characterized divergent lineages, or “species,” within what was previously thought to be a single entity (B1 or B184). In contrast to the Indo-Pacific where host-generalist symbionts dominate many coral communities, partner specificity in the Caribbean is relatively high and is influenced little by the host’s apparent mode of symbiont acquisition. Habitat depth (ambient light) and geographic isolation appeared to influence the bathymetric zonation and regional distribution for most of the Symbiodinium spp. characterized. Approximately 80% of Symbiodinium types were endemic to either the eastern or western Caribbean and 40–50% were distributed to compatible hosts living in shallow, high-irradiance, or deep, low-irradiance environments. These ecologic, geographic, and phylogenetic patterns indicate that most of the present Symbiodinium diversity probably originated from adaptive radiations driven by ecological specialization in separate Caribbean regions during the Pliocene and Pleistocene periods.     

Role of host genetics and heat‐tolerant algal symbionts in sustaining populations of the endangered coral Orbicella faveolata in the Florida Keys with ocean warming

Identifying which factors lead to coral bleaching resistance is a priority given the global decline of coral reefs with ocean warming. During the second year of back‐to‐back bleaching events in the Florida Keys in 2014 and 2015, we characterized key environmental and biological factors associated with bleaching resilience in the threatened reef‐building coral Orbicella faveolata. Ten reefs (five inshore, five offshore, 179 corals total) were sampled during bleaching (September 2015) and recovery (May 2016). Corals were genotyped with 2bRAD and profiled for algal symbiont abundance and type. O. faveolata at the inshore sites, despite higher temperatures, demonstrated significantly higher bleaching resistance and better recovery compared to offshore. The thermotolerant Durusdinium trenchii (formerly Symbiondinium trenchii) was the dominant endosymbiont type region‐wide during initial (78.0% of corals sampled) and final (77.2%) sampling; >90% of the nonbleached corals were dominated by D. trenchii. 2bRAD host genotyping found no genetic structure among reefs, but inshore sites showed a high level of clonality. While none of the measured environmental parameters were correlated with bleaching, 71% of variation in bleaching resistance and 73% of variation in the proportion of D. trenchii was attributable to differences between genets, highlighting the leading role of genetics in shaping natural bleaching patterns. Notably, D. trenchii was rarely dominant in O. faveolata from the Florida Keys in previous studies, even during bleaching. The region‐wide high abundance of D. trenchii was likely driven by repeated bleaching associated with the two warmest years on record for the Florida Keys (2014 and 2015). On inshore reefs in the Upper Florida Keys, O. faveolata was most abundant, had the highest bleaching resistance, and contained the most corals dominated by D. trenchii, illustrating a causal link between heat tolerance and ecosystem resilience with global change.     

Allelopathy in the tropical alga Lobophora variegata (Phaeophyceae): mechanistic basis for a phase shift on mesophotic coral reefs?

Macroalgal phase shifts on Caribbean reefs have been reported with increasing frequency, and recent reports of these changes on mesophotic coral reefs have raised questions regarding the mechanistic processes behind algal population expansions to deeper depths. The brown alga Lobophora variegata is a dominant species on many shallow and deep coral reefs of the Caribbean and Pacific, and it increased in percent cover (>50%) up to 61 m on Bahamian reefs following the invasion of the lionfish Pterois volitans. We examined the physiological and ecological constraints contributing to the spread of Lobophora on Bahamian reefs across a mesophotic depth gradient from 30 to 61 m, pre‐ and post‐lionfish invasion. Results indicate that there were no physiological limitations to the depth distribution of Lobophora within this range prior to the lionfish invasion. Herbivory by acanthurids and scarids in algal recruitment plots at mesophotic depths was higher prior to the lionfish invasion, and Lobophora chemical defenses were ineffective against an omnivorous fish species. In contrast, Lobophora exhibited significant allelopathic activity against the coral Montastraea cavernosa and the sponge Agelas clathrodes in laboratory assays. These data indicate that when lionfish predation on herbivorous fish released Lobophora from grazing pressure at depth, Lobophora expanded its benthic cover to a depth of 61 m, where it replaced the dominant coral and sponge species. Our results suggest that this chemically defended alga may out‐compete these species in situ, and that mesophotic reefs may be further impacted in the near future as Lobophora continues to expand to its compensation point.