Performance of Orbicella faveolata larval cohorts does not align with previously observed thermal tolerance of adult source populations.

Orbicella faveolata, commonly known as the mountainous star coral, is a dominant reef-building species in the Caribbean, but populations have suffered sharp declines since the 1980s due to repeated bleaching and disease-driven mortality. Prior research has shown that inshore adult O. faveolata populations in the Florida Keys are able to maintain high coral cover and recover from bleaching faster than their offshore counterparts. However, whether this origin-specific variation in thermal resistance is heritable remains unclear. To address this knowledge gap, we produced purebred and hybrid larval crosses from O. faveolata gametes collected at two distinct reefs in the Upper Florida Keys, a nearshore site (Cheeca Rocks, CR) and an offshore site (Horseshoe Reef, HR), in two different years (2019, 2021). We then subjected these aposymbiotic larvae to severe (36°C) and moderate (32°C) heat challenges to quantify their thermal tolerance. Contrary to our expectation based on patterns of adult thermal tolerance, HR purebred larvae survived better and exhibited gene expression profiles that were less driven by stress response under elevated temperature compared to purebred CR and hybrid larvae. One potential explanation could be the compromised reproductive output of CR adult colonies due to repeated summer bleaching events in 2018 and 2019, as gametes originating from CR in 2019 contained less storage lipids than those from HR. These findings provide an important counter-example to the current selective breeding paradigm, that more tolerant parents will yield more tolerant offspring, and highlight the importance of adopting a holistic approach when evaluating larval quality for conservation and restoration purposes.

What drives phenotypic divergence among coral clonemates of Acropora palmata?

Evolutionary rescue of populations depends on their ability to produce phenotypic variation that is heritable and adaptive. DNA mutations are the best understood mechanisms to create phenotypic variation, but other, less well-studied mechanisms exist. Marine benthic foundation species provide opportunities to study these mechanisms because many are dominated by isogenic stands produced through asexual reproduction. For example, Caribbean acroporid corals are long lived and reproduce asexually via breakage of branches. Fragmentation is often the dominant mode of local population maintenance. Thus, large genets with many ramets (colonies) are common. Here, we observed phenotypic variation in stress responses within genets following the coral bleaching events in 2014 and 2015 caused by high water temperatures. This was not due to genetic variation in their symbiotic dinoflagellates (Symbiodinium "fitti") because each genet of this coral species typically harbours a single strain of S. "fitti". Characterization of the microbiome via 16S tag sequencing correlated the abundance of only two microbiome members (Tepidiphilus, Endozoicomonas) with a bleaching response. Epigenetic changes were significantly correlated with the host's genetic background, the location of the sampled polyps within the colonies (e.g., branch vs. base of colony), and differences in the colonies' condition during the bleaching event. We conclude that long-term microenvironmental differences led to changes in the way the ramets methylated their genomes, contributing to the differential bleaching response. However, most of the variation in differential bleaching response among clonemates of Acropora palmata remains unexplained. This research provides novel data and hypotheses to help understand intragenet variability in stress phenotypes of sessile marine species.

Opportunistic consumption of coral spawn by the ruby brittle star (Ophioderma rubicundum).

Many reef invertebrates reproduce through simultaneous broadcast spawning, with an apparent advantage of overwhelming potential predators and maximizing propagule survival. Although reef fish have been observed to consume coral gamete bundles during spawning events, there are few records of such predation by benthic invertebrates. Here, we document several instances of the ruby brittle star, Ophioderma rubicundum, capturing and consuming egg-sperm bundles of the mountainous star coral, Orbicella faveolata, and the symmetrical brain coral, Pseudodiploria strigosa, during spawning events in the Cayman Islands in 2012 and the Florida Keys in 2022. These observations are widely separated in space and time (>600 km, 10 years), suggesting that this behavior may be prevalent on western Atlantic reefs. Since O. rubicundum spawns on the same or subsequent nights as these coral species, we hypothesize that this opportunistic feeding behavior takes advantage of lipid-rich coral gamete bundles to recover energy reserves expended by the brittle star during gametogenesis. The consumption of coral gametes by adult brittle stars suggests an underexplored trophic link between reef invertebrates and also provides evidence that ophiuroid-coral symbioses may oscillate between commensalism and parasitism depending on the ontogeny and reproductive status of both animals. Our observations provide insights into the nuanced, dynamic associations between coral reef invertebrates and may have implications for coral reproductive success and resilience.

Microbiome differences in disease-resistant vs. susceptible Acropora corals subjected to disease challenge assays.

In recent decades coral gardening has become increasingly popular to restore degraded reef ecosystems. However, the growth and survivorship of nursery-reared outplanted corals are highly variable. Scientists are trying to identify genotypes that show signs of disease resistance and leverage these genotypes in restoring more resilient populations. In a previous study, a field disease grafting assay was conducted on nursery-reared Acropora cervicornis and Acropora palmata to quantify relative disease susceptibility. In this study, we further evaluate this field assay by investigating putative disease-causing agents and the microbiome of corals with disease-resistant phenotypes. We conducted 16S rRNA gene high-throughput sequencing on A. cervicornis and A. palmata that were grafted (inoculated) with a diseased A. cervicornis fragment. We found that independent of health state, A. cervicornis and A. palmata had distinct alpha and beta diversity patterns from one another and distinct dominant bacteria. In addition, despite different microbiome patterns between both inoculated coral species, the genus Sphingomonadaceae was significantly found in both diseased coral species. Additionally, a core bacteria member from the order Myxococcales was found at relatively higher abundances in corals with lower rates of disease development following grafting. In all, we identified Sphingomonadaceae as a putative coral pathogen and a bacterium from the order Myxococcales associated with corals that showed disease resistant phenotypes.

Genotypic variation in disease susceptibility among cultured stocks of elkhorn and staghorn corals.

Disease mortality has been a primary driver of population declines and the threatened status of the foundational Caribbean corals, Acropora palmata and A. cervicornis. There remain few tools to effectively manage coral disease. Substantial investment is flowing into in situ culture and population enhancement efforts, while disease takes a variable but sometimes high toll in restored populations. If genetic resistance to disease can be identified in these corals, it may be leveraged to improve resistance in restored populations and possibly lead to effective diagnostic tests and disease treatments. Using a standardized field protocol based on replicated direct-graft challenge assays, we quantified this important trait in cultured stocks from three field nurseries in the Florida Keys. Field tests of 12 genotypes of A. palmata and 31 genotypes of A. cervicornis revealed significant genotypic variation in disease susceptibility of both species measured both as risk of transmission (percent of exposed fragments that displayed tissue loss) and as the rate of tissue loss (cm2 d-1) in fragments with elicited lesions. These assay results provide a measure of relative disease resistance that can be incorporated, along with consideration of other important traits such as growth and reproductive success, into restoration strategies to yield more resilient populations.

Reef-scale trends in Florida Acropora spp. abundance and the effects of population enhancement.

Since the listing of Acropora palmata and A. cervicornis under the US Endangered Species Act in 2006, increasing investments have been made in propagation of listed corals (primarily A. cervicornis, A. palmata to a much lesser extent) in offshore coral nurseries and outplanting cultured fragments to reef habitats. This investment is superimposed over a spatiotemporal patchwork of ongoing disturbances (especially storms, thermal bleaching, and disease) as well as the potential for natural population recovery. In 2014 and 2015, we repeated broad scale (>50 ha), low precision Acropora spp. censuses (i.e., direct observation by snorkelers documented via handheld GPS) originally conducted in appropriate reef habitats during 2005-2007 to evaluate the trajectory of local populations and the effect of population enhancement. Over the decade-long study, A. palmata showed a cumulative proportional decline of 0.4 -0.7x in colony density across all sites, despite very low levels of outplanting at some sites. A. cervicornis showed similar proportional declines at sites without outplanting. In contrast, sites that received A. cervicornis outplants showed a dramatic increase in density (over 13x). Indeed, change in A. cervicornis colony density was significantly positively correlated with cumulative numbers of outplants across sites. This study documents a substantive reef-scale benefit of Acropora spp. population enhancement in the Florida Keys, when performed at adequate levels, against a backdrop of ongoing population decline.

Decadal comparison of a diminishing coral community: a study using demographics to advance inferences of community status.

The most common coral monitoring methods estimate coral abundance as percent cover, either via in situ observations or derived from images. In recent years, growing interest and effort has focused on colony-based (demographic) data to assess the status of coral populations and communities. In this study, we relied on two separate data sets (photo-derived percent cover estimates, 2002-12, and opportunistic in situ demographic sampling, 2004 and 2012) to more fully infer decadal changes in coral communities at a small, uninhabited Caribbean island. Photo-derived percent cover documented drastic declines in coral abundance including disproportionate declines in Orbicella spp. While overall in situ estimates of total coral density were not different between years, densities of several rarer taxa were. Meandrina meandrites and Stephanocoenia intersepta increased while Leptoseris cucullata decreased significantly, changes that were not discernable from the photo-derived cover estimates. Demographic data also showed significant shifts to larger colony sizes (both increased mean colony sizes and increased negative skewness of size frequency distributions, but similar maximum colony sizes) for most taxa likely indicating reduced recruitment. Orbicella spp. differed from this general pattern, significantly shifting to smaller colony sizes due to partial mortality. Both approaches detected significant decadal changes in coral community structure at Navassa, though the demographic sampling provided better resolution of more subtle, taxon-specific changes.

Environmental conditions influence tissue regeneration rates in scleractinian corals.

Natural and anthropogenic factors may influence corals' ability to recover from partial mortality. To examine how environmental conditions affect lesion healing, we assessed several water quality parameters and tissue regeneration rates in corals at six reefs around St. Thomas, US Virgin Islands. We hypothesized that sites closer to developed areas would have poor water quality due to proximity to anthropogenic stresses, which would impede tissue regeneration. We found that water flow and turbidity most strongly influenced lesion recovery rates. The most impacted site, with high turbidity and low flow, recovered almost three times slower than the least impacted site, with low turbidity, high flow, and low levels of anthropogenic disturbance. Our results illustrate that in addition to lesion-specific factors known to affect tissue regeneration, environmental conditions can also control corals' healing rates. Resource managers can use this information to protect low-flow, turbid nearshore reefs by minimizing sources of anthropogenic stress.

Disease dynamics and potential mitigation among restored and wild staghorn coral, Acropora cervicornis.

The threatened status (both ecologically and legally) of Caribbean staghorn coral, Acropora cervicornis, has prompted rapidly expanding efforts in culture and restocking, although tissue loss diseases continue to affect populations. In this study, disease surveillance and histopathological characterization were used to compare disease dynamics and conditions in both restored and extant wild populations. Disease had devastating effects on both wild and restored populations, but dynamics were highly variable and appeared to be site-specific with no significant differences in disease prevalence between wild versus restored sites. A subset of 20 haphazardly selected colonies at each site observed over a four-month period revealed widely varying disease incidence, although not between restored and wild sites, and a case fatality rate of 8%. A tropical storm was the only discernable environmental trigger associated with a consistent spike in incidence across all sites. Lastly, two field mitigation techniques, (1) excision of apparently healthy branch tips from a diseased colony, and (2) placement of a band of epoxy fully enclosing the diseased margin, gave equivocal results with no significant benefit detected for either treatment compared to controls. Tissue condition of associated samples was fair to very poor; unsuccessful mitigation treatment samples had severe degeneration of mesenterial filament cnidoglandular bands. Polyp mucocytes in all samples were infected with suspect rickettsia-like organisms; however, no bacterial aggregates were found. No histological differences were found between disease lesions with gross signs fitting literature descriptions of white-band disease (WBD) and rapid tissue loss (RTL). Overall, our results do not support differing disease quality, quantity, dynamics, nor health management strategies between restored and wild colonies of A. cervicornis in the Florida Keys.

Removal of corallivorous snails as a proactive tool for the conservation of acroporid corals.

Corallivorous snail feeding is a common source of tissue loss for the threatened coral, Acropora palmata, accounting for roughly one-quarter of tissue loss in monitored study plots over seven years. In contrast with larger threats such as bleaching, disease, or storms, corallivory by Coralliophila abbreviata is one of the few direct sources of partial mortality that may be locally managed. We conducted a field experiment to explore the effectiveness and feasibility of snail removal. Long-term monitoring plots on six reefs in the upper Florida Keys were assigned to one of three removal treatments: (1) removal from A. palmata only, (2) removal from all host coral species, or (3) no-removal controls. During the initial removal in June 2011, 436 snails were removed from twelve 150 m(2) plots. Snails were removed three additional times during a seven month "removal phase", then counted at five surveys over the next 19 months to track recolonization. At the conclusion, snails were collected, measured and sexed. Before-After-Control-Impact analysis revealed that both snail abundance and feeding scar prevalence were reduced in removal treatments compared to the control, but there was no difference between removal treatments. Recolonization by snails to baseline abundance is estimated to be 3.7 years and did not differ between removal treatments. Recolonization rate was significantly correlated with baseline snail abundance. Maximum snail size decreased from 47.0 mm to 34.6 mm in the removal treatments. The effort required to remove snails from A. palmata was 30 diver minutes per 150 m(2) plot, compared with 51 min to remove snails from all host corals. Since there was no additional benefit observed with removing snails from all host species, removals can be more efficiently focused on only A. palmata colonies and in areas where C. abbreviata abundance is high, to effectively conserve A. palmata in targeted areas.