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In recent years, coral populations in the western Atlantic have undergone widespread declines from climate change, anthropogenic stressors, and infectious disease outbreaks. The pillar coral, Dendrogyra cylindrus, has been one of the most affected species, prompting its listing as threatened under the United States Endangered Species Act in 2014 and critically endangered under the IUCN Red List in 2022. However, due to its natural rarity, it is particularly difficult to study using conventional long-term monitoring studies or less common paleontological investigations. Here, we document for the first time, the multi-century persistence of D. cylindrus on high-latitude nearshore reefs off southeast Florida during the late Holocene. Using high-precision uranium–thorium (U-Th) dating, we constrain the ages of well-preserved subfossil D. cylindrus colonies recovered from newly described coral death assemblages. We also describe specific morphological characteristics and taphonomic indicators reflecting their unique depositional environment. Our findings demonstrate long-term persistence of D. cylindrus in southeast Florida, despite geographical isolation and historical rarity in the region. [ABSTRACT FROM AUTHOR]

Corals populations worldwide are declining rapidly due to elevated ocean temperatures and other human impacts. The Caribbean harbors a high number of threatened, endangered, and critically endangered coral species compared to reefs of the larger Indo-Pacific. The reef corals of the Caribbean are also long diverged from their Pacific counterparts and may have evolved different survival strategies. Most genomic resources have been developed for Pacific coral species which may impede our ability to study the changes in genetic composition of Caribbean reef communities in response to global change. To help fill the gap in genomic resources, we used PacBio HiFi sequencing to generate the first genome assemblies for three Caribbean, reef-building corals, Colpophyllia natans, Dendrogyra cylindrus , and Siderastrea siderea. We also explore the genomic novelties that shape scleractinian genomes. Notably, we find abundant gene duplications of all classes (e.g., tandem and segmental), especially in S. siderea. This species has one of the largest genomes of any scleractinian coral (822Mb) which seems to be driven by repetitive content and gene family expansion and diversification. As the genome size of S. siderea was double the size expected of stony corals, we also evaluated the possibility of an ancient whole genome duplication using Ks tests and found no evidence of such an event in the species. By presenting these genome assemblies, we hope to develop a better understanding of coral evolution as a whole and to enable researchers to further investigate the population genetics and diversity of these three species., Competing Interests: Conflict of Interest The authors declare no conflict of interest.

As stony coral tissue loss disease (SCTLD) swept through the Florida Reef Tract, one of the most severely impacted species was the iconic pillar coral, Dendrogyra cylindrus. As the species’ population experienced a precipitous decline, a collaborative rescue project collected colony fragments for safekeeping at onshore and offshore nursery facilities. Between 2015 and 2019, a total of 574 fragments representing 128 genotypes were collected. These are currently dispersed among five facilities where they continue to provide opportunities to (1) refine best husbandry practices for D. cylindrus, (2) develop treatment options for SCTLD that have been adapted for use on other species, (3) maximize growth and fragmentation to provide the live tissue needed for eventual restoration, and (4) provide a source of parent colonies for assisted sexual reproduction and new genetic diversity. With the wild pillar coral population in Florida at the end of 2020 at less than 6% of its known 2014 population and continuing to decline, the rescued ex situ colonies represent the entirety of the restoration potential for this species in Florida.

Coral reefs worldwide are in a state of decline, but the population status and impacts of stressors for rare species are generally not well documented using broad-scale monitoring protocols. We fate-tracked all known colonies of the pillar coral, Dendrogyra cylindrus, on the Florida Reef Tract (FRT) from 2013 to 2020 to assess population condition and trend, and to document the relative impacts of chronic and acute stressors. Large average colony size, an absence of juveniles, and large geographic distances between genotypes suggest that the Florida D. cylindrus population has been reproductively extinct for decades. During the study period, low-intensity chronic stressors were balanced by regrowth, while back-to-back years of coral bleaching and thermally-exacerbated disease led to declines that the subsequent recovery rates suggest would require 11 uninterrupted years to overcome. The most recent stressor on Florida’s D. cylindrus population is “stony coral tissue loss disease” (SCTLD). Following the appearance of the disease in Florida in 2014, unrecoverable losses occurred within the D. cylindrus population as tissue, colonies, and whole genotypes suffered complete mortality. Losses of 94% of coral tissue, 93% of colonies, and 86% of genotypes between 2014 and the end of 2020 have led to functional extinction of D. cylindrus on the FRT.

Contrasts in spawning time between in situ and ex situ colonies of the pillar coral Dendrogyra cylindrus were assessed by comparing 8 years of in situ spawning observations with 3 years of observations on ex situ corals held in outdoor flow-through tanks. In situ colonies exhibited a 3-day spawning window, with peak spawning occurring three nights after the full moon and 90 (males) – 96 (females) min after sunset. The ex situ spawning window extended across 7 days, with a peak on nights 4–5 after the full moon; females continued to spawn through night 8. Ex situ spawning occurred ∼50 min later than in situ spawning, and the spawning window for ex situ females was significantly greater than for in situ colonies. Fragments held ex situ for as few as 10 days experienced delayed spawning times, but corals held for greater than one lunar year exhibited significantly later spawning than those held less than one lunar year. Early and late full moons resulted in earlier male spawn time and asynchronous gamete release between males and females. Comparing spawn times throughout the Caribbean identified distance from lighted shorelines as a strong correlate with spawn time in minutes after sunset; proximity to artificial light resulted in delayed spawn times. We propose that artificial lights are red-shifting the twilight spectrum and affecting corals’ perception of lighting cues that trigger spawning. Coral colonies held at outdoor ex situ facilities, which are subject to even higher levels of artificial light, exhibit even further asynchrony in spawning time as well as spawning night. The effects of widespread and increasing light pollution on spawning synchrony may represent a potential stressor that could inhibit natural reef recovery.

With ongoing changes in climate, rare and ecologically specialized species are at increased risk of extinction. In sessile foundation fauna that reproduce asexually via fragmentation of existing colonies, the number of colonies does not reflect the number of genets and thus can obscure genotypic diversity. Colonies that are the product of fragmentation are not visually distinguishable from colonies that stem from sexual recruits. For this reason, molecular markers are necessary to assess genotypic variation and population structure in clonal organisms such as reef-building corals and their endosymbiotic dinoflagellates. For the rare Caribbean pillar coral, Dendrogyra cylindrus, and its endosymbiotic dinoflagellate, Breviolum dendrogyrum, we use de novo microsatellite markers to infer past demographic changes, describe modern population structure, and quantify the frequency of asexual reproduction. Our analyses show that D. cylindrus comprises three distinct populations across the Greater Caribbean whereas the symbiont could be differentiated into four populations, indicating barriers to gene flow differ between host and symbiont. In Florida, host and symbiont populations reproduced mainly asexually, yielding lower genotypic diversity than predicted from census size. When multiple coral ramets were present, they often associated with the same clonal strain of B. dendrogyrum, pointing to the high fidelity of this relationship. Models of past demographic events revealed no evidence for historical changes in population sizes, consistent with the paleontological record of D. cylindrus indicating it has been rare for hundreds of thousands of years. The most recent global thermal stress event likely triggered a severe disease outbreak among D. cylindrus in Florida, resulting in a severe population decline. Projections indicate a high likelihood that this species will become extinct in the Northern Greater Caribbean within a few decades. The ecosystem consequences of losing rare coral species and their symbionts with increasingly frequent extreme warming events are not known but require urgent study.

Most scleractinian corals form obligate symbioses with photosynthetic dinoflagellates (family Symbiodiniaceae), which provide differential tolerances to their host. Previously, research has focused on the influence of symbiont composition and the dynamic processes of symbiont repopulation during single episodes of hyperthermal events, followed by years of less-stressful conditions. In contrast, this study characterized for the first time, the role of Symbiodiniaceae species changes in response to annually recurring hyperthermal events, a scenario soon expected to become the norm. Consecutive hyperthermal events during summer 2014 and 2015 along the Florida Reef Tract offered a unique opportunity to study bleaching susceptibility and recovery under recurrent annual hyperthermal scenarios. We utilized Illumina amplicon sequencing of the chloroplast 23S DNA region to assess with fine resolution the Symbiodiniaceae diversity associated with pillar coral, Dendrogyra cylindrus. Our findings show diverse assemblages of Symbiodiniaceae species and that some cryptic members are not transient associates but persistent and ecologically relevant, especially during recurrent annual warming events. This was evidenced by changes in relative abundance from the typically dominant host-specialist endosymbiont, Breviolum dendrogyrum, to B. meandrinium a host-generalist species common to corals in the family Meandrinidae but occurs at background densities in most coral colonies of D. cylindrus. The rise in abundance of B. meandrinium associated strongly with bleaching resistance in the coral host during two consecutive hyperthermal events. In some cases, host-compatible background symbionts can rapidly increase in abundance during episodes of stress and may impart physiological resilience to rapid environmental change and thus, represents a potentially important ecological process by which symbiotic corals acclimatize to changing ocean conditions.

The IUCN considers the stony coral Dendrogyra cylindrus as vulnerable. However, there is insufficient information on its population structure and dynamics, conservation status, or extinction risk and population decreases have been inferred from observations of habitat degradation. In 2002 and 2012, surveys using manta tows, circular plots and satellite images were performed in Old Providence and Santa Catalina Islands (Seaflower Biosphere Reserve) to determine changes in the condition and structure of a local population of D. cylindrus and its habitat. Size-frequency histograms were asymmetric and leptokurtic, showing positive distribution induced by colony fragmentation, which is indicative of reef degradation. Signs of degradation were more evident in 2012, when partial mortality of living tissue in the parent colony yielded 96.6% of the asexually produced fragments. Most of the fragments were from larger colonies (≥115 cm), which exhibited the highest partial and total mortality (>50%). Three of the four benthic habitats used by the species in 2002 were seen in 2012, but with reduced areas. The results suggest that the reduction of living tissue, the dominance of colonies produced asexually, and reduced size of fragments limit population growth and species viability in an unfavorable and changing habitat within this marine protected area (MPA) of the southwestern Caribbean. In the west of the reef complex of Old Providence, a synergy of multiple stressors could cause the habitat degradation and the fragmentation of colonies, limiting the potential recovery of the species and therefore the ability to create a healthy, genetically diverse and resilient population. Thus, these stressors must be minimized to prevent local extinction. Monitoring the population trends and recording sexual recruitment continues to be vital to understand the larvae’s habitat selection and determine whether these habitats are suitable for the survival of coral recruits. Other stressors to be monitored include anchor damage, diseases and bleaching. We recommend the MPA management program to include specific plans of conservation, recovery and restoration for coral reef builders species like D. cylindrus.

Scleractinian corals typically reproduce sexually as either gonochoric (separate male and female) or hermaphroditic (producing both eggs and sperm) colonies. The Caribbean pillar coral Dendrogyra cylindrus has been classified as gonochoric, but multi-year spawning observations at a Florida Keys site revealed incidences of hermaphroditism. Separate clonal colonies (ramets) of a single genet released either male or female gametes. Furthermore, 22% of observed ramets produced both eggs and sperm within different regions of a single colony. Over multiple years, one ramet switched from female to hermaphrodite, one from male to hermaphrodite, and one from hermaphrodite to male. Proposed evolutionary mechanisms include size- or age-based energy allocation, environmental energy allocation, or chemically induced change in a single-sex region. Because of the low population density of D. cylindrus in the Florida Keys, sexual partners are scarce, and hermaphroditism may be a strategy to yield higher rates of successful sexual reproduction. The findings also have implications for future restoration efforts aiming to strategically outplant individuals to maximize in situ fertilization. [ABSTRACT FROM AUTHOR]

Black band disease (BBD) affects many coral species worldwide and is considered a major contributor to the decline of reef-building coral. On the Florida Reef Tract BBD is most prevalent during summer and early fall when water temperatures exceed 29 °C. BBD is rarely reported in pillar coral ( Dendrogyra cylindrus) throughout the Caribbean, and here we document for the first time the appearance of the disease in this species on Florida reefs. The highest monthly BBD prevalence in the D. cylindrus population were 4.7% in 2014 and 6.8% in 2015. In each year, BBD appeared immediately following a hyperthermal bleaching event, which raises concern as hyperthermal seawater anomalies become more frequent. [ABSTRACT FROM AUTHOR]

Background: The Caribbean pillar coral Dendrogyra cylindrus was recently listed as a threatened species under the United States Endangered Species Act. One of the major threats to this species is its low, virtually undetectable recruitment rate. To our knowledge, sexually-produced recruits have never been found in over 30 years of surveys of Caribbean reefs. Until recently, the reproductive behavior of D. cylindrus was uncharacterized, limiting efforts to study its early life history, identify population bottlenecks, and conduct outplanting projects with sexually-produced offspring. In Curaçao, we observed the spawning behavior of this species over three years and five lunar cycles. We collected gametes from spawning individuals on three occasions and attempted to rear larvae and primary polyp settlers. Results: Here we describe successful fertilization methods for D. cylindrus and we document rapid embryonic development. We describe the successful propagation of embryos to the swimming larvae stage, the first settlement of larvae in the laboratory, and the survival of primary polyp settlers for over seven months. We show that spawning times are highly predictable from year to year relative to the lunar cycle and local sunset times. We use colony-level data to confirm that males begin spawning before females. We also provide the first reports of split-spawning across months in this species. Conclusions: Together, our findings of consistent spawning times, split-spawning, rapid embryonic development, and remarkable robustness of larvae and settlers now enable expanded research on the early life history and settlement ecology of D. cylindrus. This will help biologists to identify the population bottlenecks in nature that underlie low recruitment rates. Further, the settlement of D. cylindrus larvae in the laboratory now makes out-planting for restoration more feasible. Asynchronous spawning times and rapid embryonic development may have important consequences for population biology, connectivity, and management, by affecting fertilization dynamics and larval dispersal distances. We argue that a precautionary approach to conservation is warranted, given this species' peculiar life history traits and still-unresolved population structure. Overall, the natural history and husbandry contributions presented here should facilitate accelerated research and conservation of this threatened coral. [ABSTRACT FROM AUTHOR]