Growth Dynamics of the Threatened Caribbean Staghorn Coral Acropora cervicornis: Influence of Host Genotype,Symbiont Identity,Colony Size,and Environmental Setting

Background

The drastic decline in the abundance of Caribbean acroporid corals (Acropora cervicornis, A. palmata) has prompted the listing of this genus as threatened as well as the development of a regional propagation and restoration program. Using in situ underwater nurseries, we documented the influence of coral genotype and symbiont identity, colony size, and propagation method on the growth and branching patterns of staghorn corals in Florida and the Dominican Republic.

Methodology/Principal Findings

Individual tracking of> 1700 nursery-grown staghorn fragments and colonies from 37 distinct genotypes (identified using microsatellites) in Florida and the Dominican Republic revealed a significant positive relationship between size and growth, but a decreasing rate of productivity with increasing size. Pruning vigor (enhanced growth after fragmentation) was documented even in colonies that lost 95% of their coral tissue/skeleton, indicating that high productivity can be maintained within nurseries by sequentially fragmenting corals. A significant effect of coral genotype was documented for corals grown in a common-garden setting, with fast-growing genotypes growing up to an order of magnitude faster than slow-growing genotypes. Algal-symbiont identity established using qPCR techniques showed that clade A (likely Symbiodinium A3) was the dominant symbiont type for all coral genotypes, except for one coral genotype in the DR and two in Florida that were dominated by clade C, with A- and C-dominated genotypes having similar growth rates.

Conclusion/Significance

The threatened Caribbean staghorn coral is capable of extremely fast growth, with annual productivity rates exceeding 5 cm of new coral produced for every cm of existing coral. This species benefits from high fragment survivorship coupled by the pruning vigor experienced by the parent colonies after fragmentation. These life-history characteristics make A. cervicornis a successful candidate nursery species and provide optimism for the potential role that active propagation can play in the recovery of this keystone species.     

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.     

Occupation Dynamics and Impacts of Damselfish Territoriality on Recovering Populations of the Threatened Staghorn Coral,Acropora cervicornis

Large-scale coral reef restoration is needed to help recover structure and function of degraded coral reef ecosystems and mitigate continued coral declines. In situ coral propagation and reef restoration efforts have scaled up significantly in past decades, particularly for the threatened Caribbean staghorn coral, Acropora cervicornis, but little is known about the role that native competitors and predators, such as farming damselfishes, have on the success of restoration. Steep declines in A. cervicornis abundance may have concentrated the negative impacts of damselfish algal farming on a much lower number of coral prey/colonies, thus creating a significant threat to the persistence and recovery of depleted coral populations. This is the first study to document the prevalence of resident damselfishes and negative effects of algal lawns on A. cervicornis along the Florida Reef Tract (FRT). Impacts of damselfish lawns on A. cervicornis colonies were more prevalent (21.6% of colonies) than those of other sources of mortality (i.e., disease (1.6%), algal/sponge overgrowth (5.6%), and corallivore predation (7.9%)), and damselfish activities caused the highest levels of tissue mortality (34.6%) among all coral stressors evaluated. The probability of damselfish occupation increased as coral colony size and complexity increased and coral growth rates were significantly lower in colonies with damselfish lawns (15.4 vs. 29.6 cm per year). Reduced growth and mortality of existing A. cervicornis populations may have a significant effect on population dynamics by potentially reducing important genetic diversity and the reproductive potential of depleted populations. On a positive note, however, the presence of resident damselfishes decreased predation by other corallivores, such as Coralliophila and Hermodice, and may offset some negative impacts caused by algal farming. While most negative impacts of damselfishes identified in this study affected large individual colonies and <50% of the A. cervicornis population along the FRT, the remaining wild staghorn population, along with the rapidly increasing restored populations, continue to fulfill important functional roles on coral reefs by providing essential habitat and refuge to other reef organisms. Although the effects of damselfish predation are, and will continue to be, pervasive, successful restoration efforts and strategic coral transplantation designs may help overcome damselfish damage by rapidly increasing A. cervicornis cover and abundance while also providing important information to educate future conservation and management decisions.     

Genetic Diversity and Local Connectivity in the Mediterranean Red Gorgonian Coral after Mass Mortality Events

Estimating the patterns of connectivity in marine taxa with planktonic dispersive stages is a challenging but crucial task because of its conservation implications. The red gorgonian Paramuricea clavata is a habitat forming species, characterized by short larval dispersal and high reproductive output, but low recruitment. In the recent past, the species was impacted by mass mortality events caused by increased water temperatures in summer. In the present study, we used 9 microsatellites to investigate the genetic structure and connectivity in the highly threatened populations from the Ligurian Sea (NW Mediterranean). No evidence for a recent bottleneck neither decreased genetic diversity in sites impacted by mass mortality events were found. Significant IBD pattern and high global F_ST confirmed low larval dispersal capability in the red gorgonian. The maximum dispersal distance was estimated at 20–60 km. Larval exchange between sites separated by hundreds of meters and between different depths was detected at each site, supporting the hypothesis that deeper subpopulations unaffected by surface warming peaks may provide larvae for shallower ones, enabling recovery after climatically induced mortality events.     

The reproductive seasonality and gametogenic cycle of Acropora cervicornis off Broward County, Florida, USA

Reproductive characters of the Caribbean reef-building coral Acropora cervicornis were investigated based on histological samples collected from April 2001 through October 2002. Oogenesis commenced in early to mid-October through November and spermatogenesis was initiated from January to March. The onset of gametogenesis was staggered, exhibiting up to approximately a 1-month delay within colonies. In the hermaphroditic polyps, the observed male-to-female gonad ratio was nearly 1:1 and ripe oocytes represented over 70% of the total gonadal volume. Fecundity estimates based on Stage IV ova ranged between 10.4 and 21.8 mm³ per square centimeter per year, comparable to A. cervicornis in Puerto Rico and other broadcasting Indo-Pacific Acropora. Fecundity estimates based on Stage III vitellogenic oocytes indicated statistically significant differences among study sites. Spawning in field conditions was observed in 2001, 2003, and 2004 from 2300 to 2330 h. Gamete release generally occurred synchronously between nights two and seven after the full moon of July or August. However in 2003, multiple, small-scale gamete release episodes occurred over more than one lunar cycle. This coincided with the full moon occurring early in the month of July. While prolific gamete production is reported in this study, low levels of recruitment have been reported for this species. Thus, the highly fragmenting A. cervicornis may rely heavily on asexual reproduction for population maintenance and expansion, and recovery after disturbance may be greatly protracted.     

Differential survival of nursery‐reared Acropora cervicornis outplants along the Florida reef tract

In recent decades, the Florida reef tract has lost over 95% of its coral cover. Although isolated coral assemblages persist, coral restoration programs are attempting to recover local coral populations. Listed as threatened under the Endangered Species Act, Acropora cervicornis is the most widely targeted coral species for restoration in Florida. Yet strategies are still maturing to enhance the survival of nursery‐reared outplants of A. cervicornis colonies on natural reefs. This study examined the survival of 22,634 A. cervicornis colonies raised in nurseries along the Florida reef tract and outplanted to six reef habitats in seven geographical subregions between 2012 and 2018. A Cox proportional hazards regression was used within a Bayesian framework to examine the effects of seven variables: (1) coral‐colony size at outplanting, (2) coral‐colony attachment method, (3) genotypic diversity of outplanted A. cervicornis clusters, (4) reef habitat, (5) geographical subregion, (6) latitude, and (7) the year of monitoring. The best models included coral‐colony size at outplanting, reef habitat, geographical subregion, and the year of monitoring. Survival was highest when colonies were larger than 15 cm (total linear extension), when outplanted to back‐reef and fore‐reef habitats, and when outplanted in Biscayne Bay and Broward–Miami subregions, in the higher latitudes of the Florida reef tract. This study points to several variables that influence the survival of outplanted A. cervicornis colonies and highlights a need to refine restoration strategies to help restore their population along the Florida reef tract.     

Small-scale mapping of indeterminate arborescent acroporid coral (Acropora cervicornis) patches

Coral Reefs - Western Atlantic populations of the staghorn coral Acropora cervicornis have drastically declined over the past few decades. Hence, interest in its ecology and spatial extent has...     

Staghorn tempestites in the Florida Keys

Thirty-one samples of transported Holocene Acropora cervicornis "sticks" sampled from carbonate sand tempestite accumulations at 19 sites along a 180-km-long stretch of the Florida reef tract were dated using the radiocarbon (¹⁴C) method. The "modern fossils" collected from just a few centimeters below the surface ranged in age from 0.5 to 6.4 ka. The majority lived between 3.5 and 5.5 ka. The time of transport and deposition is not known. There were no A. cervicornis samples centered around 4.5 ka. Acropora cervicornis is living on many Florida reefs, but the youngest tempestite sample was 500 years old. Two 500-year-long gaps in dated staghorn suggest that the documented decline in living A. cervicornis over the past 25 years may not be without precedent.     

Acropora cervicornis genet performance and symbiont identity throughout the restoration process

Coral Reefs - In the Caribbean, corals are commonly cultured in ocean-based nurseries and outplanted back to reefs for population enhancement. Intraspecific diversity in host and symbiont is an...     

Evaluating Genetic Diversity for the Conservation of the Threatened Galapagos Endemic Calandrinia galapagosa (Portulacaceae)

Calandrinia galapagosa (Portulacaceae) is a threatened plant endemic to San Cristobal Island, Galapagos. The species is threatened by goat herbivory: less than 1300 individuals remain in nine populations, three of which have been fenced for protection. It is not known whether these three populations are genetically representative of the species at large or whether the three distinct color morphs exhibited by the species represent different taxonomic units. We measured the frequency of 113 polymorphic amplified fragment length polymorphism markers in 189 specimens representing three different phenotypes from all nine populations to relate the genetic structure of the species to both its geological history and morphological variation. The analysis revealed high diversity within populations and low, but significant, differentiation between populations. In addition, no genetic diversification was observed across color morphs. We conclude that (1) regular gene flow has historically occurred between populations, and (2) individual color morphs are not separate taxa. We identify another population that should be fenced to ensure maximal protection of genetic variation. Our research serves as a case study of using population molecular genetics for optimizing protection strategies for rare plants in tropical archipelagoes affected by introduced herbivores.     

Examination of species boundaries in the Acropora cervicornis group (Scleractinia, cnidaria) using nuclear DNA sequence analyses

Although Acropora is the most species-rich genus of the scleractinian (stony) corals, only three species occur in the Caribbean: A. cervicornis, A. palmata and A. prolifera. Based on overall coral morphology, abundance and distribution patterns, it has been suggested that A. prolifera may be a hybrid between A. cervicornis and A. palmata. The species boundaries among these three morphospecies were examined using DNA sequence analyses of the nuclear Pax-C 46/47 intron and the ribosomal DNA Internal Transcribed Spacer (ITS1 and ITS2) and 5.8S regions. Moderate levels of sequence variability were observed in the ITS and 5.8S sequences (up to 5.2% overall sequence difference), but variability within species was as large as between species and all three species carried similar sequences. Since this is unlikely to represent a shared ancestral polymorphism, the data suggest that introgressive hybridization occurs among the three species. For the Pax-C intron, A. cervicornis and A. palmata had very distinct allele frequencies and A. cervicornis carried a unique allele at a frequency of 0.769 (although sequence differences between alleles were small). All A. prolifera colonies examined were heterozygous for the Pax-C intron, whereas heterozygosity was only 0.286 and 0.333 for A. cervicornis and A. palmata, respectively. These data support the hypothesis that A. prolifera is the product of hybridization between two species that have a different allelic composition for the Pax-C intron, i.e. A. cervicornis and A. palmata. We therefore suggest that A. prolifera is a hybrid between A. cervicornis and A. palmata, which backcrosses with the parental species at low frequency.     

Genomic patterns in Acropora cervicornis show extensive population structure and variable genetic diversity

Threatened Caribbean coral communities can benefit from high‐resolution genetic data used to inform management and conservation action. We use Genotyping by Sequencing (GBS) to investigate genetic patterns in the threatened coral, Acropora cervicornis, across the Florida Reef Tract (FRT) and the western Caribbean. Results show extensive population structure at regional scales and resolve previously unknown structure within the FRT. Different regions also exhibit up to threefold differences in genetic diversity (He), suggesting targeted management based on the goals and resources of each population is needed. Patterns of genetic diversity have a strong spatial component, and our results show Broward and the Lower Keys are among the most diverse populations in Florida. The genetic diversity of Caribbean staghorn coral is concentrated within populations and within individual reefs (AMOVA), highlighting the complex mosaic of population structure. This variance structure is similar over regional and local scales, which suggests that in situ nurseries are adequately capturing natural patterns of diversity, representing a resource that can replicate the average diversity of wild assemblages, serving to increase intraspecific diversity and potentially leading to improved biodiversity and ecosystem function. Results presented here can be translated into specific goals for the recovery of A. cervicornis, including active focus on low diversity areas, protection of high diversity and connectivity, and practical thresholds for responsible restoration.     

Mechanical properties,spectral vibrational response,and flow-field analysis of the aragonite skeleton of the staghorn coral (Acropora cervicornis)

Coral Reefs - Understanding the structural and mechanical properties of coral skeletons is important to assess their responses to natural and anthropogenic challenges and to predict the long-term...     

Coral recruitment patterns in the Florida Keys

This study examines scleractinian zooxanthellate coral recruitment patterns in the Florida Keys to determine if differences in density or community composition exist between regions. From July to September 2002, nine patch reefs, three in each of the upper, middle and lower Keys, were surveyed for coral recruits (colonies <5 cm in diameter) using randomly placed quadrats and transects. Coral recruits were enumerated, measured, and identified to genus. Fourteen genera of corals were observed across all sites and ranged from five to 13 per site. Densities ranged from 6.29 +/- 1.92 (mean +/- SE) to 39.08 +/- 4.53 recruits m(-2), and there were significant site and regional differences in recruit densities. The density of recruits in the upper Keys was significantly lower than in the middle and lower Keys. In addition, the upper Keys were less diverse and had a different recruit size-frequency distribution. The majority of recruits were non-massive scleractinian species that contribute relatively little to overall reef-building processes, a finding that is similar to previous studies. Fewer recruits of massive species were found in the upper Keys compared to the middle and lower Keys. The recruitment patterns of the reefs in the upper Keys could potentially hinder their ability to recover from stress and disturbances.