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.     

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.     

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...     

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...     

Effects of light and elevated pCO2 on the growth and photochemical efficiency of Acropora cervicornis

The effects of light and elevated pCO₂ on the growth and photochemical efficiency of the critically endangered staghorn coral, Acropora cervicornis, were examined experimentally. Corals were subjected to high and low treatments of CO₂ and light in a fully crossed design and monitored using 3D scanning and buoyant weight methodologies. Calcification rates, linear extension, as well as colony surface area and volume of A. cervicornis were highly dependent on light intensity. At pCO₂ levels projected to occur by the end of the century from ocean acidification (OA), A. cervicornis exhibited depressed calcification, but no change in linear extension. Photochemical efficiency (F _v /F _m ) was higher at low light, but unaffected by CO₂. Amelioration of OA-depressed calcification under high-light treatments was not observed, and we suggest that the high-light intensity necessary to reach saturation of photosynthesis and calcification in A. cervicornis may limit the effectiveness of this potentially protective mechanism in this species. High CO₂ causes depressed skeletal density, but not linear extension, illustrating that the measurement of extension by itself is inadequate to detect CO₂ impacts. The skeletal integrity of A. cervicornis will be impaired by OA, which may further reduce the resilience of the already diminished populations of this endangered species.     

Restricted gene flow in the Caribbean staghorn coral Acropora cervicornis: implications for the recovery of endangered reefs

Coral reef conservation requires information about the distance over which healthy reefs can rescue damaged reefs through input of coral larvae. This information is desperately needed in the Caribbean where the 2 dominant shallow water corals Acropora cervicornis and Acropora palmata have suffered unprecedented declines. Here we compare the population genetic structure in the staghorn coral A. cervicornis across the greater Caribbean using DNA sequence data from 1 mitochondrial and 3 nuclear genes. Data from 160 individuals from 22 populations and 9 regions show that A. cervicornis exhibits significant population genetic structure across the greater Caribbean in both the mitochondrial (Phi(st) = 0.130) and nuclear data (Phi(st) = 0.067). The highest population structure was observed in the species' own, native mtDNA haplotypes (Phi(st) = 0.235). Introgressed alleles from A. palmata tempered higher population structure in A. cervicornis over regional scales but in some cases generated highly localized "introgression hot spots" and fine-scale genetic structure among reefs separated by as few as 2 km. These data show that larval dispersal over moderate or long distances (>500 km) is limited for this threatened species and in some cases locally limited as well. Thus, the endangered Caribbean staghorn corals require local source populations for their recovery and targeted conservation efforts over spatial scales much smaller than the hundreds to thousands of kilometers usually proposed for marine reserves.     

Skeletal development in Acropora cervicornis: I. Patterns of calcium carbonate accretion in the axial corallite

Summary Scanning electron microscopy and serial petrographic thin sections were used to investigate skeletal elongation and mineralization in the perforate coral, Acropora cervicornis. The axial corallite extends by the formation of randomly oriented fusiform crystals which are deposited on its distal edge. Aragonitic needle-like crystals grow in random directions from the surface of these fusiform crystals. Only those needle-like crystals growing toward the calicoblastic epithelium (i.e. crystals whose growth axis is perpendicular to the plane of the calicoblastic cell membrane) continue to elongate. Groups of these growing crystals join to form well-defined fasciculi which make up the primary skeletal elements comprising the septotheca. The resulting skeleton is highly porous with all surfaces covered by the continuous calicoblastic epithelium. This cell layer is separated by thin mesoglea from the flagellated gastrodermis which lines the highly ramified coelenteron. Porosity and permeability of the skeleton decrease with distance from the tip. Density correspondingly increases due to the addition of aragonite to the fasciculi whose boundaries become less distinct as channels fill with calcium carbonate.     

Larval settlement preferences and post-settlement survival of the threatened Caribbean corals Acropora palmata and A. cervicornis

The settlement specificity of two threatened Caribbean corals, Acropora palmata and A. cervicornis, was tested by measuring their rates of larval metamorphosis in response to crustose coralline algae (CCA) and other substrata. In the no-choice experiments, the coral larvae were placed in six treatments: filtered seawater (FSW), a fragment of biofilmed dead skeleton of A. palmata, or a fragment of one of four species of CCA (Hydrolithon boergesenii, Porolithon pachydermum, Paragoniolithon solubile, and Titanoderma prototypum). Within each CCA treatment, there were three different substrata on which to settle and metamorphose: (1) the CCA surface, (2) the rock under the CCA, or (3) the plastic dish. The 5-day-old larvae of both A. palmata and A. cervicornis had similar rates of total metamorphosis (all substrata combined) in every treatment (excluding FSW) even in the absence of CCA. However, there were differences in larval behavior among the CCA species since the larvae settled and metamorphosed on different substrata in the presence of different CCA species. In the no-choice experiments the larvae of both corals had higher rates of metamorphosis on the top surfaces of H. boergesenii and/or T. prototypum than on P. pachydermum. In the choice experiments, the coral larvae were offered two species of CCA in the same dish. When given a choice, both species of coral larvae had more settlement and metamorphosis on the surface of H. boergesenii or T. prototypum or clean rock than onto the surface of P. solubile. After 6 weeks in the field, transplanted A. palmata recruits had approximately 15% survival on both T. prototypum and H. boergesenii, but A. cervicornis recruits only survived on T. prototypum (13%). Some, but not all, CCA species facilitated the larval settlement and post-settlement survival of these two threatened corals, highlighting the importance of benthic community composition for successful coral recruitment.     

Microbiome signatures in Acropora cervicornis are associated with genotypic resistance to elevated nutrients and heat stress

Coral Reefs - The staghorn coral, Acropora cervicornis, was once abundant in the Caribbean, but now is listed as critically endangered. To recover A. cervicornis populations, restoration efforts...     

Utilization of Mucus from the Coral Acropora palmata by the Pathogen Serratia marcescens and by Environmental and Coral Commensal Bacteria

In recent years, diseases of corals caused by opportunistic pathogens have become widespread. How opportunistic pathogens establish on coral surfaces, interact with native microbiota, and cause disease is not yet clear. This study compared the utilization of coral mucus by coral-associated commensal bacteria (“Photobacterium mandapamensis” and Halomonas meridiana) and by opportunistic Serratia marcescens pathogens. S. marcescens PDL100 (a pathogen associated with white pox disease of Acroporid corals) grew to higher population densities on components of mucus from the host coral. In an in vitro coculture on mucus from Acropora palmata, S. marcescens PDL100 isolates outgrew coral isolates. The white pox pathogen did not differ from other bacteria in growth on mucus from a nonhost coral, Montastraea faveolata. The ability of S. marcescens to cause disease in acroporid corals may be due, at least in part, to the ability of strain PDL100 to build to higher population numbers within the mucus surface layer of its acroporid host. During growth on mucus from A. palmata, similar glycosidase activities were present in coral commensal bacteria, in S. marcescens PDL100, and in environmental and human isolates of S. marcescens. The temporal regulation of these activities during growth on mucus, however, was distinct in the isolates. During early stages of growth on mucus, enzymatic activities in S. marcescens PDL100 were most similar to those in coral commensals. After overnight incubation on mucus, enzymatic activities in a white pox pathogen were most similar to those in pathogenic Serratia strains isolated from human mucosal surfaces.Serratia is a gammaproteobacterium frequently isolated from waters, plants, and animals (7). Some isolates of Serratia are well-characterized symbionts of invertebrates. Serratia marcescens and Serratia liquefaciens have been identified as vertically transmitted symbionts of the sugar beet maggot (9). Serratia colonizes male and female reproductive tracts of the maggots, eggs, and pharyngeal filter. There, the bacteria are hypothesized to aid in metamorphosis by digesting chitinous puparial walls (9). In the gut of another insect, the diamondback moth, strains of S. marcescens appear to live as commensals capable of modestly (5 to 8%) increasing growth rates of the host (8). Serratia strains have also been isolated from feces and cloacal swabs from clinically normal captive birds, but not from organs or carcasses of sick or diseased animals housed within the same facility (3, 20). Serratia spp. have also been linked to diseases of invertebrate animals and their larvae (for reviews, see references 7, 15, and 21). To cause diseases in nematodes and flies, S. marcescens first colonizes the intestines, degrades cells of the alimentary tract and then spreads to other organs (14, 21). There are, however, exceptions to this mode of infection. Serratia entomophila, the causal agent of amber disease in grubs, grows within the alimentary tract of the animal to >10⁶ CFU. However, bacteria neither attach to nor colonize surfaces of the gut; rather, they adhere to gut contents (10) and cause the appearance of signs by producing the Sep toxin that inhibits accumulation of the insect''s digestive serine proteases and disrupts the cytoskeletal network (6). It appears, therefore, that various isolates of Serratia are capable of entering into a full range of interactions (from mutualistic to commensal to pathogenic) with their animal hosts (for reviews, see references 7, 15, and 21).A strain of S. marcescens, PDL100, was shown to be associated with white pox disease of the threatened Caribbean coral Acropora palmata (22, 27). White pox disease results in coral tissue necrosis, exposing carbonate skeleton at a rate of 2.5 cm² day⁻¹ (22). It is not yet clear how S. marcescens PDL100 colonizes and infects corals. It is likely that to cause disease, the pathogen first needs to colonize and establish within the coral surface mucus layer.The coral surface mucus layer contains polymers of mixed origin. Coral mucus is made in the mucocytes of the polyp, where the photosynthate produced by the coral symbiotic dinoflagellate Symbiodinium spp. is converted into polymers that are excreted onto the coral surface (for a review, see reference 2). A glycoprotein is the major component of coral mucus from both hard and soft corals (16, 17, 19). The composition of the glycoprotein differs among coral species (4, 17). The mucus polymer of Acropora formosa, for example, contains 36 to 38% of neutral sugars, 18 to 22% of amino sugars, and 19 to 30% of amino acids; lipids make up 4.2% of the polymer (17). In the mucus of A. formosa, the oligosaccharide decorations (two to four sugar residues long) are attached to the polypeptide backbone by an O-glycosidic link to serine or threonine through the carbon 1 of mannose (16). The glycoproteins from A. formosa and Pseudopterogorgia americana corals contain terminal arabinose residues linked by a β1→2 or β1→3 bond. In the mucus of acroporid corals, arabinose, N-acetyl-glucosamine, mannose, glucose, galactose, N-acetyl-galactosamine, and fucose were the major sugars; serine and threonine were the major amino acids (4, 17). The elucidation of the chemical structure of coral mucus is complicated by the fact that the mucus contains excretions of coral mucocytes, extracellular substances produced by the associated microbiota as well as oligomers that may result from the degradation of these polymers (for reviews, see references 2 and 24).In this study, we tested the hypothesis that S. marcescens PDL100 is capable of a more extensive utilization of A. palmata mucus than other environmental or pathogenic isolates of S. marcescens. This hypothesis is based on the recent discoveries that pathogenic and commensal host-associated bacteria differ in their patterns of carbon source utilization during growth on components of the mucus that lines host surfaces (5, 26). These different strategies of mucus utilization may allow pathogenic bacteria to outcompete native residents and establish within the host''s mucosa (5, 13, 26). To test this hypothesis, growth of the strain PDL100 on coral mucus and enzymatic activities induced during growth on mucus were assayed and compared to those of pathogenic and environmental isolates of S. marcescens and three native coral-associated bacteria.     

In-situ Effects of Eutrophication and Overfishing on Physiology and Bacterial Diversity of the Red Sea Coral Acropora hemprichii

Coral reefs of the Central Red Sea display a high degree of endemism, and are increasingly threatened by anthropogenic effects due to intense local coastal development measures. Overfishing and eutrophication are among the most significant local pressures on these reefs, but there is no information available about their potential effects on the associated microbial community. Therefore, we compared holobiont physiology and 16S-based bacterial communities of tissue and mucus of the hard coral Acropora hemprichii after 1 and 16 weeks of in-situ inorganic nutrient enrichment (via fertilizer diffusion) and/or herbivore exclusion (via caging) in an offshore reef of the Central Red Sea. Simulated eutrophication and/or overfishing treatments did not affect coral physiology with respect to coral respiration rates, chlorophyll a content, zooxanthellae abundance, or δ ¹⁵N isotopic signatures. The bacterial community of A. hemprichii was rich and uneven, and diversity increased over time in all treatments. While distinct bacterial species were identified as a consequence of eutrophication, overfishing, or both, two bacterial species that could be classified to the genus Endozoicomonas were consistently abundant and constituted two thirds of bacteria in the coral. Several nitrogen-fixing and denitrifying bacteria were found in the coral specimens that were exposed to experimentally increased nutrients. However, no particular bacterial species was consistently associated with the coral under a given treatment and the single effects of manipulated eutrophication and overfishing could not predict the combined effect. Our data underlines the importance of conducting field studies in a holobiont framework, taking both, physiological and molecular measures into account.