Quantifying Spatial Genetic Structuring in Mesophotic Populations of the Precious Coral Corallium rubrum

While shallow water red coral populations have been overharvested in the past, nowadays, commercial harvesting shifted its pressure on mesophotic organisms. An understanding of red coral population structure, particularly larval dispersal patterns and connectivity among harvested populations is paramount to the viability of the species. In order to determine patterns of genetic spatial structuring of deep water Corallium rubrum populations, for the first time, colonies found between 58–118 m depth within the Tyrrhenian Sea were collected and analyzed. Ten microsatellite loci and two regions of mitochondrial DNA (mtMSH and mtC) were used to quantify patterns of genetic diversity within populations and to define population structuring at spatial scales from tens of metres to hundreds of kilometres. Microsatellites showed heterozygote deficiencies in all populations. Significant levels of genetic differentiation were observed at all investigated spatial scales, suggesting that populations are likely to be isolated. This differentiation may by the results of biological interactions, occurring within a small spatial scale and/or abiotic factors acting at a larger scale. Mitochondrial markers revealed significant genetic structuring at spatial scales greater then 100 km showing the occurrence of a barrier to gene flow between northern and southern Tyrrhenian populations. These findings provide support for the establishment of marine protected areas in the deep sea and off-shore reefs, in order to effectively maintain genetic diversity of mesophotic red coral populations.     

Harvesting Effects,Recovery Mechanisms,and Management Strategies for a Long-Lived and Structural Precious Coral

Overexploitation is a major threat for the integrity of marine ecosystems. Understanding the ecological consequences of different extractive practices and the mechanisms underlying the recovery of populations is essential to ensure sustainable management plans. Precious corals are long-lived structural invertebrates, historically overfished, and their conservation is currently a worldwide concern. However, the processes underlying their recovery are poorly known. Here, we examined harvesting effects and recovery mechanisms of red coral Corallium rubrum by analyzing long-term photographic series taken on two populations that were harvested. We compared the relative importance of reproduction and re-growth as drivers of resilience. Harvesting heavily impacted coral populations causing large decreases in biomass and strong size-class distribution shifts towards populations dominated by small colonies. At the end of the study (after 4 and 7 years) only partial recovery was observed. The observed general pattern of low recruitment and high mortality of new recruits demonstrated limited effects of reproduction on population recovery. Adversely, low mortality of partially harvested adults and a large proportion of colonies showing new branches highlighted the importance of re-growth in the recovery process. The demographic projections obtained through stochastic models confirmed that the recovery rates of C. rubrum can be strongly modulated depending on harvesting procedures. Thus, leaving the basal section of the colonies when harvesting to avoid total mortality largely enhances the resilience of C. rubrum populations and quickens their recovery. On the other hand, the high survival of harvested colonies and the significant biomass reduction indicated that abundance may not be an adequate metric to assess the conservation status of clonal organisms because it can underestimate harvesting effects. This study highlights the unsustainability of current harvesting practices of C. rubrum and provides urgently needed data to improve management practices that are still largely based on untested assumptions.     

Population dynamics and conservation biology of the over-exploited Mediterranean red coral

The main goal of ecologists is nowadays to foster habitat and species conservation. Life-history tables and Leslie-Lewis transition matrices of population growth can be powerful tools suitable for the study of age-structured over harvested and/or endangered species dynamics. Red coral (Corallium rubrum L 1758) is a modular anthozoan endemic to the Mediterranean Sea. This slow growing, long lived species has been harvested since ancient times. In the last decades harvesting pressure increased and the overall Mediterranean yield reduced by 23. Moreover, mass mortality (putatively-linked to global warming) recently affected some coastal populations of this species. Red coral populations are discrete genetic units, gonochoric, composed by several overlapping generations and provided of a discrete (annual) reproduction. A population of this precious octocoral was studied in detail and its static life table was compiled. In order to simulate the trends overtime of the population under different environmental conditions and fishing pressures, a discrete, non-linear model, based on Leslie-Lewis transition matrix, was applied to the demographic data. In this model a bell-shaped curve, based on experimental data, representing the dependence of recruitment on adult colonies density was included. On these bases the stability of the population under different density, reproduction and mortality figures was analysed and simulations of the population trends overtime were set out. Some simulations were also carried out applying to the studied population the mortality values measured during the anomalous mass mortality event which really affected some red coral populations in 1999. The population under study showed high stability and a strong resilience capability, surviving to a 61% reduction of density, to a 27.7% reduction of reproduction rate and to an unselective harvesting affecting 95% of the reproductive colonies.     

An adaptive management approach to an octocoral fishery based on the Beverton-Holt model

Coral reef species are frequently the focus of bio-prospecting, and when promising bioactive compounds are identified there is often a need for the development of responsible harvesting based on relatively limited data. The Caribbean gorgonian Pseudopterogorgia elisabethae has been harvested in the Bahamas for over a decade. Data on population age structure and growth rates in conjunction with harvest data provide an opportunity to compare fishery practices and outcomes to those suggested by a Beverton-Holt fishery model. The model suggests a minimum colony size limit of 7–9 years of age (21–28 cm height), which would allow each colony 2–4 years of reproduction prior to harvesting. The Beverton-Holt model assumes that colonies at or above the minimum size limit are completely removed. In the P. elisabethae fishery, colonies are partially clipped and can be repeatedly harvested. Linear growth of surviving colonies was up to 3 times that predicted for colonies that were not harvested and biomass increase was up to 9 times greater than that predicted for undisturbed colonies. The survival of harvested colonies and compensatory growth increases yield, and yields at sites that had previously been harvested were generally greater than predicted by the Beverton-Holt model. The model also assumes recruitment is independent of fishing intensity, but lower numbers of young colonies in the fished populations, compared to unfished populations, suggest possible negative effects of the harvest on reproduction. This suggests the need for longer intervals between harvests. Because it can be developed from data that can be collected at a single time, the Beverton-Holt model provides a rational starting point for regulating new fisheries where long-term characterizations of population dynamics are rarely available. However, an adaptive approach to the fishery requires the incorporation of reproductive data.     

Settlement and early survival of red coral on artificial substrates in different geographic areas: some clues for demography and restoration

The red coral Corallium rubrum (L 1758) is a long-lived, slow-growing gorgonian, endemic to Mediterranean rocky bottoms. Because of its high economic value, red coral has long been harvested, and most populations have been depleted. In the present study, 54 marble tiles were placed in June 2003 within red coral populations over 3 different geographic areas (Calafuria–Livorno and Elba MPA in Italy and Medes Islets MPA, in Spain), on vertical cliffs between 25 and 35 m. In each area 2 different sites were randomly selected. Tiles were subsequently sampled photographically. Between July and August 2003 red coral recruits settled on tiles in all the geographic areas and sites, exhibiting wide variability in their density. On the basis of a 2-factors nested ANOVA a significant variability between different sites at a few hundred metres distance occurred, indicating high variations in the recruitment process within the same red coral population. Mortality, measured in June 2004, widely varied between different geographic areas.     

Strategies for Gardening Denuded Coral Reef Areas: The Applicability of Using Different Types of Coral Material for Reef Restoration

Recreational and other human activities degrade coral reefs worldwide to a point where efficient restoration techniques are needed. Here we tested several strategies for gardening denuded reefs. The gardening concept consists of in situ or ex situ mariculture of coral recruits, followed by their transplantation into degraded reef sites. In situ nurseries were established in Eilat's (Northern Red Sea) shallow waters, sheltering three types of coral materials taken from the branching species Stylophora pistillata (small colonies, branch fragments, and spat) that were monitored for up to two years. Pruning more than 10% of donor colonies' branches increased mortality, and surviving colonies displayed reduced reproductive activity. Maricultured isolated branches, however, exceeded donor colony life span and reproductive activity and added 0.5–45% skeletal mass per year. Forty‐four percent of the small colonies survived after 1.5‐year mariculture, revealing average yearly growth of 75 ± 32%. Three months ex situ maintenance of coral spat (sexual recruits) prior to the in situ nursery phase increased survivorship. Within the next 1.5 years, they developed into colonies of 3–4 cm diameter. Nursery periods of 2 years, 4–5 years, and more than> 5 years have been estimated for small colonies, spat, and isolated branches, respectively. These and other results, including the possible use of nubbins (minute fragments the size of a single or few polyps), are discussed, revealing benefits and drawbacks for each material. In situ coral mariculture is an improved practice to the common but potentially harmful protocol of direct coral transplantation. It is suggested that reef gardening may be used as a key management tool in conservation and restoration of denuded reef areas. The gardening concept may be applicable for coral reefs worldwide through site‐specific considerations and the use of different local coral species.     

Coral recruitment and juvenile mortality as structuring factors for reef benthic communities in Biscayne National Park, USA

Coral communities of Biscayne National Park (BNP) on offshore linear bank-barrier reefs are depauperate of reef corals and have little topographic relief, while those on lagoonal patch reefs have greater coral cover and species richness despite presumably more stressful environmental regimes closer to shore. We hypothesized that differences in rates of coral recruitment and/or of coral survivorship were responsible for these differences in community structure. These processes were investigated by measuring: (1) juvenile and adult coral densities, and (2) size-frequency distributions of smaller coral size classes, at three pairs of bank- and patch-reefs distributed along the north-south range of coral reefs within the Park. In addition, small quadrats (0.25 m²) were censused for colonies <2 cm in size on three reefs (one offshore and one patch reef in the central park, and one intermediate reef at the southern end), and re-surveyed after 1 year. Density and size frequency data confirmed that large coral colonies were virtually absent from the offshore reefs, but showed that juvenile corals were common and had similar densities to those of adjacent bank and patch reefs. Large coral colonies were more common on inshore patch reefs, suggesting lower survivorship (higher mortality) of small and intermediate sized colonies on the offshore reefs. The more limited small-quadrat data showed similar survivorship rates and initial and final juvenile densities at all three sites, but a higher influx of new recruits to the patch reef site during the single annual study period. We consider the size-frequency data to be a better indicator of juvenile coral dynamics, since it is a more time-integrated measurement and was replicated at more sites. We conclude that lack of recruitment does not appear to explain the impoverished coral communities on offshore bank reefs in BNP. Instead, higher juvenile coral mortality appears to be a dominant factor structuring these communities. Accepted: 9 September 1999     

In Situ Coral Nurseries Serve as Genetic Repositories for Coral Reef Restoration after an Extreme Cold‐Water Event

During an unusual cold‐water event in January 2010, reefs along the Florida Reef Tract suffered extensive coral mortality, especially in shallow reef habitats in close proximity to shore and with connections to coastal bays. The threatened staghorn coral, Acropora cervicornis, is the focus of propagation and restoration activities in Florida and one of the species that exhibited high susceptibility to low temperatures. Complete mortality of wild staghorn colonies was documented at 42.9% of donor sites surveyed after the cold event. Remarkably, 72.7% of sites with complete A. cervicornis mortality had fragments surviving within in situ coral nurseries. Thus, coral nurseries served as repositories for genetic material that would have otherwise been completely lost from donor sites. The location of the coral nurseries at deeper habitats and distanced from shallow nearshore habitats that experienced extreme temperature conditions buffered the impacts of the cold‐water event and preserved essential local genotypes for future Acropora restoration activities.     

Spawning of the colonial coral <Emphasis Type="Italic">Cladocora caespitosa</Emphasis> (Anthozoa,Scleractinia) in the Southern Adriatic Sea

Data on sexual reproduction of scleractinian coral species living in temperate zones, particularly in the Mediterranean Sea, are quite scarce. This paper describes sexual reproduction of the colonial coral Cladocora caespitosa from Veliko jezero (Mljet Island) in the Adriatic Sea. Spawned orange eggs and white sperm bundles were observed on the coral bank of C. caespitosa two nights before the full moon (20 June 2005) coinciding with increasing water temperature and correlated with the lunar cycle. Spawning was observed during five nights, involving about 30% of the colonies from the coral bank. Different colonies on the bank released only one type of gamete during the reproductive period. The diameter of the sperm bundles ranged from 100 to 200 μm (average 163 μm; SD = 47.08), while the female gametes diameter ranged from 300 to 500 μm (average 416 μm; SD = 73.12).     

Coral mass- and split-spawning at a coastal and an offshore Venezuelan reefs,southern Caribbean

This study aimed to evaluate potential differences in coral spawning behavior between a fringing coastal reef and an offshore reef in the southern Caribbean. For this, scleractinian and gorgonian colonies (N = 324) of 21 species were mapped along eight transects, each 10-m long, at two study sites located in Morrocoy and Los Roques National Parks, Venezuela. Observations were made between 19:30 and 23:00 from August 23 to 30 and from September 26 to 30, 2002. Ninety one colonies belonging to six hard coral and seven octocoral species spawned or planulated during this period. We were unable to observe any signs of reproductive activity in 95 colonies of nine species different from those that reproduced. Despite the differences in environmental conditions between the two sites, we observed high synchrony in the spawning behavior of seven coral species common to both reefs. The most striking result was the ability of colonies of Montastraea faveolata and Eusmilia fastigiata to split spawn up to three times, either in consecutive nights or in different months.     

Sex, Symbiosis and Coral Reef Communities

SYNOPSIS. Questions about how today's corals and coral reefswill fare in a future that holds not only increasing directanthropogenic impacts, but also global change, cannot be satisfactorilyanswered if we do not understand the relations of corals andreef systems to today's environmental conditions. This paperdiscusses four aspects of modern reef biology: coral reproduction,coral population biology, the coral-zooxanthella symbiosis,and reef community ecology. Conclusions of this survey of currentknowledge are that complexities of cnidarian reproductive biology,and our rudimentary knowledge of reproductive patterns in reefcnidarians, make forecasting based on current knowledge uncertainat best; new discoveries about the coral algal symbiotic systemsuggest a possible mode of adjustment to environmental changethat warrants a strong research effort; coral communities ofthe future may well be unlike what we are familiar with today;and these new assemblages will be shaped by the interactionof novel environmental conditions and the characteristics ofindividual reef species.     

Into the depth of population genetics: pattern of structuring in mesophotic red coral populations

Deep-sea reef-building corals are among the most conspicuous invertebrates inhabiting the hard-bottom habitats worldwide and are particularly susceptible to human threats. The precious red coral (Corallium rubrum, L. 1758) has a wide bathymetric distribution, from shallow up to 800 m depth, and represents a key species in the Mediterranean mesophotic reefs. Several studies have investigated genetic variability in shallow-water red coral populations, while geographic patterns in mesophotic habitats are largely unknown. This study investigated genetic variability of C. rubrum populations dwelling between 55 and 120 m depth, from the Ligurian to the Ionian Sea along about 1500 km of coastline. A total of 18 deep rocky banks were sampled. Colonies were analyzed by means of a set of microsatellite loci and the putative control region of the mitochondrial DNA. Collected data were compared with previous studies. Both types of molecular markers showed high genetic similarity between populations within the northern (Ligurian Sea and Tuscan Archipelago) and the southern (Tyrrhenian and Ionian seas) study areas. Variability in habitat features between the sampling sites did not affect the genetic variability of the populations. Conversely, the patchy distribution of suitable habitats affected populations’ connectivity within and among deep coral banks. Based on these results and due to the emphasis on red coral protection in the Mediterranean Sea by international institutions, red coral could be promoted as a ‘focal species’ to develop management plans for the conservation of deep coralligenous reefs, a reservoir of marine biodiversity.     

Patterns of Gene Expression in a Scleractinian Coral Undergoing Natural Bleaching

Coral bleaching is a major threat to coral reefs worldwide and is predicted to intensify with increasing global temperature. This study represents the first investigation of gene expression in an Indo-Pacific coral species undergoing natural bleaching which involved the loss of algal symbionts. Quantitative real-time polymerase chain reaction experiments were conducted to select and evaluate coral internal control genes (ICGs), and to investigate selected coral genes of interest (GOIs) for changes in gene expression in nine colonies of the scleractinian coral Acropora millepora undergoing bleaching at Magnetic Island, Great Barrier Reef, Australia. Among the six ICGs tested, glyceraldehyde 3-phosphate dehydrogenase and the ribosomal protein genes S7 and L9 exhibited the most constant expression levels between samples from healthy-looking colonies and samples from the same colonies when severely bleached a year later. These ICGs were therefore utilised for normalisation of expression data for seven selected GOIs. Of the seven GOIs, homologues of catalase, C-type lectin and chromoprotein genes were significantly up-regulated as a result of bleaching by factors of 1.81, 1.46 and 1.61 (linear mixed models analysis of variance, P < 0.05), respectively. We present these genes as potential coral bleaching response genes. In contrast, three genes, including one putative ICG, showed highly variable levels of expression between coral colonies. Potential variation in microhabitat, gene function unrelated to the stress response and individualised stress responses may influence such differences between colonies and need to be better understood when designing and interpreting future studies of gene expression in natural coral populations.     

A new method for measuring growth and age in the precious red coral<Emphasis Type="Italic"> Corallium rubrum</Emphasis> (L.)

A new technique for aging red coral Corallium rubrum (L.) colonies based on staining the organic matrix found in the axial calcareous skeleton is presented and validated. This method provided clear-cut images of growth rings of red coral. To demonstrate their annual periodicity, two approaches have been used: (i) applying this technique to adult colonies of known age (more than 20 years old), and (ii) labeling colonies with calcein and allowing them to grow for 1 year. Results provided evidence of the annual periodicity of growth rings. This new method assesses colony age with an underestimate of true age by 3–4 years. The difference between estimated age and actual age could be attributed to the phase of initial growth during which rings are not formed. Colonies from different sites, depths, and habitats (n=33) were analyzed yielding preliminary data on longevity and mean growth rates in red coral. Colonies from shallow habitats (15–62 m) examined here with basal diameter of about 7 mm were at least 30–40 years old. Mean growth rate of basal diameter was 0.35±0.15 mm year^–1. Comparison with previous aging methods used for red coral resulted in considerable differences in estimations of age (about 10 years greater in this study) and growth rates (about four times lower). The application of this method to red coral will provide key data as a basis for developing management and conservation plans for this valuable species.Communicated by: H.R. Lasker     

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.     

Gametogenesis and fecundity of <Emphasis Type="Italic">Acropora tenella</Emphasis> (Brook 1892) in a mesophotic coral ecosystem in Okinawa,Japan

Mesophotic coral ecosystems (below 30–40 m depth) host a large diversity of zooxanthellate coral communities and may play an important role in the ecology and conservation of coral reefs. Investigating the reproductive biology of mesophotic corals is important to understand their life history traits. Despite an increase in research on mesophotic corals in the last decade, their reproductive biology is still poorly understood. Here, gametogenesis and fecundity of the Indo-Pacific mesophotic coral, Acropora tenella, were examined in an upper mesophotic reef (40 m depth) in Okinawa, Japan for the first time. Acropora tenella is a hermaphrodite with a single annual gametogenic cycle, and both oogenesis and spermatogenesis occurring for 11–12 and 5–6 months, respectively. Timing of spawning of this species was similar to other shallow Acropora spp. in the region. However, colonies had longer gametogenic cycles and less synchronous gamete maturation compared to shallow acroporids with spawning extended over consecutive months. Both the polyp fecundity (number of eggs per polyp) and gonad index (defined as the number of eggs per square centimeter) of A. tenella were lower than most acroporids. Our findings contribute to understanding of the life history of corals on mesophotic reefs and suggest that the reproductive biology of upper mesophotic corals is similar to that of shallow-water corals.     

First geo-marine survey of living cold-water Lophelia reefs in the Ionian Sea (Mediterranean basin)

Abstract Prosperous deep coral mounds including living colonies of Lophelia pertusa together with Madrepora oculata and Desmophyllum dianthus (= D. cristagalli) have been discovered in 2000, by fishery operations on the eastern side of the Ionian Sea. The living coral mounds are located between ca. 300 and 1,100 m on a gently dipping shelf off Apulia at Santa Maria di Leuca (SML), and characterized by a complex seabed topography. Side scan sonar, shallow high-resolution seismics and sampling indicate that these Lophelia-bearing coral mounds colonize quasi-indurate (firmground) Pleistocene sediment. At places live corals were found on Pleistocene coral-hardgrounds. The fauna associated with these Ionian modern coral mounds is less diversified than modern Eastern Atlantic counterparts. The core of living coral mounds colonies is at present located in 500–700 m and is tentatively suggested that their survival is mostly controlled by oceanographic factors. The SML coral banks represent so far a unique example of living Lophelia-bearing coral mounds in the Mediterranean basin.This revised version was published online in January 2005 with corrections to the author name and figure captions 4 and 5.     

Coral disease outbreak at Navassa,a remote Caribbean island

In November 2004, a high prevalence of coral disease was observed at several sites around Navassa, an uninhabited Caribbean island between Haiti and Jamaica. At least fifteen mounding and foliaceous scleractinian species were affected with ‘white disease’ signs. Coral disease incidence was observed to be absent in quantitative surveys in 2002, but in 2004 average prevalence (i.e., % of colonies) of active disease ranged up to 15% and an additional 19% prevalence of colonies with patterns of recent mortality consistent with disease. Large and/or Montastraea spp. colonies were disproportionately affected and the anticipated loss of these large, reef-building colonies will impact coral community structure. One or more potential factors may influence the initiation and persistence of disease outbreak conditions at Navassa including recent hurricane disturbance, regional patterns of increasing disease impact in deep or remote Caribbean reefs, or vectoring of disease by the corallivorous worm, Hermodice carunculata.