Reduced growth rate of Montastrea annularis following the 1987–1988 coral-bleaching event

Montastrea annularis, the major Caribbean reef building coral, was severely affected by the unprecedented 1987–1988 bleaching event. Most colonies on the fore reef were affected but few were bleached in the back reef. Skeletal growth rates of M. annularis populations were measured non-destructively in the field at Discovery Bay, Jamaica, from the peak of bleaching in Nov. 1987 until recovery was almost complete, in May 1988. Unbleached corals grew at normal rates. Partially bleached corals survived but skeletal growth ceased through this period.     

Transportation techniques for massive scleractinian corals

Transportation techniques for scleractinian corals have been described mainly for fragments and small colonies. As part of a recent study on captive sexual reproduction of the Caribbean species Montastrea annularis and Diploria strigosa, we transported relatively large (max. diameter of 21 cm), heavy (max. weight of 9,200 g) colonies of both species from Curaçao, Netherlands Antilles, to Rotterdam, The Netherlands. A new transportation technology was applied whereby the corals were transplanted to specially designed PVC crosses to provide stabilization during transport. In two transports (November 2001 and February 2002), 100 colonies were transported submerged, in a shipping time of >35 hr. The survival rate measured 2 weeks after transport was 100%. Four and 8 months after transport, respectively, two colonies of D. strigosa died without any obvious cause. In November 2002 we observed an outbreak of Dark Spots disease (DSD) affecting two‐thirds of the colonies of M. annularis. Although the colonies did not show any symptoms when they were collected, the disease most probably was transferred when the coral were transported from the field to the laboratory. The presented method is appropriate for transporting large, heavy corals–especially for scientific purposes. In general, species‐specific properties, colony size, and transportation time determine which transportation method should be applied. In the future, there may be a shift toward transports of fragments, coral larvae, and primary polyps to reduce collections in the field. Zoo Biol 23:165–176, 2004. © 2004 Wiley‐Liss, Inc.     

Seawater temperature and sublethal coral bleaching in Jamaica

Permanent study sites were established at 6 m, 12 m and 18 m on the West Fore Reef at Discovery Bay, Jamaica. Colonies of Montastrea annularis, Porites astreoides, Porites porites and Agaricia spp. were assessed for presence and extent of bleached tissue at two month intervals between October 1986 and September 1987. In 98% of all corals exhibiting a bleaching response, less than 25% of the colony appeared pale. In the remaining 2%, more than 25% of the tissue appeared pale. M. annularis, P. astreoides and Agaricia spp. showed a significant positive correlation between the percent of colonies exhibiting a partial bleaching response and seawater temperature. There was no significant difference in the percentage of colonies bleached between the three depths. M. annularis and Agaricia spp. exhibited a significantly higher percentage of colonies bleached than P. astreoides and P. porites. For M. annularis 15% of coral colonies studied showed 1–2 cm² randomly seattered patches of pale tissue which remained constant throughout the study. The partial bleaching patterns observed in this study were never lethal and are considered, in part, to be a response to seasonal variations in seawater temperature. Study location: Discovery Bay Marine Laboratory, P.O. Box 35, Discovery Bay, Jamaica, W. Indies     

Grazing dynamics on a Caribbean reef-building coral

Corals in certain Caribbean coral reef habitats are constantly grazed-on due to the territorial marking behavior of the stoplight parrotfish Sparisoma viride. We studied the grazing dynamics on the Caribbean reef-building coral Montastraea annularis. We transplanted colonies to algae-dominated reefs (Rosario Islands, Cartagena, Colombia), where they encountered higher grazing pressure. We counted grazed polyps every month throughout a year. Over the course of a year, 4,101 different grazed polyps were counted on lobe-like M. annularis transplants ( n =23). Grazing was evaluated on a monthly basis as the probabilities of all the possible transitions among four grazing categories (0%, >0–1%, >1–5%, >5% grazed tissue), uncovering a dynamic process. Higher transition probabilities were always between 0 and 1% (coral tissue grazed) grazing states, indicating that grazing did not usually exceed 1% per coral per month. The probability of remaining uninjured in a month was 0.19, 0.17 of a change from 0–1% grazing state, 0.31 of remaining at 1%, and of full recovery from 1% grazing was 0.16. More than one month was usually required for complete recovery ( P<<1) probably due to both steady grazing pressure and slow regeneration rates. Since the marking behavior of the parrotfish was not as common on other zones of the reef no comparison on the grazing among environments was possible. In spite of this, it is possible to have stable transplanted populations of corals such as M. annularis on algae-dominated Caribbean reef environments due to their tolerance to the natural grazing pressure.Communicated by: K. S. Sealey     

Parrotfish abundance and selective corallivory on a Belizean coral reef

Parrotfish are important members of coral reef communities because they consume macroalgae that would otherwise outcompete reef-building corals for space. However, some Caribbean parrotfish species also feed directly on live corals, and thus have the potential to negatively impact coral fitness and survival. This study investigates selective grazing by parrotfish on particular coral species, differences in grazing incidence among reef habitats and intraspecific discrimination among colonies of several coral species. We also investigate spatial and temporal patterns of parrotfish species abundance across habitats on the Belize barrier reef, and examine correlations between parrotfish abundance and grazing intensity across reef habitats. We found that members of the Montastraea annularis species complex, major builders of Caribbean reefs, were preferred targets of parrotfish grazing across all reef habitats, while M. cavernosa, Agaricia agaricites, Diploria strigosa, Porites astreoides and Porites porites were not preferred; Siderastrea siderea was preferentially grazed only in the spur and groove habitats. Parrotfish grazing preferences varied across habitats; M. annularis was grazed most often in shallow habitats, whereas M. franksi was consumed more at depth. Although it was not possible to directly observe parrotfish grazing on corals, we did find a positive correlation between Sparisoma aurofrenatum abundance and M. franksi grazing incidence across habitats. Finally, when we compared our results to parrotfish abundances measured by a previous study, we found that Sparisoma viride and Sp. aurofrenatum, two species known to be corallivorous, had increased abundances between 1982 and 2004. In light of escalating threats on Caribbean reef corals, it would be important for future studies to evaluate the impact of parrotfish corallivory on coral survival.     

Phenotypic plasticity in the reef corals Montastraea annularis (Ellis & Solander) and Siderastrea siderea (Ellis & Solander)

Mature colonies of Montastraea annularis (Ellis & Solander) and Siderastrea siderea (Ellis & Solander) were transplanted reciprocally between four reef environments near Discovery Bay, Jamaica. Multivariate analyses of variables describing corallite structures show that colonies of M. annularis change their skeletal morphology after transplantation from that characteristic of their original habitat to that characteristic of the environment to which they were moved. Control colonies of M. annularis, however, retain the morphology characteristic of their original habitat after manipulation. Many colonies of S. siderea similarly altered their morphology after transplantation, but some retained the morphology characteristic of their original habitat. Most control colonies of S. siderea did not change after manipulation. In general, control colonies of S. siderea show more morphologic variation between skeleton deposited before and after manipulation within colonies and also between colonies within populations, than did control colonies of M. annularis.These results indicate that, although M. annularis shows more plasticity than S. siderea. both species have highly plastic phenotypes. A large number of characters describing the architecture of corallites respond to environmental factors such as light intensity, sedimentation rate, water activity, and food availability. The most plastic characters in M. annularis describe coenosteal features and the thickness of thecae. The most plastic characters in S. siderea describe the thicknesses of thecae. septa, and columellae.This study suggests that phenotypic plasticity is an important species attribute in scieractinians and may be a significant mechanism in controlling the distribution and abundance of scleractinians on reefs.     

Sea surface temperature and the growth of the West Atlantic reef-building coral Montastraea annularis

Relationships were analyzed between sea surface temperature (SST) and annual growth characteristics (density, extension rate and calcification rate) of the Caribbean reef-building coral Montastraea annularis. Colonies were collected from 12 localities in the Gulf of Mexico and the Caribbean Sea. Two well-separated relationships were found, one for the Gulf of Mexico and the other for the Caribbean Sea. Calcification rate and skeletal density increased with increasing SST in both regions, while extension rate tended to decrease. Calcification rate increased ∼0.57 g cm⁻² year⁻¹ for each 1 °C increase in SST. Zero calcification was projected to occur at 23.7 °C in corals from the Gulf of Mexico and at 25.5 °C in corals from the Caribbean Sea. The 24 °C annual average SST isotherm marks the northern limit of distribution of M. annularis. Montastraea annularis populations of the Gulf of Mexico are isolated from those of the Caribbean Sea, and results indicate that corals from the Gulf of Mexico are adapted to growth at lower minimum and average annual SST. Corals from both the Gulf of Mexico and the Caribbean Sea, growing at lower SSTs and having lower calcification rates, extend their skeletons the same or more than those growing at higher SSTs. They achieve this by putting more of their calcification resources into extension and less into thickening, i.e., by sacrificing density.     

Nutrient enrichment can increase the severity of coral diseases

The prevalence and severity of marine diseases have increased over the last 20 years, significantly impacting a variety of foundation and keystone species. One explanation is that changes in the environment caused by human activities have impaired host resistance and/or have increased pathogen virulence. Here, we report evidence from field experiments that nutrient enrichment can significantly increase the severity of two important Caribbean coral epizootics: aspergillosis of the common gorgonian sea fan Gorgonia ventalina and yellow band disease of the reef‐building corals Montastraea annularis and M. franksii. Experimentally increasing nutrient concentrations by 2–5× nearly doubled host tissue loss caused by yellow band disease. In a separate experiment, nutrient enrichment significantly increased two measures of sea fan aspergillosis severity. Our results may help explain the conspicuous patchiness of coral disease severity, besides suggesting that minimizing nutrient pollution could be an important management tool for controlling coral epizootics.     

Patterns of association between Symbiodinium and members of the Montastraea annularis species complex on spatial scales ranging from within colonies to between geographic regions

Patterns of associations between coral colonies and the major clades of zooxanthellae can vary across scales ranging from individual colonies to widely separated geographic regions. This is exemplified in this study of the Montastraea annularis species complex from six sites on the Mesoamerican Reef, Belize and nine sites in the Bocas del Toro archipelago, Panama. Restriction fragment length polymorphism (RFLP) analysis of small subunit ribosomal DNA (SSU rDNA) was used to identify the zooxanthellae. In Belize (M. annularis), Symbiodinium B (79% of the colonies), Symbiodinium A, and Symbiodinium C were observed. In Panama (primarily M. franksi, but also M. annularis and M. faveolata), there was greater diversity and evenness with Symbiodinium A, B, C, C′ (a new symbiont) and D all being common in at least some host/habitat combinations. Non-metric multidimensional scaling ordinations showed that distribution patterns of symbionts across sites are best explained by enclosure (relative influence of open ocean vs. coastal water) and total suspended solids. Because members of clade D are known to be temperature resistant and Symbiodinium C′ was found in environments characterized by high sedimentation, these Panamanian reefs may have importance from a management perspective as reservoirs of corals better able to tolerate human impacts.     

The effects of prolonged “bleaching” on the tissue biomass and reproduction of the reef coral Montastrea annularis

Colonies of Montastrea annularis from Carysfort Reef, Florida, that remained bleached seven months after the 1987 Caribbean bleaching event were studied to determine the long term effects of bleaching on coral physiology. Two types of bleached colonies were found: colonies with low numbers of zooxanthellae with normal pigment content, and a colony with high densities of lowpigment zooxanthellae. In both types, the zooxanthellae had an abnormal distribution within polyp tissues: highest densities were observed in basal endoderm and in mesenteries where zooxanthellae are not normally found. Bleached corals had 30% less tissue carbon and 44% less tissue nitrogen biomass per skeletal surface area, but the same tissue C:N ratio as other colonies that either did not bleach (normal) or that bleached and regained their zooxanthellae (recovered). Bleached corals were not able to complete gametogenesis during the reproductive season following the bleaching, while recovered corals were able to follow a normal gametogenic cycle. It appears that bleached corals were able to survive the prolonged period without nutritional contribution from their zooxanthellae by consuming their own structural materials for maintenance, but then, did not have the resources necessary for reproduction. The recovered corals, on the other hand, must have regained their zooxanthellae soon after the bleaching event since neither their tissue biomass nor their ability to reproduce were impaired.     

<Emphasis Type="Italic">Symbiodinium</Emphasis> associations with diseased and healthy scleractinian corals

Despite recent advances in identifying the causative agents of disease in corals and understanding the impact of epizootics on reef communities, little is known regarding the interactions among diseases, corals, and their dinoflagellate endosymbionts (Symbiodinium spp.). Since the genotypes of both corals and their resident Symbiodinium contribute to colony-level phenotypes, such as thermotolerance, symbiont genotypes might also contribute to the resistance or susceptibility of coral colonies to disease. To explore this, Symbiodinium were identified using the internal transcribed spacer-2 region of ribosomal DNA from diseased and healthy tissues within individual coral colonies infected with black band disease (BB), dark spot syndrome (DSS), white plague disease (WP), or yellow blotch disease (YB) in the Florida Keys (USA) and the US Virgin Islands. Most of the diseased colonies sampled contained B1, B5a, or C1 (depending on host species), while apparently healthy colonies of the same coral species frequently hosted these types and/or additional symbiont diversity. No potentially “parasitic” Symbiodinium types, uniquely associated with diseased coral tissue, were detected. Within most individual colonies, the same dominant Symbiodinium type was detected in diseased and visually healthy tissues. These data indicate that specific Symbiodinium types are not correlated with the infected tissues of diseased colonies and that DSS and WP onset do not trigger symbiont shuffling within infected tissues. However, few diseased colonies contained clade D symbionts suggesting a negative correlation between hosting Symbiodinium clade D and disease incidence in scleractinian corals. Understanding the influence of Symbiodinium diversity on colony phenotypes may play a critical role in predicting disease resistance and susceptibility in scleractinian corals.     

Rapid phase-shift reversal on a Jamaican coral reef

Many Caribbean reefs have experienced a phase-shift in community structure, the principle features being a decline in coral cover and an increase in macroalgal biomass. However, one Jamaican reef—Dairy Bull on the north shore near Discovery Bay—is once again dominated by scleractinian corals and several key species have returned. Living coral cover at 6–8 m depth at Dairy Bull has doubled over the past 9 years and is now ~54%. The absolute cover of Acropora cervicornis was <1% in 1995, but increased to ~11% by January 2004. During this time the cover of macroalgae decreased by 90%, from 45 to 6%. We speculate that long-lived colonies of Montastraea annularis may have facilitated the recovery of this reef by providing structural refugia.     

Character release following extinction in a Caribbean reef coral species complex

Abstract The Pleistocene extinction of the widespread organ‐pipe Montastraea coral had measurable morphological and ecological effects on surviving lineages of the Montastraea“annularis” species complex. Extinction of the organ‐pipe Montastraea occurred after more than 500,000 years of dominance in the shallow‐water reef habitat of Barbados. Extinction resulted in a morphological shift of the columnar Montastraea lineage from thick to thin columns in modern reef environments. Pleistocene colonies of the columnar morphotype sympatric with organ‐pipe Montastraea showed greater column widths than those in allopatry. We subjected our data to a number of criteria for interpreting the morphological shift as character release following lifting of competitive pressure after extinction. The morphological differences do not appear to be due either to chance or to physical properties of the marine environment. Differential local extinction and recolonization of four members of the species complex did not occur on Barbados, so that the species coexisted and appear to have coevolved between more than 600,000 and 82,000 years ago. The morphological shift is related to coral growth form and growth rate, and thus reflects the acquisition of a primary resource in corals‐light. Character release occurred at the same oceanic Caribbean island (Barbados) where environments have fluctuated with similar variance throughout the period of coexistence. Not only has competition among living members of the Montastraea“annularis” species complex been convincingly demonstrated, but trends in relative abundance among fossil members of the species complex strongly suggest that a competitive hierarchy was operating during their Pleistocene coexistence on Barbados. We also observed an ecological analogue to character release on another Caribbean island, Curaçao. The distribution and abundance of living columnarM. annularis s.s. and massive M. faveolata from the leeward reef crest in Curaçao is greater now than in the Pleistocene, when organ‐pipe Montastraea dominated this shallow‐water reef habitat. Extinction of the faster growing, shallow‐water organ‐pipe Montastraea resulted in higher abundance of the columnar Montastraea lineage in shallow‐water habitats, where it shifted its morphology to one adapted to high light levels. The species extinction released surviving lineages from a competitive network that had resulted in lower rank abundance in the Pleistocene community and enhanced abundance of both columnar M. annularis s.s. and M. faveolata in modern communities. Full validation of our interpretation of character release must await experiments that demonstrate whether phenotypic differences between populations have a genetic basis. However, we believe the results of this study point to the important, yet heretofore neglected, role that biological interactions have played in the evolution of closely related reef coral species.     

Caribbean corals exhibit species-specific differences in competitive abilities with an aggressive encrusting alga,Ramicrusta textilis

Caribbean coral cover has decreased substantially in recent decades, with much of the live coral being replaced by macroalgae. Encrusting red algae in the genus Ramicrusta have become abundant throughout the region and have demonstrated widespread harm to corals by overgrowing living tissue, causing colony mortality, and impairing coral recruitment. In this research, Ramicrusta textilis was identified by morpho-anatomy and DNA sequencing from nine sites around St. Thomas, US Virgin Islands, and 3D photogrammetry was used to measure the rate of algal growth on stony corals. 3D models of individual coral colonies (five species plus controls, N = 72) competing with R. textilis revealed differential competitive abilities among taxa, with Siderastrea siderea being the only species capable of inhibiting overgrowth by the alga (mean linear algal growth − 1.1 mm yr⁻¹). Important reef building coral species such as Orbicella annularis and Orbicella faveolata were poor competitors (mean linear algal growth + 15 mm yr⁻¹ and + 7.7 mm yr⁻¹, respectively), indicating that the emergence of the alga could have significant impacts on Caribbean coral reef species diversity, community composition, and structural complexity.

     

Asymmetric conspecific sperm precedence in relation to spawning times in the Montastraea annularis species complex (Cnidaria: Scleractinia)

In broadcast spawners, prezygotic reproductive isolation depends on differences in the spatial and temporal patterns of gamete release and gametic incompatibility. Typically, gametic incompatibility is measured in no‐choice crosses, but conspecific sperm precedence (CSP) can prevent hybridization in gametes that are compatible in the absence of sperm competition. Broadcast spawning corals in the Montastraea annularis species complex spawn annually on the same few evenings. Montastraea franksi spawns an average of 110 min before M. annularis, with a minimum gap of approximately 40 min. Gametes are compatible in no‐choice heterospecific assays, but it is unknown whether eggs exhibit choice when in competition. Hybridization depends on either M. franksi eggs remaining unfertilized and in proximity to M. annularis when the latter species spawns or M. franksi sperm remaining in sufficient viable concentrations when M. annularis spawns. We found that the eggs of the early spawning M. franksi demonstrate strong CSP, whereas CSP appears to be lacking for M. annularis eggs. This study provides evidence of diverging gamete affinities between these recently separated species and suggests for the first time that selection may favour CSP in earlier spawning species when conspecific sperm is diluted and aged and is otherwise at a numeric and viability disadvantage with heterospecific sperm.     

Single‐copy gene markers isolated from the Caribbean coral,Montastraea annularis

We report the isolation of seven single‐copy nuclear DNA loci from the Caribbean reef‐building coral, Montastraea annularis. All loci are polymorphic at the nucleotide level, and three loci have readily screened restriction enzyme site polymorphisms that can help to rapidly assess population genetic structure. Use of these markers can provide baseline genetic information concerning the population dynamics of dominant stony corals and fuel the implementation and management of appropriate conservation strategies.     

Recovery of the coral Montastrea annularis in the Florida Keys after the 1987 Caribbean “bleaching event”

Many reef-building corals and other cnidarians lost photosynthetic pigments and symbiotic algae (zooxanthellae) during the coral bleaching event in the Caribbean in 1987. The Florida Reef Tract included some of the first documented cases, with widespread bleaching of the massive coral Montastrea annularis beginning in late August. Phototransects at Carysfort Reef showed discoloration of >90% of colonies of this species in March 1988 compared to 0% in July 1986; however no mortality was observed between 1986 and 1988. Samples of corals collected in February and June 1988 had zooxanthellae densities ranging from 0.1 in the most lightly colored corals, to 1.6x10⁶ cells/cm² in the darker corals. Minimum densities increased to 0.5x10⁶ cells/cm² by August 1989. Chlorophyll-a content of zooxanthellae and zooxanthellar mitotic indices were significantly higher in corals with lower densities of zooxanthellae, suggesting that zooxanthellar at low densities may be more nutrientsufficient than those in unbleached corals. Ash-free dry weight of coral tissue was positively correlated with zooxanthellae density at all sample times and was significantly lower in June 1988 compared to August 1989. Proteins and lipids per cm² were significantly higher in August 1989 than in February or June, 1988. Although recovery of zooxanthellae density and coral pigmentation to normal levels may occur in less than one year, regrowth of tissue biomass and energy stores lost during the period of low symbiont densities may take significantly longer.     

The genetic identity of dinoflagellate symbionts in Caribbean octocorals

Many cnidarians (e.g., corals, octocorals, sea anemones) maintain a symbiosis with dinoflagellates (zooxanthellae). Zooxanthellae are grouped into clades, with studies focusing on scleractinian corals. We characterized zooxanthellae in 35 species of Caribbean octocorals. Most Caribbean octocoral species (88.6%) hosted clade B zooxanthellae, 8.6% hosted clade C, and one species (2.9%) hosted clades B and C. Erythropodium caribaeorum harbored clade C and a unique RFLP pattern, which, when sequenced, fell within clade C. Five octocoral species displayed no zooxanthella cladal variation with depth. Nine of the ten octocoral species sampled throughout the Caribbean exhibited no regional zooxanthella cladal differences. The exception, Briareum asbestinum, had some colonies from the Dry Tortugas exhibiting the E. caribaeorum RFLP pattern while elsewhere hosting clade B. In the Caribbean, octocorals show more symbiont specificity at the cladal level than scleractinian corals. Both octocorals and scleractinian corals, however, exhibited taxonomic affinity between zooxanthella clade and host suborder.Communicated by R.C. Carpenter     

Water flow influences oxygen transport and photosynthetic efficiency in corals

Recent studies indicate that the incidence and persistence of damage from coral reef bleaching are often highest in areas of restricted water motion, and that resistance to and recovery from bleaching is increased by enhanced water motion. We examined the hypothesis that water motion increases the efflux of oxygen from coral tissue thereby reducing oxidative stress on the photosynthetic apparatus of endosymbiotic zooxanthellae. We experimentally exposed colonies of Montastrea annularis and Agaricia agaricites to manipulations of water flow, light intensity, and oxygen concentration in the field using a novel mini-flume. We measured photosynthetic efficiency using a pulse amplitude modulated fluorometer to test the short-term response of corals to our manipulations. Under normal oxygen concentrations, A. agaricites showed a significant 8% increase in photosynthetic efficiency from 0.238 (± 0.032) in still water to 0.256 (± 0.037) in 15 cm s⁻¹ flow, while M. annularis exhibited no detectable change. Under high-ambient oxygen concentrations, the observed effect of flow on A. agaricites was reversed: photosynthetic efficiencies showed a significant 11% decrease from 0.236 (± 0.056) in still water to 0.211 (± 0.048) in 15 cm s⁻¹ flow. These results support the hypothesis that water motion helps to remove oxygen from coral tissues during periods of maximal photosynthesis. Flow mitigation of oxidative stress may at least partially explain the increased incidence and severity of coral bleaching in low flow areas and observations of enhanced recovery in high-flow areas.