Deep down on a Caribbean reef: lower mesophotic depths harbor a specialized coral-endosymbiont community.

The composition, ecology and environmental conditions of mesophotic coral ecosystems near the lower limits of their bathymetric distributions remain poorly understood. Here we provide the first in-depth assessment of a lower mesophotic coral community (60-100 m) in the Southern Caribbean through visual submersible surveys, genotyping of coral host-endosymbiont assemblages, temperature monitoring and a growth experiment. The lower mesophotic zone harbored a specialized coral community consisting of predominantly Agaricia grahamae, Agaricia undata and a "deep-water" lineage of Madracis pharensis, with large colonies of these species observed close to their lower distribution limit of ~90 m depth. All three species associated with "deep-specialist" photosynthetic endosymbionts (Symbiodinium). Fragments of A. grahamae exhibited growth rates at 60 m similar to those observed for shallow Agaricia colonies (~2-3 cm yr(-1)), but showed bleaching and (partial) mortality when transplanted to 100 m. We propose that the strong reduction of temperature over depth (Δ5°C from 40 to 100 m depth) may play an important contributing role in determining lower depth limits of mesophotic coral communities in this region. Rather than a marginal extension of the reef slope, the lower mesophotic represents a specialized community, and as such warrants specific consideration from science and management.

Sharing the slope: depth partitioning of agariciid corals and associated Symbiodinium across shallow and mesophotic habitats (2-60 m) on a Caribbean reef.

BACKGROUND: Scleractinian corals and their algal endosymbionts (genus Symbiodinium) exhibit distinct bathymetric distributions on coral reefs. Yet, few studies have assessed the evolutionary context of these ecological distributions by exploring the genetic diversity of closely related coral species and their associated Symbiodinium over large depth ranges. Here we assess the distribution and genetic diversity of five agariciid coral species (Agaricia humilis, A. agaricites, A. lamarcki, A. grahamae, and Helioseris cucullata) and their algal endosymbionts (Symbiodinium) across a large depth gradient (2-60 m) covering shallow to mesophotic depths on a Caribbean reef. RESULTS: The five agariciid species exhibited distinct depth distributions, and dominant Symbiodinium associations were found to be species-specific, with each of the agariciid species harbouring a distinct ITS2-DGGE profile (except for a shared profile between A. lamarcki and A. grahamae). Only A. lamarcki harboured different Symbiodinium types across its depth distribution (i.e. exhibited symbiont zonation). Phylogenetic analysis (atp6) of the coral hosts demonstrated a division of the Agaricia genus into two major lineages that correspond to their bathymetric distribution ("shallow": A. humilis / A. agaricites and "deep": A. lamarcki / A. grahamae), highlighting the role of depth-related factors in the diversification of these congeneric agariciid species. The divergence between "shallow" and "deep" host species was reflected in the relatedness of the associated Symbiodinium (with A. lamarcki and A. grahamae sharing an identical Symbiodinium profile, and A. humilis and A. agaricites harbouring a related ITS2 sequence in their Symbiodinium profiles), corroborating the notion that brooding corals and their Symbiodinium are engaged in coevolutionary processes. CONCLUSIONS: Our findings support the hypothesis that the depth-related environmental gradient on reefs has played an important role in the diversification of the genus Agaricia and their associated Symbiodinium, resulting in a genetic segregation between coral host-symbiont communities at shallow and mesophotic depths.

Comparison between colony morphology and molecular phylogeny in the Caribbean scleractinian coral genus Madracis.

A major challenge in coral biology is to find the most adequate and phylogenetically informative characters that allow for distinction of closely related coral species. Therefore, data on corallite morphology and genetic data are often combined to increase phylogenetic resolution. In this study, we address the question to which degree genetic data and quantitative information on overall coral colony morphologies identify similar groupings within closely related morphospecies of the Caribbean coral genus Madracis. Such comparison of phylogenies based on colony morphology and genetic data will also provide insight into the degree to which genotype and phenotype overlap. We have measured morphological features of three closely related Caribbean coral species of the genus Madracis (M. formosa, M. decactis and M. carmabi). Morphological differences were then compared with phylogenies of the same species based on two nuclear DNA markers, i.e. ATPSα and SRP54. Our analysis showed that phylogenetic trees based on (macroscopical) morphological properties and phylogenetic trees based on DNA markers ATPSα and SRP54 are partially similar indicating that morphological characteristics at the colony level provide another axis, in addition to commonly used features such as corallite morphology and ecological information, to delineate genetically different coral species. We discuss this new method that allows systematic quantitative comparison between morphological characteristics of entire colonies and genetic data.

A comparison between coral colonies of the genus Madracis and simulated forms.

In addition to experimental studies, computational models provide valuable information about colony development in scleractinian corals. Using our simulation model, we show how environmental factors such as nutrient distribution and light availability affect growth patterns of coral colonies. To compare the simulated coral growth forms with those of real coral colonies, we quantitatively compared our modelling results with coral colonies of the morphologically variable Caribbean coral genus Madracis. Madracis species encompass a relatively large morphological variation in colony morphology and hence represent a suitable genus to compare, for the first time, simulated and real coral growth forms in three dimensions using a quantitative approach. This quantitative analysis of three-dimensional growth forms is based on a number of morphometric parameters (such as branch thickness, branch spacing, etc.). Our results show that simulated coral morphologies share several morphological features with real coral colonies (M. mirabilis, M. decactis, M. formosa and M. carmabi). A significant correlation was found between branch thickness and branch spacing for both real and simulated growth forms. Our present model is able to partly capture the morphological variation in closely related and morphologically variable coral species of the genus Madracis.

Morphogenesis of the branching reef coral Madracis mirabilis.

Understanding external deciding factors in growth and morphology of reef corals is essential to elucidate the role of corals in marine ecosystems, and to explain their susceptibility to pollution and global climate change. Here, we extend on a previously presented model for simulating the growth and form of a branching coral and we compare the simulated morphologies to three-dimensional (3D) images of the coral species Madracis mirabilis. Simulation experiments and isotope analyses of M. mirabilis skeletons indicate that external gradients of dissolved inorganic carbon (DIC) determine the morphogenesis of branching, phototrophic corals. In the simulations we use a first principle model of accretive growth based on local interactions between the polyps. The only species-specific information in the model is the average size of a polyp. From flow tank and simulation studies it is known that a relatively large stagnant and diffusion dominated region develops within a branching colony. We have used this information by assuming in our model that growth is entirely driven by a diffusion-limited process, where DIC supply represents the limiting factor. With such model constraints it is possible to generate morphologies that are virtually indistinguishable from the 3D images of the actual colonies.

Simulation and analysis of flow patterns around the scleractinian coral Madracis mirabilis (Duchassaing and Michelotti).

Three-dimensional morphologies of Madracis mirabilis were obtained using X-ray computed tomography scanning techniques. The morphologies were used to simulate the flow patterns around the colony. In the simulations, the thin-branching low-flow morph with a relatively larger branch-spacing was compared with the more compact high-flow morph of M. mirabilis. For both morphologies, the inside-colony flow velocities were computed for Reynolds numbers ranging from 154 to 3840. In the high-flow morph, it was found that in the range of investigated Reynolds numbers a stagnant region develops within the colony, whereas in the low-flow morph the stagnant region disappeared. Experiments done under natural conditions suggest that a morph is adapted to a certain external flow velocity and develops a stagnant region below a particular threshold for the external flow velocity. When the external flow velocity exceeds a certain threshold, which is characteristic for the growth form, the core velocity becomes equal to the external velocity. A potential application of a profile of core velocities for a range of Reynolds numbers for a certain morph is the prediction of the optimal external flow velocity for a certain morph, and this can be used to assess the state of the physical (palaeo-) environment.

Constancy and change in coral reef habitats along depth gradients at Curaçao.

The cover of the main components of the substratum, their spatial relations as well as mortality of the most important living component (Scleractinia) were studied at the leeward reef of Curaçao, Netherlands Antilles. We used a point intercept method to analyse cover as well as change in spatial arrangement in sets of photographs of the same 12 quadrats (3mx3m) taken in 1973 and 1978. Four quadrats were situated, along each of three transects, on the reef slope at depth of 10, 20, 30 and 40 m.Cover was very constant in both living and non-living components over the study period. There was a small but significant change in coral cover caused by a decrease at 10 and 20 m.Spatial arrangement of substratum components was subjected to changes equally large in living and non-living components. There was a significant difference in the magnitude of such changes between the shallower (10, 20 m) and the deeper quadrats (30, 40 m), the spatial rearrangement being much greater in the shallower habitats. In addition, there are important variations in the relative spatial change of the different coral species. The observed patterns of species that are more and less mobile through time, such as Agaricia agaricites and Montastrea spp. respectively, are related to life history phenomena such as recruitment and mortality.Mortality of corals was studied using interval (8-10 months) sets of photographs. We found mortality to be high in colonies (≧30 cm diameter) of A. agaricites and low in A. lamarcki and Montastrea spp. Mortality of coral colonies in this size class is often catastrophic in character.Our evidence indicates that community organization in deep coral reefs, both along the depth gradient and along the coast, is more influenced by spatial rearrangement of the substrata than has previously been recognized.

Predation of the sea urchin Diadema antillarum Philippi on living coral.

On the coral reefs of Curaçao and Bonaire (Netherlands Antilles) the sea urchin Diadema antillarum is a major coral predator. In areas with high coral cover, up to 8.2% of the Diadema population (with a density of 8.5 animals/m2) was feeding on living coral surfaces at night. Acropora species are the most heavily attacked corals.