R. P. M. Bak

Variation in symbiont distribution between closely related coral species over large depth ranges

Symbiotic algae in coral species distributed over a large depth range are confronted with major differences in light conditions. We studied the genetic variation of Symbiodinium in the coral genus Madracis over depth (5–40 m) and at two different colony surface positions. Using polymerase chain reaction–denaturing gradient gel electrophoresis ITS2 nuclear ribosomal DNA analyses, we consistently identified three symbiont genotypes with distributions that reveal patterns of host specificity and depth‐based zonation. ITS2 type B7 Symbiodinium is the generalist type, occurring in all zooxanthellate Madracis corals and at all depths. Type B13 is restricted to the shallow water specialist Madracis mirabilis. Type B15 is typical of deep reef environments and replaces B7 in the depth generalist Madracis pharensis. Contrasting with variation over depth, we found strong functional within‐colony uniformity in symbiont diversity. Relating symbiont distributions to measured physical factors (irradiance, light spectral distribution, temperature), suggests depth‐based ecological function and host specificity for Symbiodinium ITS2 types, even among closely related coral species.

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.

Genetic variation within Symbiodinium clade B from the coral genus Madracis in the Caribbean (Netherlands Antilles)

Abstract. The internal transcribed spacer (ITS) region was sequenced in symbiotic dinoflagellates (zooxanthellae) from five morphospecies in the genus Madracis. The phylogeny of the symbionts is congruent with a companion phylogeny of the coral host. Comparison with known clade B symbiont ITS types reveals that M. mirabilis contains the B13 symbiont and that the other morphospecies contain the B7 symbiont. Madracis formosa also contains a previously undescribed type. The B7 and B13 symbionts appear to be highly specific to morphospecies in the genus Madracis. The host specificity between the B13 symbionts and its coral host may be the result of co-evolution of the coral–symbiont association and suggests that the brooding species, M. mirabilis, is reproductively isolated. Microhabitat differentiation associated with light utilization independent of depth is discussed.

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.

The reproductive biology of closely related coral species: gametogenesis in Madracis from the southern Caribbean

Reproductive patterns were studied in closely related coral species of the genus Madracis on Curaçao, Netherlands Antilles. Gonadal development of six sympatric species was examined over a 13-month period. Reproductive differences among Madracis species are small. All species are hermaphroditic brooders and show similar patterns in gamete development. Timing of gamete maturation is positively correlated with seawater temperature in all species. Oocyte development typically begins in June and precedes the development of spermaries. Mature gametes, male and female, are present from August to November when seawater temperatures reach their yearly maximum. Developmental pathways for male and female gametes are identical among species. Interspecific differences exist in the number and size of oocytes. Our data indicates that differences in gametogenic development between closely related, but ecologically different subspecies are small or absent and do not necessarily match with species separations based on morphological criteria.

Semi-permeable species boundaries in the coral genus Madracis: Introgression in a brooding coral system

Introgressive hybridization is described in several phylogenetic studies of mass-spawning corals. However, the prevalence of this process among brooding coral species is unclear. We used a mitochondrial (mtDNA: nad5) and two nuclear (nDNA: ATPSα and SRP54) intron markers to explore species barriers in the coral genus Madracis and address the role of hybridization in brooding systems. Specimens of six Caribbean Madracis morphospecies were collected from 5 to 60 m depth at Buoy One, Curaçao, supplemented by samples from Aruba, Trinidad & Tobago and Bermuda. Polymerase chain reaction and denaturing gradient gel electrophoresis were coupled to detect distinct alleles within single colonies. The recurrent nDNA phylogenetic non-monophyly among taxa is only challenged by Madracis senaria, the single monophyletic species within the genus. nDNA AMOVAs indicated overall statistical divergence (0.1% significance level) among species but pairwise comparisons of genetic differentiation revealed some gene exchange between Madracis taxa. mtDNA sequences clustered in two main groups representing typical shallow and deep water Madracis species. Madracis pharensis shallow and deep colonies (with threshold at about 23-24 m) clustered in different mtDNA branches, together with their depth-sympatric congenerics. This divergence was repeated for the nDNA (ATPSα) suggestive of distinct M. pharensis depth populations. These matched the vertical distribution of the dinoflagellate symbionts hosted by M. pharensis, with Symbiodinium ITS2 type B7 in the shallows but type B15 in the deep habitats, suggesting symbiont-related disruptive selection. Recurrent non-monophyly of Madracis taxa and high levels of shared polymorphism reflected in ambiguous phylogenetic networks indicate that hybridization is likely to have played a role in the evolution of the genus. Using coalescent forward-in-time simulations, lineage sorting alone was rejected as an explanation to the SRP54 genetic variation contained in Madracis mirabilis and Madracis decactis (species with an old fossil record), showing that introgressive hybridization has taken place between these species, either directly or through the gene pool of other Madracis taxa. Madracis widespread non-monophyly and the absence of statistical divergence between some species suggest that introgressive hybridization plays an important role in the evolution of the genus. Different reproductive traits and symbiont signatures of taxa forming distinct genetic clusters also point to the same conclusion. We suggest that Madracis morphospecies remain recognizable because introgressive hybridization is non-pervasive and/or because disruptive selection is in action.

Depth-related variation in regeneration of artificial lesions in the Caribbean corals Porites astreoides and Stephanocoenia michelinii

Regeneration of artificial lesions was studied along a depth gradient from 5–35 m in the Caribbean corals Porites astreoides (brown morph) and Stephanocoenia michelinii (massive morph). During the first 3–4 weeks of the regeneration process tissue recovery in both coral species was higher in shallow water than in deep water colonies. After 7 weeks when the lesions were almost closed, however, shallow as well as deep water colonies had restored the damage to the same degree, showing that regeneration is a high priority process in coral ecology. The deep water colonies did not show signs of photoacclimatization. The zooxanthellae densities and the total chlorophyll concentration per algal cell in the coral tissue did not vary significantly with depth. Furthermore, there was no decrease with depth of the chlorophyll a/c2 ratio, which would have indicated photoacclimatization by means of a relative increase of chlorophyll c2 which is more efficient in using the blue light available at depth. One possibility which may explain the slower tissue recovery in deep water colonies during the first stage of the regeneration process, is a combination of the reduced light levels at depth and a lack of chlorophyll acclimatization in the deep water colonies.

Organic sedimentation and macrofauna as forcing factors in marine benthic nanofagellate communities.

We investigated how benthic nanoflagellate communities in marine sediments respond to sedimentation of organic material and to the presence of macrofaunal organisms in controlled boxcosms. An input of 24 g C m−2 resulted in a sharp increase in densities, from 93 to 477 × 103 flagellates cm−3 within 11 days. At the onset, this increase was paralleled by enhanced bacterial production and bacterial numbers. When bacterial production collapsed, flagellate ingestion rates, varying from 17 to 67 bact flag−1 h−1, were sufficient to control bacterial abundance. The presence of macrofauna accelerated the burst in flagellate densities. With macrofauna the same maximum densities were reached, but later densities dropped to relatively low levels. Macrofaunal bioturbation resulted in higher flagellate densities deeper in the sediment (up to 1200% at 3 cm and up to 460% at 6 cm deep).

Bacteria, auto- and heterotrophic nanoflagellates, and their relations in mixed, frontal and stratified waters of the North Sea☆

Abstract The horizontal and vertical distributions of bacteria and bacterial productivity were compared with nanoflagellate densities in the southern part of the central North Sea. Mixed, frontal and stratified waters were sampled in transects during summer 1988. High bacterial abundance, 2.7 to 4.5 ∗ 10 6 cells·cm −3 , distinguished coastal from offshore waters. Bacterial production and nanoflagellate densities were also high in the coastal zone but reached comparable or even higher values further offshore in frontal systems. We crossed two conspicuous fronts: the Frisian Frontal zone and a frontal zone along the northern slope of the Dogger Bank. These fronts were characterized by enhanced bacterial production and/or enhanced bacterial specific growth rates. In fronts as well as mixed waters, nanoflagellate densities covaried with bacterial specific growth rates and reached highest numbers in fronts, e.g. heterotrophic nanoflagellate densities peaked in the Frisian Front with 6000 to more than 10 000 cells·cm −3 . These high densities were accompanied by low bacterial abundances (0.45 ∗ 10 6 cells·cm −3 ) suggesting a regulation of bacterial numbers by heterotrophic nanoflagellates. A comparable pattern was found in the Dogger Bank front. Biomass of autotrophic nanoflagellates was significantly correlated with biomass of heterotrophic nanoflagellates. A maximum of nanoflagellates was present in the thermocline in stratified waters. The carbon distribution between bacteria and nanoflagellates over the water column was always dominated by flagellates, except in the coastal zone. Offshore, in mixed waters, bacterial biomass made up 30 to 51% of the bacterial plus auto/heterotrophic nanoflagellate biomass. In fronts and stratified waters the biomass of heterotrophic nanoflagellates alone exceeded bacterial biomass. Bacterial production amounted to a fraction of 3 to 31% of the primary production.

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.