Simultaneous extension of both basic microstructural components in scleractinian coral skeleton during night and daytime,visualized by in situ 86Sr pulse labeling

Using in situ (12 h) pulse-labeling of scleractinian coral aragonitic skeleton with stable ⁸⁶Sr isotope, the diel pattern of skeletal extension was investigated in the massive Porites lobata species, grown at 5 m depth in the Gulf of Eilat. Several microstructural aspects of coral biomineralization were elucidated, among which the most significant is simultaneous extension of the two basic microstructural components Rapid Accretion Deposits (RAD; also called Centers of Calcification) and Thickening Deposits (TD; also called fibers), both at night and during daytime. Increased thickness of the ⁸⁶Sr-labeled growth-front in the RADs compared to the adjacent TDs revealed that in this species RADs extend on average twice as fast as TDs. At the level of the individual corallite, skeletal extension is spatially highly heterogeneous, with sporadic slowing or cessation depending on growth directions and skeletal structure morphology. Daytime photosynthesis by symbiotic dinoflagellates is widely acknowledged to substantially increase calcification rates at the colony and the corallite level in reef-building corals. However, in our study, the average night-time extension rate (visualized in three successive 12 h pulses) was similar to the average daytime extension (visualized in the initial 12 h pulse), in all growth directions and skeletal structures. This research provides a platform for further investigations into the temporal calibration of coral skeletal extension via cyclic growth increment deposition, which is a hallmark of coral biomineralization.     

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.     

Skeletal response of <Emphasis Type="Italic">Lophelia pertusa</Emphasis> (Scleractinia) to bioeroding sponge infestation visualised with micro-computed tomography

The skeleton morphology of the azooxanthellate cold-water coral Lophelia pertusa can be strongly influenced by invasive boring sponges that infest corallites in the still living part of the colony. Atypically swollen corallites of live Lophelia pertusa from the Galway Mound (Belgica Carbonate Mound Province, Porcupine Seabight, NE Atlantic), heavily excavated by boring organisms, have been examined with a wide range of non-destructive and destructive methods: micro-computed tomography, macro- and microscopic observations of the outer coral skeleton, longitudinal and transversal thin sections and SEM analyses of coral skeleton casts. As a result, three excavating sponge species have been distinguished within the coral skeleton: Alectona millari, Spiroxya heteroclita and Aka infesta. Furthermore, four main coral/sponge growth stages have been recognised: (1) cylindrical juvenile corallite/no sponge cavities; (2) flared juvenile corallite/linear sponge cavities (if present); (3) slightly swollen adult corallites/chambered oval sponge cavities; (4) very swollen adult corallites/widespread cavities. The inferred correlation between corallite morphology and boring sponge infestation has been detected in micro-computed tomography (micro-CT) images and confirmed in sponge trace casts and peculiar features of coral skeleton microstructure. Electronic supplementary material The online version of this article (doi:) contains supplementary material, which is available to authorised users.     

Ostracodes swallowed by Palaeozoic corals?

Middle Devonian heliolitids and favositids from Central Bohemia, belonging to Heliolites 'intermedius' LeMaitre and Favosites goldfussi Orbigny , incorporated ostracode shells within their living corallite structures. The ostracode shells were sealed in by skeletal tissue that was septal in origin (Heliolites) or they were roofed over by tabulae (Favosites). The foreign shell was near the axis of the polyp when trapped within the coral skeleton. Only ostracodes, not other rounded shells or sedimentary particles, were trapped in this way. Approximately one in 30 favositid corallites and one in 70 heliolitid corallites display this peculiar condition, where the ostracode shells seem to have been swallowed by the polyps. A probable scenario involves the injury of the mouth area and the trapping of the ostracodes. A high probability that the basal part of the polyp experienced a controlled penetration is the most striking part of the process. □ Favositids, heliolitids, ostracodes, coral growth violence, behavior, Middle Devonian, Bohemia.     

Skeletal microstructure of Galaxea fascicularis exsert septa: a high-resolution SEM study

The deposition of four crystal types at the growth surface of the septa of several color morphs of the coral Galaxea fascicularis was investigated over a 24-h period. Results suggest that nanocrystals, on denticles at the apices of exsert septa, may be the surface manifestation of centers of calcification. These crystals were also found on the septa of the axial corallite of Acropora formosa. The deposition of nanocrystals appears to be independent of diurnal rhythms. Internally and proximal to the septal apices, distinct clusters of polycrystalline fibers originate from centers of calcification and form fanlike fascicles. Upon these fascicles, acicular crystals grow and extend to form the visible fasciculi at the skeletal surface. Deposition of aragonitic fusiform crystals in both G. fascicularis and A. formosa occurs without diurnal rhythm. Nucleation of fusiform crystals appears to be independent of centers of calcification and may occur by secondary nucleation. Formation of semi-solid masses by fusiform crystals suggests that the crystals may play a structural role in septal extension. Lamellar crystals, which have not been reported as a component of scleractinian coral skeletons before, possess distinct layers of polyhedral plates, although these layers also do not appear to be associated with daily growth increments. The relationship of lamellar crystals to other components of the scleractinian coral skeleton and their involvement in skeletal growth is unknown.     

On the causes of density banding in skeletons of corals of the genus Montastraea

To obtain a reliable climate reconstruction from coral skeletons it is first necessary to understand the way these grow and incorporate information. Thickness of skeletal elements (exothecal and endothecal dissepiments, costae, septa, and theca-wall) as well as the spacing between exothecal and endothecal dissepiments of the four extant Atlantic species of Montastraea (M. annularis, M. faveolata, M. franksi and M. cavernosa) were measured through high and low density bands. Our results show that growth periodicity, controlled by the effect of temperature, is expressed in changes in thickness of costae and exothecal dissepiments in the four studied Montastraea species, with no changes in endothecal elements and theca-wall thickness which, in turn, has implications for research on inclusive records using these species. Spacing between both exothecal and endothecal dissepiments resulted without changes along the high and low density bands, and we found evidence that there is a rhythmical formation of these structures linked somehow to lunar cycles.     

Ontogeny of 'epithecal' and septal structures in scleractinian corals

The ontogenetic development of a solitary scleractinian coral, Flabellum distinctum Edwards & Haime, has been studied in serial thin section, with special attention being paid to epithecal nature in relation to septal growth. The term 'epitheca' has been confusingly used for two different skeletal structures: epitheca ( sensu stricto ) and marginotheca. The latter is here newly proposed. 'epitheca' is defined as a calcareous investment developed on the outside of other skeletal structures of a corallite. It can be distinguished from the marginotheca in section by lacking a dark line (calcification centre) and by being unrelated to the formation of septa. 'marginotheca' defines the outer margin of the main skeletal structures of a corallite. It has a dark line which functionally coincides with that of the eutheca. It is of primary origin, preceding formation of septa and provides the origin of the septa. The marginotheca is one of the more important and fundamental skeletal structures for coral classification.     

In vivo light-microscopic documentation for primary calcification processes in the hermatypic coral Stylophora pistillata

Skeletogenesis in the hermatypic coral Stylophora pistillata was studied by using the lateral skeleton preparative (LSP) assay, viz., a coral nubbin attached to a glass coverslip glued to the bottom of a Petri dish. Observations on tissue and skeletal growth were made by polarized microscopy and by using vital staining. The horizontal distal tissue edges developed thin transparent extensions of ectodermal and calicoblastic layers only. Four stages (I-IV) of skeletogenesis were observed at these edges, underneath the newly developed tissue. In stage I, a thin clear layer of coral tissue advanced 3–40 μm beyond the existing LSP peripheral zone, revealing no sign of spiculae deposition. At stage II, primary fusiform crystals (1 μm each) were deposited, forming a primary discontinuous skeletal front 5–30 μm away from the previously deposited skeleton. During stage III, needle-like crystals appeared, covering the primary fusiform crystals. Stage IV involved further lengthening of the needle-like crystals, a process that resulted in occlusion of the spaces between adjacent crystals. Calcification stages I-III developed within hours, whereas stage IV was completed in several days to weeks. Two basic skeletal structures, “scattered” and “laminar” skeletons, were formed, integrating the growth patterns of the needle-like crystals. High variation was recorded in the expression of the four calcification stages, either between different locations along a single LSP or between different preparations observed at the same diurnal time. All four skeletogenesis stages took place during both day and night periods, indicating that an intrinsic process controls S. pistillata calcification. This study was supported by the Israel Science Foundation (206/01 to J.E.), by the BARD, US-Israel Bi-National Agricultural Research and Development, by INCO-DEV project (REEFRES), and by CORALZOO, EC Collective Research project.     

Skeletal development inAcropora cervicornis

Scanning electron microscopy, field studies using dyes which become incorporated into the skeleton of living corals as time markers, and petrographic and mineralogic techniques were used to describe the diel pattern of calcium carbonate accretion in the extending axial corallite ofAcropora cervicornis. The axial corallite extends by the formation of randomly oriented fusiform crystals at the distal tip of the branch. Morphological and mineralogical characteristics suggest that these might be calcite crystals. They form a framework upon which needle-like aragonite crystals (initially small tufts) begin to grow. As the needles elongate, groups of them form well defined bundles, fasciculi, which compose the primary skeletal elements. There is a diel pattern in the deposition of the skeleton. At night (1800–0600 hours) the distal spines are pointed and composed primarily of fusiform crystals. During the day (0600–1800 hours) mineral accretion occurs on all surfaces of the skeleton, apparently by epitaxial growth on the aragonite needles of the fasciculi.     

Quantification of porosity in Acropora pulchra (Brook 1891) using X-ray micro-computed tomography techniques

Skeletal density and porosity characteristics are key parameters for investigations into scleractinian coral growth and for assessing the effects of a range of anthropogenic influences on coral reefs. Typically, skeletal density is measured by using planar X-rays of thin slabs cut from mound-shaped colonies or, for branching forms, by using methods based on Archimedean principles. This paper describes a novel non-destructive technique based on micro-computed tomography (micro-CT) to measure porosity of branching coral skeleton. This approach incorporates methods for segmenting internal and external portions of branch and for distinguishing between skeleton and air, whilst accounting for the effects of beam hardening. Measurements were obtained from colonies of branching Acropora pulchra collected across a reef-flat transect at King Reef, central nearshore Great Barrier Reef. The results show significant variation in porosity within and among branches sampled from individual colonies, but not within a reef-flat transect. Micro-CT techniques yield comparable results to traditional methods based on Archimedean principles, but offer advantages in their suitability for a wider range of coral specimens because of the non-destructive nature of the technique and in their more rigorous control of model parameters that can bias results.     

Skeletal form and growth in Acropora aspera (Dana) from the Pulau Seribu,Indonesia

Linear extension and calcium carbonate accretion were measured in the branching coral Acropora aspera (Dana) from shallow-water sites around Pulau Pari, Pulau Seribu, Indonesia, during both wet and dry monsoon periods. Skeletal density and corallite form were also monitored in specimens collected from sites, variously affected by wave energy resulting from the monsoonal influence. Although the reversing monsoon appeared to exert the greatest effect on skeleton growth (by influencing temperature and possibly number of “sun-hours”) wave energy was also shown to affect skeletal extension, skeletal accretion, and skeletal density. The scale of differences between growth rate measurements was greatest for weight of skeleton accreted between monsoon period (8-fold), followed by between site differences (maximum 3-fold during west monsoon) and finally between station differences (maximum 3-fold during west monsoon at an outer reef flat and reef edge station). Skeletal extension did not appear to be as sensitive to the reversing monsoon influence as skeletal accretion.     

On the nature and causes of luminescent lines and bands in coral skeletons: II. Contribution of skeletal crystals

Slices cut from skeletons of massive Porites display two types of luminescence when illuminated by ultra-violet (UV) light: (1) faint luminescent banding associated with the annual skeletal density banding pattern and (2) narrow lines of strong luminescence associated with monsoonal runoff of fresh water from nearby land. Barnes and Taylor [Barnes, D.J. Taylor, R.B. 2001a. On the nature and causes of luminescent lines and bands in coral skeletons. Coral Reefs 19, 221-230] showed how larger skeletal holes could give rise to increased luminescence—thus accounting for the link between skeletal density banding and faint luminescent banding. Work described here tests the notion that strongly luminescent lines are also regions of lower skeletal density. Experiments involving real and artificial coral skeletons indicated that likely changes in hole size in real skeletons cannot account for the amount of luminescence associated with luminescent lines. Larger particles (< 50 μm) of powdered skeleton from cut from luminescent lines were more luminescent than similar particles cut from adjacent less luminescent skeleton. However, very small particles (< 3 μm) from the two regions of skeleton showed no difference in luminescence. Since skeletal crystals would have been largely destroyed by powdering skeleton to very small particle sizes, most of the luminescence of strongly luminescent lines is probably associated with changed crystal size and packing, with changed crystal chemistry, or with a combination of these possibilities.     

Stable isotopic records of bleaching and endolithic algae blooms in the skeleton of the boulder forming coral Montastraea faveolata

Within boulder forming corals, fixation of dissolved inorganic carbon is performed by symbiotic dinoflagellates within the coral tissue and, to a lesser extent, endolithic algae within the coral skeleton. Endolithic algae produce distinctive green bands in the coral skeleton, and their origin may be related to periods of coral bleaching due to complete loss of dinoflagellate symbionts or “paling” in which symbiont populations are patchily reduced in coral tissue. Stable carbon isotopes were analyzed in coral skeletons across a known bleaching event and 12 blooms of endolithic algae to determine whether either of these types of changes in photosynthesis had a clear isotopic signature. Stable carbon isotopes tended to be enriched in the coral skeleton during the initiation of endolith blooms, consistent with enhanced photosynthesis by endoliths. In contrast, there were no consistent δ¹³C patterns directly associated with bleaching, suggesting that there is no unique isotopic signature of bleaching. On the other hand, isotopic values after bleaching were lighter 92% of the time when compared to the bleaching interval. This marked drop in skeletal δ¹³C may reflect increased kinetic fractionation and slow symbiont recolonization for several years after bleaching.     

Coral calcification: autoradiography of a scleractinian coral Galaxeafascicularis after incubation in 45Ca and 14C

 The uptake of ⁴⁵Ca and/or ¹⁴C by the skeleton of coral colonies has been commonly used to investigate the processes of calcification. This study reports the differential uptake of these tracers within different regions of the skeleton and tissues of individual corallites and polyps of the hermatypic coral Galaxea fascicularis. Incubation in ⁴⁵Ca in the light resulted in 80 percent of the ⁴⁵Ca taken up being deposited in the skeleton. Autoradiography of transverse and longitudinal slices of freeze-substituted polyps and corallites showed that in the light ⁴⁵Ca was incorporated into the exsert septa, the outside of the thecal walls of the corallite and the inner edges of the septa. Incorporation did not occur in the costae. The radioactivity in the skeleton was considerably greater than in the tissues. In the dark, or in the presence of the photosynthetic inhibitor Diuron, ⁴⁵Ca was taken up by the exsert septa and was patchily distributed in the corallite walls which suggests that it was not a result of isotopic exchange. The differential incorporation of ⁴⁵Ca onto the exsert septa was confirmed by scintillation counting. Negligible radioactivity remained in the extrathecal coelenteron after a brief 5 min rinse in non-radioactive seawater. Only 0.1% of ¹⁴C taken up in the light was incorporated into the skeleton and this was confirmed by autoradiography. In the presence of Diuron or in the dark, very little ¹⁴C was incorporated into tissues or skeleton and in autoradiographs was either not evident in the skeleton or the distribution was similar to that seen in autoradiographs of ⁴⁵Ca uptake. These results show that the deposition of ⁴⁵Ca, and therefore calcium carbonate, occurs at specific loci on the skeleton of a corallite. In the dark, deposition occurs specifically at the growing points of the corallite. Differential deposition of calcium carbonate within individual corallites has not been previously reported. Accepted: 27 May 1997     

The impact of seawater temperature on coral growth parameters of the colonial coral Cladocora caespitosa (Anthozoa, Scleractinia) in the eastern Adriatic Sea

The scleractinian coral Cladocora caespitosa deserves a special place among the major carbonate bioconstructors of the Mediterranean Sea. Annual coral skeleton growth, coral calcification, and skeleton density of the colonial coral C. caespitosa taken from 25 locations in the eastern Adriatic Sea were analyzed and compared with annual sea surface temperatures (SST). The growth rates of the coral C. caespitosa from the 25 stations in the Adriatic Sea ranged from 1.92 to 4.19?mm per year, with higher growth rates of the investigated corallites in the southern part of the Adriatic Sea. These growth rates are similar to those measured in other areas of the Mediterranean Sea. The correlation between coral growth and sea temperatures in the Adriatic Sea is seen as follows: An X-radiograph analysis of coral growth in C. caespitosa colonies that are over 60?years old showed that higher growth rates of this coral coincided with a warmer period in the Mediterranean Sea. A positive significant correlation exists between corallite growth rates and SST and coral calcification and SST. A negative correlation exists between coral density and SST. Coral growth rates also showed a correlation with higher eutrophication caused by nearby fish farms, along with a greater depth of the investigated colonies and high bottom currents.     

Seasonal growth bands in Famennian rugose coral Scruttonia kunthi and their environmental significance

Large colonies of rugose coral Scruttonia kunthi occurring in the upper Famennian of Sudetes (southern Poland) reveal distinct growth banding in their skeletons. They were investigated for internal structural characteristics and stable isotopic composition. The skeletal tissue consists of alternating light and dark bands which differ in thickness, density and morphology of structural elements, and in occurrence of corallite contraction and rejuvenescense. Darker parts with densely arranged thick skeletal elements are thin in comparison to lighter parts. In addition, they include frequently offsets and contraction of corallites. A couplet of dense and less dense bands is interpreted to represent most probably an annual cycle. The calculated growth rate for Scruttonia kunthi varied from 6 mm/yr to 12 mm/yr. Growth-band formation was influenced environmentally. Oxygen isotopic data provide an evidence that high-density bands were formed in the season of higher environmental stress, with relatively warmer temperatures and higher sedimentation rates. Carbon isotopic signatures are very uniform, and thus enigmatic. They indicate that at least growth rate of the skeleton and seawater temperature had no influence on the coral δ¹³C.     

Contrasting Light Spectra Constrain the Macro and Microstructures of Scleractinian Corals

The morphological plasticity of scleractinian corals can be influenced by numerous factors in their natural environment. However, it is difficult to identify in situ the relative influence of a single biotic or abiotic factor, due to potential interactions between them. Light is considered as a major factor affecting coral skeleton morphology, due to their symbiotic relation with photosynthetic zooxanthellae. Nonetheless, most studies addressing the importance of light on coral morphological plasticity have focused on photosynthetically active radiation (PAR) intensity, with the effect of light spectra remaining largely unknown. The present study evaluated how different light spectra affect the skeleton macro- and microstructures in two coral species (Acropora formosa sensu Veron (2000) and Stylophora pistillata) maintained under controlled laboratory conditions. We tested the effect of three light treatments with the same PAR but with a distinct spectral emission: 1) T5 fluorescent lamps with blue emission; 2) Light Emitting Diodes (LED) with predominantly blue emission; and 3) Light Emitting Plasma (LEP) with full spectra emission. To exclude potential bias generated by genetic variability, the experiment was performed with clonal fragments for both species. After 6 months of experiment, it was possible to detect in coral fragments of both species exposed to different light spectra significant differences in morphometry (e.g., distance among corallites, corallite diameter, and theca thickness), as well as in the organization of their skeleton microstructure. The variability found in the skeleton macro- and microstructures of clonal organisms points to the potential pitfalls associated with the exclusive use of morphometry on coral taxonomy. Moreover, the identification of a single factor influencing the morphology of coral skeletons is relevant for coral aquaculture and can allow the optimization of reef restoration efforts.     

IMAGING OF OXYGEN DYNAMICS WITHIN THE ENDOLITHIC ALGAL COMMUNITY OF THE MASSIVE CORAL PORITES LOBATA1

We used transparent planar oxygen optodes and a luminescence lifetime imaging system to map (at a pixel resolution of <200 μm) the two‐dimensional distribution of O₂ within the skeleton of a Porites lobata colony. The O₂ distribution was closely correlated to the distribution of the predominant endolithic microalga, Ostreobium quekettii Bornet et Flahault that formed a distinct green band inside the skeleton. Oxygen production followed the outline of the Ostreobium band, and photosynthetic O₂ production was detected at only 0.2 μmol photons m^?2 · s^?1, while saturation occurred at ～37 μmol photons m^?2 · s^?1. Oxygen levels varied from ～60% to 0% air saturation in the illuminated section of the coral skeleton in comparison to the darkened section. The O₂ production within the Ostreobium band was lower in the region below the upward facing surface of the coral and elevated on the sides. Oxygen consumption in darkness was also greatest within the Ostreobium zone, as well as in the white skeleton zone immediately below the corallites. The rate of O₂ depletion was not constant within zones and between zones, showing pronounced heterogeneity in endolithic respiration. When the coral was placed in darkness after a period of illumination, O₂ levels declined by 50% within 20 min and approached steady‐state after 40–50 min in darkness. Our study demonstrates the use of an important new tool in endolith photobiology and presents the first data of spatially resolved O₂ concentration and its correlation to the physical structures and specific zones responsible for O₂ production and consumption within the coral skeleton.     

Skeletal ontogeny in basal scleractinian micrabaciid corals

The skeletal ontogeny of the Micrabaciidae, one of two modern basal scleractinian lineages, is herein reconstructed based on serial micro‐computed tomography sections and scanning electron micrographs. Similar to other scleractinians, skeletal growth of micrabaciids starts from the simultaneous formation of six primary septa. New septa of consecutive cycles arise between septa of the preceding cycles from unique wedge‐shaped invaginations of the wall. The invagination of wall and formation of septa are accompanied by development of costae alternating in position with septa. During corallite growth, deepening invagination of the wall results in elevation of septa above the level of a horizontal base. The corallite wall is regularly perforated thus invaginated regions consist of pillars inclined downwardly and outwardly from the lower septal margins. Shortly after formation of septa (S2 and higher cycles) their upper margins bend and fuse with the neighboring members of a previous cycle, resulting in a unique septal pattern, formerly misinterpreted as “septal bifurcation.” Septa as in other Scleractinia are hexamerally arranged in cycles. However, starting from the quaternaries, septa within single cycles do not appear simultaneously but are inserted in pairs and successively flank the members of a preceding cycle, invariably starting from those in the outermost parts of the septal system. In each pair, the septum adjacent to older septa arises first (e.g., the quinaries between S2 and S4 before quinaries between S3 and S4). Unique features of micrabaciid skeletal ontogeny are congruent with their basal position in scleractinian phylogeny, which was previously supported by microstructural and molecular data. J. Morphol., 2013. © 2012 Wiley Periodicals, Inc.