Microstructure, growth banding and age determination of a primnoid gorgonian skeleton (Octocorallia) from the late Younger Dryas to earliest Holocene of the Bay of Biscay

A fossil primnoid gorgonian skeleton (Octocorallia) was recovered on the eastern Galician Massif in the Bay of Biscay (NE Atlantic) from 720 m water depth. The skeleton shows a growth banding of alternating Mg–calcitic and organic (gorgonin) increments in the inner part, surrounded by a ring of massive fibrous calcite. Three calcite-dominated cycles, bounded by thick organic layers, consist of five light-dark couplets of calcite and gorgonin. Two AMS-¹⁴C datings of the fossil skeleton give ages of 10,880 and 10,820 ± 45 ¹⁴C years before present (BP). We arrive at a calibrated age range of 11,829–10,072 cal. years BP (two σ), which comprises the late Younger Dryas to the earliest part of the Holocene. The cyclic calcitic–organic growth banding may be controlled by a constant rate of calcite secretion with a fluctuating rate of gorgonin production, possibly related to productivity cycles. The skeletal fabric change of alternating calcitic–organic increments to massive fibrous calcite may be the result of hydrographic changes during the deglaciation as reflected by preliminary stable isotope data. If this hypothesis proves to be correct, primnoid gorgonians are able to match with varying hydrodynamic conditions by changing their biomineralisation mode.     

Varying growth rates in bamboo corals: sclerochronology and radiocarbon dating of a mid-Holocene deep-water gorgonian skeleton (<Emphasis Type="Italic">Keratoisis</Emphasis> sp<Emphasis Type="Italic">.</Emphasis>: Octocorallia) from Chatham Rise (New Zealand)

A branched mid-Holocene bamboo coral skeleton of the isidid gorgonian genus Keratoisis (Octocorallia) recovered at southwestern Chatham Rise (New Zealand) from an average water depth of 680 m is described with respect to sclerochronology and age determination. Growth rates of the Mg-calcitic internodal increments were investigated by the counting of colour bands and radiocarbon dating. Growth banding is produced by varying orientations of crystal fan bundles towards the image plane. The skeleton shows three growth interruptions, which are documented in all branches. AMS ¹⁴C ages decrease from base to top of the trunk and from the central axes to the margins of the branches, documenting a simultaneous vertical and lateral growth. The data provide a maximum age of 3,975 ± 35 years BP, and a record spanning 240 ± 35 years. While calculated longitudinal growth rates amount to an average of 5 mm year⁻¹ during a 55-year record, average lateral linear extension rates of 0.4 mm year⁻¹ are an order of magnitude lower, still allowing for a seasonal to annual resolution of colour bands on a macroscopic scale and for a daily to monthly resolution on microscales of individual crystal generations to fascicle bundles. Hence, the isidid skeleton provides a high-resolution archive of paleoceanographic dynamics in deeper water masses. Concentric incremental accretion around the central axis in the early growth stages changed into a unilaterally asymmetric growth during late-stage evolution, probably triggered by the establishment of a stable system of unidirectional currents and nutrient flux. While colour band counts, related to the AMS ¹⁴C ages, support a seasonal to annual accretion of macroscopic growth bands in the inner concentric and complete outer parts of the skeleton, incremental growth rates at the condensed side are highly variable, as documented by hiatuses and unconformities. Thus the specimen proves that growth rates of bamboo corals may vary within individual skeletons and strongly deviate from the annual mode, hence showing implications on paleoceanographic proxy analyses.     

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.     

On the nature and causes of luminescent lines and bands in coral skeletons

Holes pushed into the surface of laboratory grade CaCO₃ powder reproduced visible and measurable luminescence similar to that seen and measured in coral skeletons. Heating such powder to 450 °C for 2 h did not destroy the luminescence although it did destroy luminescence in powdered coral skeleton. The effect in coral skeletal powder was probably due to carbonisation of contained organics because addition of small and increasing amounts of powdered charcoal to laboratory grade CaCO₃ increasingly attenuated luminescence. Luminescent lines and bands in coral skeletons have previously been ascribed to incorporation of humic substances. However, coating laboratory grade powder with humic acid attenuates rather than enhances luminescence. Ultra-violet lamps used to display coral luminescent lines and bands emit significant amounts of violet and blue visible light. Reflection of these visible wavelengths from the surface of laboratory grade CaCO₃ powder obscured luminescence of the powder. Multiple reflections within a hole in the powder resulted in absorption of the short wavelengths of visible light, including violet and blue light that would otherwise mask luminescence, and their re-emission at longer wavelengths. Luminescent bands in offshore corals were associated with the low-density regions of the annual density banding pattern. Luminescent lines in skeletons of inshore corals were in narrow regions of low-density skeleton, probably resulting from altered growth during periods of lowered salinity. Accepted: 20 April 2000     

Fine-Scale Skeletal Banding Can Distinguish Symbiotic from Asymbiotic Species among Modern and Fossil Scleractinian Corals

Understanding the evolution of scleractinian corals on geological timescales is key to predict how modern reef ecosystems will react to changing environmental conditions in the future. Important to such efforts has been the development of several skeleton-based criteria to distinguish between the two major ecological groups of scleractinians: zooxanthellates, which live in symbiosis with dinoflagellate algae, and azooxanthellates, which lack endosymbiotic dinoflagellates. Existing criteria are based on overall skeletal morphology and bio/geo-chemical indicators—none of them being particularly robust. Here we explore another skeletal feature, namely fine-scale growth banding, which differs between these two groups of corals. Using various ultra-structural imaging techniques (e.g., TEM, SEM, and NanoSIMS) we have characterized skeletal growth increments, composed of doublets of optically light and dark bands, in a broad selection of extant symbiotic and asymbiotic corals. Skeletons of zooxanthellate corals are characterized by regular growth banding, whereas in skeletons of azooxanthellate corals the growth banding is irregular. Importantly, the regularity of growth bands can be easily quantified with a coefficient of variation obtained by measuring bandwidths on SEM images of polished and etched skeletal surfaces of septa and/or walls. We find that this coefficient of variation (lower values indicate higher regularity) ranges from ~40 to ~90% in azooxanthellate corals and from ~5 to ~15% in symbiotic species. With more than 90% (28 out of 31) of the studied corals conforming to this microstructural criterion, it represents an easy and robust method to discriminate between zooxanthellate and azooxanthellate corals. This microstructural criterion has been applied to the exceptionally preserved skeleton of the Triassic (Norian, ca. 215 Ma) scleractinian Volzeia sp., which contains the first example of regular, fine-scale banding of thickening deposits in a fossil coral of this age. The regularity of its growth banding strongly suggests that the coral was symbiotic with zooxanthellates.     

Gender-related differences in the apparent timing of skeletal density bands in the reef-building coral Siderastrea siderea

Density banding in skeletons of reef-building corals is a valuable source of proxy environmental data. However, skeletal growth strategy has a significant impact on the apparent timing of density-band formation. Some corals employ a strategy where the tissue occupies previously formed skeleton during as the new band forms, which leads to differences between the actual and apparent band timing. To investigate this effect, we collected cores from female and male colonies of Siderastrea siderea and report tissue thicknesses and density-related growth parameters over a 17-yr interval. Correlating these results with monthly sea surface temperature (SST) shows that maximum skeletal density in the female coincides with low winter SSTs, whereas in the male, it coincides with high summer SSTs. Furthermore, maximum skeletal densities in the female coincide with peak Sr/Ca values, whereas in the male, they coincide with low Sr/Ca values. Both results indicate a 6-month difference in the apparent timing of density-band formation between genders. Examination of skeletal extension rates also show that the male has thicker tissue and extends faster, whereas the female has thinner tissue and a denser skeleton—but both calcify at the same rate. The correlation between extension and calcification, combined with the fact that density banding arises from thickening of the skeleton throughout the depth reached by the tissue layer, implies that S. siderea has the same growth strategy as massive Porites, investing its calcification resources into linear extension. In addition, differences in tissue thicknesses suggest that females offset the greater energy requirements of gamete production by generating less tissue, resulting in differences in the apparent timing of density-band formation. Such gender-related offsets may be common in other corals and require that environmental reconstructions be made from sexed colonies and that, in fossil corals where sex cannot be determined, reconstructions must be duplicated in different colonies.     

The skeletal structure of Desmophyllum cristagalli: the use of deep-water corals in sclerochronology

Skeletal banding has been found in the deep-water scleractinian coral Desmophyllum cristagalli , an important animal in studies of climate change. This banding pattern sheds light on skeletogenesis and suggests methods by which the record of climate change contained within the coral skeletons may be interpreted. A central wall built of trabeculae forms the interior of the septa and rings the theca. Lamellae form a sheath over the trabecular frame, showing continuity from thecal edge to septum. Skeletal bands are added by the tissue layer, which overlaps and seals the internal coral and upper portion of the outer theca. Truncated inner bands on the outer theca indicate a pattern of skeletal deposition and dissolution dependent on the presence or absence of the live tissue layer. A long-term record will be difficult to collect from D. cristagalli since lamellae are less than 10 μm thick and band position is unpredictable. Density banding in shallow-water coral skeletons has long been recognized as a valuable paleo-oceanographic tool, and deep-water corals are now being used to reconstruct deep-ocean environments. Pattern of skeletal growth must be carefully considered if deep-water corals are to be used as proxy climate recorders.     

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.     

Sex determination of adolescent skeletons using the distal humerus

Accurate determination of the sex of immature skeletal remains is difficult in the absence of DNA, due to the fact that most sexually dimorphic features of the human skeleton develop as secondary sex characteristics during adolescence. Methods of assessment of adult skeletons cannot reliably be applied to adolescent skeletons because of the transitional nature of the skeleton at puberty and the variability of the adolescent growth spurt. The purpose of this work was to evaluate the accuracy of Rogers's method of morphological sex determination using the distal humerus (Rogers: J Forensic Sci 44 ( 1999 ) 55–59) to assess the sex of adolescent skeletons. The sample consists of 7 documented adolescent skeletons from the Christ Church Spitalfields collection at the British Museum of Natural History and 35 from the Luis Lopes skeletal collection housed in the National History Museum (Museu Bocage) of the University of Lisbon, Portugal. Ages range from 11 to 20 years. The technique achieved an accuracy of 81% on the combined sample of 42. This method can be applied to adolescent skeletons once the trochlea begins fusing to the humeral diaphysis, which occurred by age 11 years in the test samples. Am J Phys Anthropol 2009. © 2009 Wiley‐Liss, Inc.     

Computerized tomography and skeletal density of coral skeletons

In this paper I describe and discuss the use of medical X-ray computerized tomography (CT) in the study of coral skeletons. CT generates X-ray images along freely chosen sections through the skeleton and offers, as well, the possibility of density measurements based on X-ray attenuation. This method has been applied to measure the skeletal density of the Caribbean reef-building coral Montastrea annularis, from Curaçao, Netherlands Antilles. The observed, non-linear increase of skeletal density with depth can be attributed to decreasing photo-synthetic rates with increasing water depth. A comparison with extension rate measurements shows the inverse relationship between extension rate and skeletal density. CT proves to be aquick and non-destructive method to reveal growth structures (density banding) since it measures skeletal density.     

Skeletal structures and habitats of Recent and fossil Acanthochaetetes (subclass Tetractinomorpha,Demospongiae, Porifera)

The investigation of the habitats, the spicular skeletons, and the structure and chemistry of the nonspicular high-Mg calcite skeletons of a fossil Acanthochaetetes from the Late Albian (Cretaceous) of Northern Spain and the extant Acanthochaetetes wellsi from Pacific reefs demonstrates an astonishing correspondence. The skeletons of both species are hemispherical or pyriform with the lower part containing an epitheca. They are built up of single calicles which are subdivided by tabulae. Spines protrude from the walls into the calicles. Scanning electron microscopy and thin sections reveal that the high-Mg calcite skeleton consists of two different microstructures: a irregular ssensu Wendt 1979 or microlamellar (sensu Cuif et al. 1979) and a completely irregular structure. AAS and EDAX analysis of the calcite skeletons produce roughly the same Mg and Sr contents. Tylostyle megascleres and aster-like microscleres are observed in the spicular skeletons of both species. The only difference between the two species is the greater variability of the microscleres in the extant species. Moreover, the fossil species incorporates the scleres in the non-spicular skeleton, while the extant species does not. Both species live/lived in the same niches of tropical reefs: the cryptic habitats of submarine caves in the reef core and the dimly lighted habitats of the deeper fore-reef.     

Decay of skeletal organic matrices and early diagenesis in coral skeletons

Due to its particular mode of growth, the coral skeleton provides a natural model for evaluating the successive stages of diagenesis in a still-living organism. The spatial distribution of skeletal organic matrices and their early diagenesis have been investigated in a scleractinian skeleton with in situ micron-scale analyses by Raman Microspectroscopy. Results indicate that the decay of the organic matrices occurs within a few years. We suggest that the gradual deterioration of the skeletal organic matrices is a key-mechanism driving earliest diagenesis in coral skeletons and represents the starting-point of the process of fossilization.     

A novel mechanism for iron incorporation into coral skeletons

Intertidal corals living in seawater with high concentrations of iron incorporate the metal into their skeletons. Cross-sections of the coral skeleton reveal orange-stained banding patterns reflecting periods of high availability of iron. The mechanism of metal incorporation involves deposition of iron compounds on to skeletal spines that are exposed as a result of temporary tissue retraction during periods of extreme stress. Subsequent tissue recovery and calcification trap the iron compounds which provide a visible environmental signature in the coral skeleton. This previously unrecognised mechanism has significant implications for the reconstruction of past environments from chemical analysis of annually-banded massive coral skeletons.     

Fluorescent and skeletal density banding in Porites lutea from Papua New Guinea and Indonesia

Shallow water Porites lutea corals were collected along two transects normal to mainland shorelines, parallel to gradients in water quality: one, 7 km long, near Motupore Island in South Papua New Guinea, the other, 70 km long, from Jakarta Bay along the Pulau Seribu chain in the Java Sea. The corals were slabbed and studies were made of skeletal density bands as revealed by X-ray photography and fluorescent bands as revealed by ultraviolet light. Water quality measurements and rain-fall data were assembled for the two areas and related to skeletal banding patterns. For both areas, with increasing distance form mainland there is a decrease in overall brightness of fluorescence in corals and an increase in the contrast between bright and dull fluorescent bands. Fluorescence is bright, but seasonal banding is obscure in corals within about 2 km of stream mouths at Motopure and about 5 km of the coast in Jakarta Bay; this suggests that, despite low freshwater run-off during dry seasons, there are sufficient organic compounds which cause fluorescence in coral skeletons, to swamp seasonal effects. During the wet seasons, deluges of freshwater consequent on mainland rainfall of greater than about 150 mm/ month extend at least 7 km offshore in the Motupore area and perhaps tens of kilometres into Java Sea, giving distinctive bright and dull fluorescent banding in off-shore corals. The fluorescent banding pattern within corals on the Motupore reefs is similar in most corals along the transect and it correlates well with the Port Moresby monthly rainfall data. This relationship suggests that the same body (or bodies) of freshwater affect all reefs of the area during the wet season. The fluorescent banding in Java Sea corals does not show a precise correlation with either mainland or island monthly rainfall data; indeed the pattern of fluorescent banding on Pulau Seribu can only be matched in corals from reefs less than about 25 km apart. This suggests that in this area discrete water bodies carrying the relevant organic acids for coral fluorescence affect the fringing reefs on the chain of islands. Comparisons of fluorescent and density banding have revealed that for these areas, in general, periods of high freshwater run-off are times of deposition of less dense skeleton in Porites lutea corals.     

Uranium in scleractinian coral skeletons

Accurate determinations have been made of the distribution of uranium in fresh and diagenetically altered coral skeletons occurring both naturally and grown under a variety of experimental conditions. Whereas live coral skeletons are homogeneous in uranium distribution, dead skeletons show heterogeneities relating to lithothamnioid algal encrustations and endolithic sponges. In the analyses of over 100 live coral skeletons, no zonal uranium distributions, described by previous workers, were found. In skeletons, free from organic material, uranium was found to exchange readily with the coral skeleton and/or to be precipitated along trabecular axes and skeletal margins. Bioeroded specimens contained higher uranium concentrations than freshly formed aragonite; they were similar to fossil coral skeletons used by previous researchers for uranium scrics dating.     

The ‘biomineralization toolkit’ and the origin of animal skeletons

Biomineralized skeletons are widespread in animals, and their origins can be traced to the latest Ediacaran or early Cambrian fossil record, in virtually all animal groups. The origin of animal skeletons is inextricably linked with the diversification of animal body plans and the dramatic changes in ecology and geosphere–biosphere interactions across the Ediacaran–Cambrian transition. This apparent independent acquisition of skeletons across diverse animal clades has been proposed to have been driven by co‐option of a conserved ancestral genetic toolkit in different lineages at the same time. This ‘biomineralization toolkit’ hypothesis makes predictions of the early evolution of the skeleton, predictions tested herein through a critical review of the evidence from both the fossil record and development of skeletons in extant organisms. Furthermore, the distribution of skeletons is here plotted against a time‐calibrated animal phylogeny, and the nature of the deep ancestors of biomineralizing animals interpolated using ancestral state reconstruction. All these lines of evidence point towards multiple instances of the evolution of biomineralization through the co‐option of an inherited organic skeleton and genetic toolkit followed by the stepwise acquisition of more complex skeletal tissues under tighter biological control. This not only supports the ‘biomineralization toolkit’ hypothesis but also provides a model for describing the evolution of complex biological systems across the Ediacaran–Cambrian transition.     

Electron backscatter diffraction (EBSD) as a tool for detection of coral diagenesis

Fine-scale structures of intact modern and fossil coralline skeletons were analysed to determine alteration to secondary cements and phases using electron backscatter diffraction (EBSD). EBSD analysis revealed secondary aragonite cements in endolithic borings in the modern skeleton and whole dissepiments of the fossil skeleton replaced by calcite, despite X-ray diffraction (XRD) bulk analysis of the general area suggesting only aragonite was present. Non-destructive, in situ screening of coral samples by EBSD analysis provides a valuable tool for assessing the extent of alteration and can determine which areas may produce more reliable climate proxy data. Communicated by Geology Editor Dr. Bernhard Riegl     

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.