Coral reefs form the most diverse of all marine ecosystems on the Earth. Corals are among their main components and owe their bioconstructing abilities to a symbiosis with algae (Symbiodinium). The coral–algae symbiosis had been traced back to the Triassic (ca 240 Ma). Modern reef-building corals (Scleractinia) appeared after the Permian–Triassic crisis; in the Palaeozoic, some of the main reef constructors were extinct tabulate corals. The calcium carbonate secreted by extant photosymbiotic corals bears characteristic isotope (C and O) signatures. The analysis of tabulate corals belonging to four orders (Favositida, Heliolitida, Syringoporida and Auloporida) from Silurian to Permian strata of Europe and Africa shows these characteristic carbon and oxygen stable isotope signatures. The δ18O to δ13C ratios in recent photosymbiotic scleractinians are very similar to those of Palaeozoic tabulates, thus providing strong evidence of such symbioses as early as the Middle Silurian (ca 430 Ma). Corals in Palaeozoic reefs used the same cellular mechanisms for carbonate secretion as recent reefs, and thus contributed to reef formation.
Modern coral reefs are the largest biogenic constructions on the Earth and the richest of all marine ecosystems . The accumulation of great quantities of calcium carbonate is possible mainly as a result of the uptake of CO2 by symbiotic algae (Symbiodinium), and thus favours CaCO3 formation . Scleractinian corals, one of the main components of modern reefs, did not appear massively until after the Permian–Triassic crisis but single finds of scleractinian-like corals of uncertain affinities are known from the Early Palaeozoic [3,4] and Permian [5,6]. These early scleractinians were possibly non-photosymbiotic . Recent molecular studies show that scleractinian corals may also be linked with Palaeozoic scleractiniamorphs .
Bioconstructions with a significant contribution from corals first appeared in the Ordovician [1,8] and small build-ups were appearing until the Early Permian . These Palaeozoic reefs and build-ups were constructed by corals, sponges and microbialites [1,9,10], among them tabulates were important components of these environments [1,11]. Large quantities of CaCO3 in these structures allow us to formulate the working hypothesis that these corals also possessed symbiotic algae.
Apart from morphological similarities to recent photosymbiotic corals, such as massive coralla, colony integration and annual/seasonal growth banding [12,13], no evidence of algal symbiosis in tabulates has hitherto been presented. Conversely, Scrutton  advocated for the lack of photosymbiotic algae in tabulates stating that growth rates should differ between shallow and deep water environments, owing to differing light availability, as it is in recent scleractinians [14,15].
Besides skeletal morphology, scleractinian photosymbiotic corals differ from aposymbiotic equivalents by their characteristic way of fractionating oxygen and carbon stable isotopes [16,17]. This stable isotope fractionation in photosymbiotic corals is indirectly caused by photosynthesis of symbiotic algae. Both photosynthesis and calcification use inorganic carbon from the same pool. Symbiotic algae preferentially fix 12C, increasing the heavier isotope contents which are incorporated in the skeleton and the oxygen isotope contents remain in relation with temperature . Values of photosymbiotic and aposymbiotic coral isotopic compositions plotted on the δ18O to δ13C diagram form two separate clusters of points . In addition, aposymbiotic corals show a correlation between the content of oxygen and carbon isotopes, absent in photosymbiotic corals (zooxanthellates) [16–18].
Studies of stable isotopes have shown that many Triassic scleractinians possessed algal symbionts , but not all scleractinians were photosymbiotic, similar to modern corals . Tabulates had calcitic rather than aragonitic skeletons  and it is assumed here that if algae were involved in their secretion, then carbon and oxygen isotope fractionation should show similar stable isotope composition as photosymbiotic aragonitic scleractinians. The aim of this study is therefore to verify the hypothesis that tabulate corals possessed algal symbionts by analysing the stable isotope composition of their skeletons.
2. Systematic position and palaeoecology of tabulate corals
Tabulates were Palaeozoic organisms of clearly cnidarian affinities [20–22], despite some previous authors claiming their poriferan status ([23,24], see discussions in [25,26]), cnidarian affinities of tabulates were proved on the basis of fossilized polyps ([20–22], see discussion in ). Tabulates differ from recent scleractinians by their Bauplan: they are exclusively colonial, having small polyps (rarely exceeding 1 mm in diameter), numerous tabulae and poorly developed septal apparatus .
Photosymbiotic scleractinian corals have, as a rule, massive, highly integrated colonies, as do tabulate corals ; moreover, both groups have the facility for bioconstruction. Recent scleractinians, owing to their similar ecological niches and systematic affinities with tabulates appear to be good models for discussions on tabulate ecology.
Tabulates, with their bioconstructing abilities, were very common in Palaeozoic reefal environments [8,11,28,29]; however, they rarely formed the reef framework [1,9]. Besides reefal, they have also occurred in other environments. Knowing whether tabulate skeletons were secreted with the aid of algae is crucial for explaining the evolution of Palaeozoic reefs and build-ups, of which tabulates formed an appreciable part of the biodiversity and biomass.
3. Material and methods
In order to have a broad coverage of tabulate corals, I have chosen 23 species belonging to four (out of six) orders: Favositida (13 species), Syringoporida (four species), Heliolitida (one species) and Auloporida (one species), and from a substantial time span covering about 140 Ma (Middle Silurian to Early Permian). These specimens come from various sites of Europe (Boulonnais, Holy Cross Mountains, Podolia, Gotland, Spitsbergen and erratic boulders of Scandinavian origin collected in Poland) and Africa (Anti-Atlas) and examples are shown in figure 1. A full list of analysed corals is given in the electronic supplementary material.
The carbon and oxygen stable isotope analyses were performed at the Institute of Geological Sciences, Polish Academy of Sciences (Warsaw); data on methodology and repository are given in the electronic supplementary material.
In order to exclude the influence of diagenesis in selected cases (specimens from Skaly, Grzegorzowice, Kowala, Dębnik Anticline, Irevik, Sokol and Boulonnais), isotopic ratios of concurring faunas (brachiopods, crinoids and rugose corals) and matrix were compared to the isotopic composition of tabulates. Moreover, conodonts from the Kowala section show very low Colour Alteration Index , which suggests a very low diagenesis level in specimens from the Kowala section and quarry.
Analysed tabulate corals show δ13C values ranging from −2.93 to 5.33‰ and δ18O from −8.50 to −1.90‰, with mean values of δ13C 0.61 ± 2.066‰ and δ18O −5.71 ± 1.621‰ (the exact values are given in table 1). The ratios between isotopes were plotted on the δ18O/δ13C diagram (figure 2); a warm non-zooxanthellate line (WNL), showing a correlation between carbon and oxygen isotope ratios in recent aposymbiotic (non-zooxanthellate) corals and separating photosymbiotic from aposymbiotic corals [16,17] has been added to facilitate interpretation. Points on the diagram obtained from tabulates are scattered, and no trend is visible; correlation between carbon and oxygen contents is non-significant (Pearson = 0.248, p = 0.11).
The δ18O and δ13C values of tabulate coral skeletons show striking similarities to those of modern and fossil photosymbiotic scleractinians . All these ratios are located below the WNL. Isotope ratios of all recent aposymbiotic corals are placed above this line and isotope ratios of Jurassic scleractinians considered to be aposymbiotic are placed immediately below this line, as marked in figure 2 . Points on the diagram obtained from tabulates are scattered and such a lack of correlation is also characteristic of modern photosymbiotic corals; those without algal symbionts show strong correlation between these two stable isotopes [16,17].
Diagenesis can considerably change isotopic composition of carbonates [31–33] and recent aragonitic scleractinian corals can easily undergo diagenetic changes [34,35]. Diagenesis can readily be excluded as a factor causing isotope ratios observed in the investigated material. Tabulates, owing to their primarily calcitic skeletons may be much more resistant to diagenetic changes and massive skeletal elements of tabulate corals may have been more permeable to diagenesis. Large variations in stable isotopic composition within the skeletons (e.g. in Yavorskia paszkowskii δ13C are 0.63 and −0.28‰ for the same corallum) suggest that there was no diagenetic erasure of the primary isotope composition.
Analysed specimens come from different geographical locations, often very distant from each other. They also come from different geological structural regions, thus having different tectonic and diagenetic histories. Analysed specimens are of different ages, hence having dissimilar levels of overall diagenetic processes. For these reasons, it is unlikely to have specimens showing similar isotopic ratios despite huge variations in diagenetic history. Finally, analysed specimens show isotopic ratios different from concurring faunas and matrix.
The single corallum of the Famennian Yavorskia paszkowskii has carbon and oxygen contents similar to those of aposymbiotic corals (see the electronic supplementary material). These values are placed close to the WNL (filled circles in figure 2). This specimen comes from deeper environments (non-reefal), probably below the photic zone, where tabulate corals generally did not occur . This species has large corallite diameters similar to modern aposymbiotic scleractinians. Hence, it is possible that this coral actually lacked symbiotic algae. Specimens from the Frasnian shallow water beds of the same locality show stable isotope ratios characteristic of photosymbiotic scleractinians (stars in figure 2).
Tabulates have morphological characteristics consistent with the concept of algal symbiosis. Similar to modern photosymbiotic scleractinians, they show high levels of colony integration [12,37]. Growth rates in tabulates are diversified and have been used as an argument against photosymbiosis in this systematic group . Some heliolitids had low growth rates that did not change in relation to bathymetry , e.g. Heliolites megastoma from the Silurian of Wales had annual growth rates from 2.8 mm to 4.2 mm per year regardless of depth , which is similar to a recent aposymbiotic Balanophyllia regia, growing about 2 mm per year . Conversely, Silurian favositids had growth rates significantly higher (Paleofavosites: 5–14 mm per year, Favosites 8–18 mm per year) . Annual growth increments in Permian tabulates may be close to 10 mm (e.g. Syringopora quadriserialis, Roemeripora wimani) or again, reach 20 mm per year (Fuchungopora arctica) . These values are close to modern photosymbiotic scleractinians, e.g. Montastaea annularis has a growth rate of 11 mm y–1 in shallow waters [14,40].
Annual (seasonal) internal growth banding occurs commonly in tabulate corals [41–43]. As this phenomenon is often considered to be related to photosymbiosis [12,44], it therefore supports the results inferred from stable isotope analysis. Growth bands may occur in non-photosymbiotic corals but they are very thin, discontinuous and usually not visible to the naked eye , therefore very different from those of tabulates. The analysis of growth rates in alveolitid tabulates  has shown that individuals within the colony often have varying growth rates and this might have been caused by significant differences in distribution of algae in soft tissues . In scleractinians, such differences even within individuals may be important , thus possibly resulting in discrepancies in carbonate secretion. Inferences from growth morphology combined with isotopic signals are considered as reliable in photosymbiosis recognition .
Besides tabulate corals, many other Palaeozoic bioconstructing organisms are considered to be photosymbiotic. Calcifying sponges are often considered to be photosymbiotic [49–51]. Stromatoporoids commonly occurring in the same environments as tabulates show seasonal growth banding  and large sizes  that may indicate photosymbiosis. Conversely, rugose corals are considered to be aposymbiotic , but on the other hand stable isotopic data suggest otherwise [53,54].
Recent algal symbionts, mostly belonging to the genus Symbiodinium (Dinoflagellata), probably originated in the Early Eocene  or earlier, near the Cretaceous–Palaeogene boundary . Early photosymbionts may also have been dinoflagellates, as they were probably already abundant in Ordovician and Silurian seas [57–59], but C and O isotopic signals cannot give precise information on the systematic affinities of the Palaeozoic algal symbionts.
Carbon and oxygen stable isotope analysis shows that photosymbiosis of tabulate corals and algae started as early as in the Middle Silurian and continued to the Early Permian. Tabulate corals appeared by the Late Cambrian, but large reefal bioconstructions containing tabulates appeared in the Late Ordovician. It is difficult to state whether tabulates possessed algal symbionts from the onset, but appearance of reefal structures suggests that symbiotic algae possibly appeared by the Silurian, and probably also Late Ordovician. If the appearance of Ordovician photosymbiosis could be confirmed, it would coincide with the Great Ordovician Biodiversification Event.
Palaeozoic reefs are very distant from the Meso-Cainozoic reefs in terms of biodiversity, but this study indicates that the ecological mechanism of massive colony formation remained very similar since the Ordovician. The appearance of scleractinians after the extinction of tabulates at the Permian–Triassic crisis allowed the continuation of a vastly important ecological system of coral–algal symbiosis that had existed since at least the Middle Silurian.
Stable isotope analysis shows that most tabulate corals had δ18O to δ13C ratios very similar to those of modern photosymbiotic scleractinians and differing visibly from the corresponding isotope ratios in modern non-photosymbiotic corals. Such an observation evidences the coral–algal symbiosis in Palaeozoic tabulate corals, thus pushing back the appearance of such a type of mutualism as early as the Middle Silurian. Therefore, this discovery pushes back the appearance of this ecological interaction about 190 Myr earlier than previously indicated.
This work is a contribution to a research grant no. N307 313236 of the Ministry of Science and Higher Education of the Republic of Poland to M.K.Z.
I am very grateful to Graham Young and four other anonymous journal referees for significant, constructive remarks and helpful corrections of this paper. Euan N. K. Clarkson is thanked for many discussions, linguistic corrections of the text and Jerzy Trammer for inspiring discussions. I express my gratitude to Ireneusz Walaszczyk, Adam T. Halamski, wojciech kozłowski and Anna Żylińska for comments on the manuscript, and to Piotr Łuczyński and Błażej Berkowski for lending specimens for study. I am grateful to Andrzej Baliński who kindly helped with preparing illustrations.
- Received October 11, 2013.
- Accepted November 8, 2013.
- © 2013 The Author(s) Published by the Royal Society. All rights reserved.