Dimorphic life cycle through transverse division in burrowing hard coral Deltocyathoides orientalis

Transverse division of Deltocyathoides orientalis

In this study, we conducted a detailed morphological analysis of an undescribed species and D. orientalis. The results showed that the two species were different in terms of their mode of life (attached vs. free-living) and GCD size (Figs. 3 and 5, Supplementary Table S3). However, some morphological characteristics such as granular septa, septal and palar arrangement, and columella were common between the two species.

A circular discoloration was observed on the basal part of the skeleton in 41/308 specimens of free-living D. orientalis collected at St. 2 (Fig. 2A–D). Similar discoloration by decalcification for transverse division has previously been observed at the basal part of almost all anthocyathi of Truncatoflabellum14,15. However, over 80% of the specimens of free-living D. orientalis did not show this basal discoloration (Fig. 5). Soft tissues on the basal part of the anthocyathus of Truncatoflabellum spheniscus are immediately lost after transverse division14. Consequently, the original basal scar and the decalcified skeleton remained without additional skeletal thickening. As the D. orientalis has soft parts covering the entire skeleton when it is alive, the outer surface of the corallum, including the discolored basal part, also undergoes additional thickening of the associated skeletal region. This means that the basal parts of the corallum of D. orientalis may not all exhibit discoloration that is hidden under the new intact skeletons. This consideration corresponds to the smaller size distribution of the GCD of anthocyathus bearing basal scars in D. orientalis, which is thought to have a shorter duration of skeletal precipitation than the GCD of anthocyathus without it (Fig. 3, Supplementary Table S1). In addition, Sentoku et al.8 showed that D. orientalis is capable of self-repair if 10% of the skeleton remains after physical damage, in which the basal discoloration can potentially be lost. Therefore, discoloration restricted to the basal part of D. orientalis is inferred to be generated by decalcification, and almost all D. orientalis may inherently have a discolored basal part.

In the attached specimens, white opaque discoloration lines on the outside of the wall perpendicular to the growth direction and double-walled structures, such as rejuvenescences, were observed (Fig. 4A–C). Anthocauli of Pliocene fossils of Truncatoflabellum carinatum and extant Truncatoflabellum spp. show successive rejuvenescences that are derived from a temporal decrease in polyp diameter due to transverse division injury14,15. Moreover, the anthocauli of extant Truncatoflabellum spp. exhibit traces of decalcification at the uppermost periphery of the outer wall portion of the rejuvenescence. A similar trace of decalcification of anthocaulus has been reported in Fungia fungites16. The discoloration and double-walled structures in the attached specimens are thought to have been formed by transverse division with decalcification.

Furthermore, the nucleotide sequences of the undescribed species and D. orientalis were completely consistent in the 16S-rDNA region (462 bp) and CO1 region (646 bp). In addition, due to the creation of phylogenetic trees using the nucleotide sequences obtained from the five gene regions, the undescribed species and D. orientalis were found to represent a single clade in all gene regions (Fig. 6A–B, Supplementary Fig. S1A–C).

Based on the results of both the morphological and molecular phylogenetic analyses, we concluded that the undescribed species was the anthocaulus of D. orientalis. Moreover, the free-living anthocyathus of D. orientalis reproduces asexually by transverse division of the attached anthocaulus.

Control of anthocyathus morphology by transverse division

Two calical morphologies were observed in the attached coralla: the depressed calice and the exerted and bulged calice with distinct costae (Fig. 4). Particularly, the skeletal characteristics of the uppermost part of the latter attached specimens were found to closely resemble those of the anthocyathus of D. orientalis (Fig. 4B). The smaller corallum of the anthocyathus of D. orientalis shows a slightly protruding base with decalcification. The center of the basal part is composed of tubercular fragments from the divided columella of the anthocaulus and is encircled by costae. From the side view, the costal edge angle is bimodal, and the angle increases (from approximately 20°–40°) at the periphery of the decalcification part. The protruding morphology of the lower section of the anthocyathus of D. orientalis fits into the depressed calice morphology of the anthocauli. Thus, the exerted and bulged calical part with the deeper part of the inner calice of the anthocaulus without the outer wall of D. orientalis corresponding to slightly bowl-shaped anthocyathus may be scooped from anthocaulus by transverse division. Since only the inside of the calice was extracted from the anthocaulus, the GBSD of the anthocyathus of D. orientalis was only slightly smaller than the GCD of anthocaulus (Fig. 3).

The bowl-shaped corallum and distinct costae of D. orientalis plays an important role when burrowing into soft substrates7,8. The corallum morphology of the anthocyathus with a protruding base immediately after division might have an ecological function that facilitates free living on soft substrates. The anthocyathi of Truncatoflabellum show truncated basal scars that are almost horizontal or along the arcuate growth line of the wall surface6,14. In addition, the increased thickening deposits in the lower parts of the anthocyathus of Truncatoflabellum might contribute towards increased stability in the substrate, as well as maintaining the calice orientation towards the sea surface, which would be advantageous for the purposes of food acquisition14. Thus, the morphological formation patterns of the prospective anthocyathus by skeletal growth and carving by decalcification in the anthocaulus stage are thought to involve not only increasing clonal individuals but also adaptations for a free-living mode of life after transverse division in the anthocyathus stage.

Alternation of generations by transverse division

Statistical examination with Steel–Dwass’s multiple comparison test showed that the size distributions of GCD and GBSD for the anthocyathi in D. orientalis were distinctly different (Fig. 3, Supplementary Table S1). The size distribution of the basal scars approximates a normal distribution (Supplementary Table S2), suggesting that transverse divisions only occur in coralla that reach a certain diameter, not randomly. The size distributions of the GCD of the anthocyathi are significantly different from GBSD (Supplementary Table S1). The difference indicates that the anthocyathus of D. orientalis does not show asexual reproduction by transverse division. In contrast, plural white opaque horizontal lines of decalcification on the outside of the wall of the anthocauli of D. orientalis indicate repeated transverse divisions (Figs. 2L,O, 5C). The statistical analysis supports the idea that the anthocauli of D. orientalis repeatedly reproduce asexually through transverse division, whereas the anthocyathi only reproduce sexually. D. orientalis, thus, exhibits a distinct alternation of generations (sexual in anthocyathi vs. asexual in anthocauli), which is also well known in Fungia and Truncatoflabellum6,14,15,17. Differences were observed in the number of anthocauli (seven individuals) and anthocyathi (384 individuals) of D. orientalis collected at St. 2. The small number of the anthocauli of D. orientalis is similar to the anthocauli of Truncatoflabellum15. These larger increasing rates of anthocyathus suggest that asexual reproduction may play an important role in increasing coral population size in soft-substrate environments, such as the sand and mud.

Anthocyathi of Peponocyathus duncani18 and Bourneotrochus stellulatus19 show repeated asexual reproduction by transverse division (e.g.20,21,22). Zibrowius23 and Stolarski21 discussed importance of the transverse divisions of anthocyathi for adaptive strategies on soft substrates, as well as the increase in clonal individuals21,23. Corallum size and weight reduction by the transverse division of the anthocyathus could lead to efficient automobility in Peponocyathus duncani having a smaller cylindrical corallum with a maximum calicular diameter of 3.7 mm21. However, the morphological analysis of D. orientalis revealed that the anthocyathi did not undergo transverse division. The acquisition of automobility in anthocyathi of D. orientalis, including burrowing, escape from burial, and righting behaviors, implies that the species is actively utilizing habitats under the seafloor. The ability of D. orientalis to retract the oral side of the polyp into the sediment is considered an anti-predator response, similar to that of burrowing sea anemones and tube-dwelling anemones7. The asexual reproduction of division that occurs after the formation of a bowl-shaped corallum with costae in the anthocaulus stage suggested in this study reduces the cost and time of skeletal formation for infaunal adaptation after transverse division. Immediately after division, D. orientalis can smoothly shift to a burrowing lifestyle that efficiently utilizes the soft-substrate environments, which probably increases its survival rate (Fig. 7).

Figure 7
figure 7

Schematic diagram showing the dimorphic life cycle of the azooxanthellate scleractinian coral Deltocyathoides orientalis. (A) Coral planula attaching to shell fragment on soft substrate. (B) Anthocaulus. (C) Anthocyathus occurring at the upper interior of the anthocaulus. (D) Division of anthocyathu from anthocaulus. (E) Anthocyathus burrowing into a soft-bottom substrate immediately after division.

In this study, we clarified the life history of D. orientalis based on morphological and molecular phylogenetic analyses. In the future, it will be necessary to clarify the frequency of sexual and asexual reproduction and the detailed growth pattern of the species by observing the gonadal development of anthocyathi and the ecology of anthocauli. Furthermore, since Deltocyathoides has been classified based on the presence or absence of transverse division with the closely related genus Peponocyathus, it will also be necessary to systematically revise both genera in the future.

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