Influence of sipunculan (peanut worm) activity on orifice formation in scleractinian Heterocyathus for adaptation to soft substrates.

Mutualism profoundly affects the morphology and ecological evolution of both hosts and symbionts involved. Heterocyathus is a solitary scleractinian coral that lives on soft substrata, and sipunculan worms live symbiotically in the tube-like cavities (orifice) inside the coral skeletons. This habitat provides protection to the sipunculan worms against predators and-owing to the mobility of the worms-prevents the coral from being buried with sediments. The orifice growth is closely related to the symbiont sipunculan worms; however, this has not been previously elucidated. Here, we clarified the growth process of scleractinian coral orifices and the influence of sipunculan activity on this. The orifices were originally formed by rapid accretion deposits. The coral soft tissue enveloping the growth edge of the orifice repeatedly retreated to the outer side due to direct damage to the soft part and/or excessive stress caused by the rubbing of the sipunculan through locomotion, excretion, and feeding behaviour. This resulted in a toppled-domino microskeletal structure appearance and maintenance of the orifice growth. These outcomes demonstrate the first example of the direct influence of symbionts on the skeletal morphogenesis of scleractinian corals. The mutualism between the two organisms is maintained by the beneficial confrontation in forming orifices.

First real-time observation of transverse division in azooxanthellate scleractinian corals.

Asexual reproduction is one of the most important traits in the evolutionary history of corals. No real-time observations of asexual reproduction in azooxanthellate solitary scleractinian corals have been conducted to date. Here, we describe previously unknown aspects of asexual reproduction by using Truncatoflabellum spheniscus (Family Flabellidae) based on observations of transverse division conducted over 1200 days. The findings revealed that (1) transverse division was caused by decalcification; (2) compared to the anthocyathus (upper part of the divided corallum), the soft parts of the anthocaulus (lower part of the divided corallum) were severely damaged and injured during division; (3) these injuries were repaired rapidly; and (4) the anthocaulus regrew and repeatedly produced anthocyathi by means of transverse division. Differences in the patterns of soft-part regeneration and repair, as well as differences in skeletal growth rates between the anthocaulus and the anthocyathus imply that the ecological requirements and reproductive success are different from each other immediately after division. The findings provide important clues for unravelling why asexual reproduction appeared frequently in free-living corals, and the extent to which those modes of reproduction has affected the adaptive and evolutionary success of scleractinian corals throughout the Phanerozoic.

Burrowing hard corals occurring on the sea floor since 80 million years ago.

We describe a previously unknown niche for hard corals in the small, bowl-shaped, solitary scleractinian, Deltocyathoides orientalis (Family Turbinoliidae), on soft-bottom substrates. Observational experiments were used to clarify how the sea floor niche is exploited by turbinoliids. Deltocyathoides orientalis is adapted to an infaunal mode of life and exhibits behaviours associated with automobility that include burrowing into sediments, vertical movement through sediments to escape burial, and recovery of an upright position after being overturned. These behaviours were achieved through repeated expansion and contraction of their peripheral soft tissues, which constitute a unique muscle-membrane system. Histological analysis showed that these muscle arrangements were associated with deeply incised inter-costal spaces characteristic of turbinoliid corals. The oldest known turbinoliid, Bothrophoria ornata, which occurred in the Cretaceous (Campanian), also possessed a small, conical skeleton with highly developed costae. An infaunal mode of life became available to turbinoliids due to the acquisition of automobility through the muscle-membrane system at least 80 million years ago. The newly discovered active burrowing strategies described herein provide new insights into the use of an unattached mode of life by corals inhabiting soft-bottom substrates throughout the Phanerozoic.

Regular budding modes in a zooxanthellate dendrophylliid Turbinaria peltata (Scleractinia) revealed by X-ray CT imaging and three-dimensional reconstruction.

The zooxanthellate dendrophylliid coral, Turbinaria peltata (Scleractinia), exhibit various growth forms that increase the photoreception area through the development of coenosteum skeletons. Because it is difficult to make detailed observations of the internal structures, we visualized inner skeletal structures using nondestructive microfocus X-ray computed tomography (CT) imaging. After removal of the coenosteum skeletons from the X-ray CT images, three-dimensional 3D-models were reconstructed for individual corallites. Regular budding was observed from the 3D-model and cross-sectional images as follows: 1) lateral corallites occurred only near the two primary septa on one side, apart from a directive primary septum with distinct polarity; 2) the budding occurred upward at acute angles; and 3) these regular structures and polarity were repeated throughout growth with every generation. Even in zooxanthellate dendrophylliids, the same budding modes as observed in azooxanthellate equivalents control the colonial growth. These characteristics provide clues for understanding the mechanisms that regulate the shapes of modular marine organisms.

Internal skeletal analysis of the colonial azooxanthellate scleractinian Dendrophyllia cribrosa using microfocus X-ray CT images: underlying basis for its rigid and highly adaptive colony structure.

Dendrophyllid Scleractinia exhibit a variety of colonial morphologies, formed under the strict constraints on (1) budding sites, (2) orientations of the directive septa of offsets, (3) inclination of budding direction, and (4) those constraints in every generation. Dendrophyllia cribrosa exhibits a sympodial dendroid form, characteristically large coralla, and occasional fusions of adjacent branches within the same colony. Adjacent corallites are bound and supported by coenosteum skeleton. This study examined the inner skeletal structures at the junctions of fused branches using a non-destructive microfocus X-ray computed tomography (CT) imaging approach, and considered the reasons for the large colonial sizes and their adaptive significance. Three-dimensional reconstructions of two-dimensional X-ray CT images reveal that individual corallites are not directly connected in fused parts. Additionally, no completely buried individuals were found within fused skeleton. When adjacent branches approach one another, constituent corallites change their growth directions to avoid collisions between the branches. The adjacent branches fuse without a reduction in the number of constituent corallites, leading to the establishment of reticular and rigid colonial structures. In addition, a nearly even distribution of individuals on the colony surface facilitates efficient intake of nutrients. Thus, the growth of large D. cribrosa colonies involves avoidance of collision between constituent individuals, the reinforcement of colonial structure, and efficient uptake of nutrients. These observations provide insights on the dynamics of interrelationships between colony-making mechanisms and the adaptive strategies required under habitat conditions such as specific current activities.

Intrinsic constraints on sympodial growth morphologies of azooxanthellate scleractinian coral Dendrophyllia.

BACKGROUND: Asexual increase occurs in virtually all colonial organisms. However, little is known about the intrinsic mechanisms that control asexual reproduction and the resultant morphologies of colonies. Scleractinian corals, both symbiotic (zoaxanthellate) and non-symbiotic (azooxanthellate) corals are known to form elaborate colonies. To better understand the growth mechanisms that control species-specific type of colony in azooxanthellate dendrophyllid scleractinian corals, we have studied details of the budding pattern in the sympodial colonies of Dendrophyllia boschmai and Dendrophyllia cribrosa. PRINCIPAL FINDINGS: Budding exhibits the following regularities: (1) the two directive septa of offset corallites are oriented almost perpendicular to the growth direction of parent corallites; (2) offsets generally occur in either of the lateral primary septa that occur on one side of a corallite; the individuals thus show a definite polarity with respect to the directive septa, and only when branching dichotomously offsets occur in both primary septa; (3) the lateral corallites grow more-or-less diagonally upwards; and (4) the regularities and polarities are maintained throughout growth. Given these regularities, D. boschmai grows in a zigzag fashion by alternately budding on the right and left sites. In contrast, D. cribrosa grows helically by budding at a particular site. CONCLUSIONS/SIGNIFICANCE: The strict constraints on budding regularities and shifts in budding sites observed in the sympodial growth forms of corals greatly affect resulting morphologies in azooxanthellate coral colonies. A precise understanding of these intrinsic constraints leads to a fundamental comprehension of colony-forming mechanisms in modular organisms.