Black corals are enigmatic creatures, which are often misidentified as gorgonians. These hexacorals have unique properties and display interesting morphology. Dr. Marzia Bo discusses these interesting corals in great depth, and touches on many aspects of their biology.

Antipatharians, commonly known as black corals, constitute a small order of colonial hexacorallians (Anthozoa, Cnidaria) comprehending up to now approximately 230 species divided into 7 families and 42 genera. Despite the relatively small number of species, black corals are spread throughout all the oceans of the world. They are found especially in tropical and subtropical areas, where they can reach very superficial waters, and in temperate and polar regions, but here never shallower than 50 meters in depth (up to 8000 m).

Figure 1: colony of Antipathes sp. at 30 m, Mentawai Islands, Indonesia.

With respect to other coral taxa, which are relatively well-studied especially in tropical environments, this group of corals remains poorly known, both from a taxonomic and ecological point of view. This is probably also related to the fact that their most common bathymetric range starts below 100 m in depth, confining them within the category of the deep coral fauna together with members of the taxa Scleractinia, Octocorallia, Stylasteridae, and the genus Gerardia.

The discovery of a rich antipatharian community in the shallow waters of the Indonesian Archipelago (counting around 40 species) allowed a long-term research project to be undertaken. Light was shed on several biological and ecological aspects concerning these black corals, such as species richness, habitat preferences, specific bathymetric ranges, symbiotic associations, feeding behaviours, reproductive strategies, growth rates and phylogenetic relationships. Black corals proved to be a keystone group for the maintenance of high biodiversity levels on coral reefs. Their ecological importance, both in shallow tropical waters and deep bottoms, highlighted the need of protecting these corals. Heavily exploited for the jewellery market in several areas of the world, such as on the Hawaiian and Caribbean islands, they have been included in Appendix II of CITES for protection of endangered species, but their importance is not limited only to their commercial value. In fact, biomedical applications based on the resistive organic skeleton of black corals have recently been identified. Furthermore, a potential source of palaeo-oceanographic information has been found in the concentric skeletal layers of these marine treasures.

History and systematics

The taxonomic origin of black corals dates back to the 18^th century when the German scientist Peter Simon Pallas separated antipatharians from gorgonians (as proposed by Linnaeus in 1758) on the basis of their spiny skeleton and their coenenchyme lacking sclerites, and called them Antipathes. In Latin, the term Antipathes refers to a stone which is supposed to act as a charm against witchcraft. In fact, black corals were collected in ancient times for their magical and curative properties. For example, in the Red Sea, they were used to cure eye illness. The same magical characteristics were already attributed to the Mediterranean red coral Corallium rubrum thousands of years earlier.

Before Linnaeus, as many other corals, antipatharians were considered marine plants, especially because of their phytomorphic appearance. Therefore, their first illustrations can be found in old plant catalogues. Black coral spines would still be the most important taxonomic feature if not for a small genus of gorgonians named Dendrobrachia, characterised by a spiny skeleton, which has only recently been moved to the octocoral subfamily. The principal characteristics distinguishing the order subsequently became the presence of polyps with only six simple non-retractile tentacles and six primary mesenteries. Because of their unpinnulated tentacles, black corals were incorporated within the taxon of sea anemones. In 1857, Milne-Edwards, on the basis of their colonial habit, considered them sufficiently distinct from actiniarians to create a separated group named “sclerobasic zoantharians”. The detailed microscopic studies of Lacaze-Duthiers, published in 1865, eventually contributed to the recognition of antipatharians as a distinct order of anthozoan hexacorals.

"Black corals have black skeletons made of chitin, hence their name."

The term Antipathidae, used for the first time by Ehrenberg in 1834 for the description of the first antipatharian family, seems to have emerged while describing a family of Scleropod bryozoans encrusting a black coral stem. What is certain is that Milne-Edwards and Haime, in 1857, used the same root to define the order name, Antipatharia, and that -pathes became the compulsory and characteristic suffix for all the genera of this taxon.

Systematic literature concerning black corals grew through the 19^th century until the beginning of the 20^th century thanks to great scientific explorations, such as the Siboga Expedition or the Challenger, supplying numerous specimens. After an almost 50 year-gap in taxonomic studies, the finding of new species in the 1970s started up a major work of taxonomic revision which is still in progress. Moreover, the modern explorative campaigns of abyssal plains are now shedding light on the enormous deep biodiversity of these organisms, especially on continental shoals and seamounts. However, the classification of the antipatharian corals has been complicated, and in many aspects still is, by the existence of species established only on the base of dry, incomplete museum material, and by the absence of clearly, universally recognised taxonomic characters defining the hierarchy of the order.

Figure 2: examples of skeletal spines in black corals.

Traditionally, the classification of antipatharians was based on morphological and anatomical characters. Since 1970, important efforts have been made to enhance the systematic status of these organisms using more modern technologies for taxonomic purposes, including, in recent years, molecular analyses. The first molecular work, dealing with the complete sequencing of the black coral Chrysopathes formosa genome, was published to support the inclusion of antipatharians in the subclass of hexacorals, and to separate it from the order Ceriantharia, finally solving a bicentenary debate. At a specific level, the main problem in taxon definition remains the extreme plasticity of the colonies, which is in part related to environmental conditions, similar to other branched cnidarians. The result is a potential overestimation of the number of species, often confused with possible ecotypes. In this regard it is possible to hypothesise that some micro-features, such as skeletal spines, could be shaped independently from environmental cues. Using scanning electron microscopy (SEM), the study of spine morphology has recently been employed with success in taxonomic works, showing microscopic differences in the deposition of skeletal material, which are often useful for species distinction.

Nucleotide sequences are an obvious source of additional evidence regarding systematic relationships of black corals. This approach may be used in combination with morphology, to solve the problem of categorising black corals to proper taxa. The genetic relationships of several species have been studied using rDNA internal transcribed spacers (ITS) sequences, already frequently used for intra- and interspecific evolution studies. Molecular data supports the division of the Indonesian species in two major clades: the family Antipathidae and the family Myriopathidae. The degree of genetic variation in these two families differs: in the Myriopathidae cluster, the analysis is not able to separate the species Myriopathes and Cupressopathes in spite of the morphological differences in the colonies, suggesting the possibility of reticulate evolution due to hybridization among these species. A clear separation is detected only with the Mediterranean Antipathella subpinnata. In the Antipathidae cluster instead the species, well distanced by spine characteristics, are more separated. It seems that the degree of variation within the different families shown by the analysis, reflects the degree of morphological variability of spines. High heterogeneity of spines is equal to a high genetic variability and vice versa. This is not the only case in which molecular analysis highlights the potential role of spines in genetic separations. For example, in the case of the new genus Pseudocirrhipathes, P. mapia and Allopathes desbonni represent a well distinct clade, showing a unique verticillated arrangement of spines.

Figure 3, left column: Myriopathes myriophylla and its spines. Right column: Cupressopathes abies and its spines.

Morphology

Black coral colonies, ranging from a few cm to several meters in height, may be characterised by a single stem or a more or less complicated branching pattern (made of stems, branches and pinnules), giving the coral a three-dimensional aspect. Pinnules represent the branching units of a black coral, being defined as the most uniform ramifications in terms of length or arrangement. The stem is anchored onto the substratum with a basal plate or, in soft bottoms, with a flat hook extremity.

"Black corals have polyps with six tentacles, placing them in the Hexacorallia subclass."

Figure 4: underwater images of black coral species photographed in different localities of the Indonesian Archipelago. Different species of Antipathes, Stichopathes, Cirrhipathes, Cupressopathes and Rhipidipathes.

The transversal section of the black coral skeleton appears circular, having a central canal surrounded by a series of concentric strata of deposited organic material. The colour of the skeleton varies from black in the thicker portions (hence the name black corals) to golden yellow in the apical pinnules. All around the branches the skeleton rises up in a series of small spines arranged in more or less regular longitudinal rows, characterised by distinct features depending on the species. No mineral elements such as spicules or sclerites are present in the tissues, which as a result are soft and fragile. The organic material composing the skeleton is produced by the ectodermic coenenchyme covering the branches, and also emerges in the polyps. The zooids display bilateral symmetry in the perpendicular direction of the main axis and possess six tentacles, two sagittal and four lateral, arranged around an oral cone bearing the mouth at its top. Black coral polyps may show a different set of colours, from transparent to white, yellow, red, orange, pink, green or brown. They have a weak muscular system; their longitudinal fibres are not completely developed and this is the reason why tentacles can only slightly contract. Polyps are never able to retract completely. The gastric cavity lumen is divided by 6-12 mesenteric septa in radial non-communicating chambers, nevertheless cavities of adjacent polyps are connected.

Figure 5: morphology of black corals. Top left: circular skeleton with central canal. Top right: transversal section of a polyp showing mesenteric septa and hollow tentacles. Bottom: SEM image of a polyp.

In other cnidarian groups, such as sea anemones and hydroids, cnidocysts are an important taxonomic character. They are useful for the definition of higher taxa, for the determination of species where no alternative method is available and they represent an additional aid in identifying species within a difficult group. In contrast, the cnidome has been rarely employed in black coral taxonomy. Some authors provided information concerning measures and distribution of cnidocysts of several species and described the typical arrangement of cnidae in wart-like batteries called “nematosores”, which give the tentacle epidermis a mosaic character.

Figure 6: cnidome of black corals. Nematosores are visible on tentacle surfaces, including various types of cnidocysts such as basitrich isorhizas and spirocysts.

Analyses conducted on several Indonesian species showed that the antipatharian cnidome typically consists of spirocysts, microbasic mastigophores, and basitrich and holotrichous isorhizas. These are however arranged differently depending on the taxon considered. Moreover, field observations on whip black corals showed that their characteristic large polyps may easily extend their tentacles up to 10 times their normal length (so-called sweeper tentacles), responding to disturbing corals or encrusting animals. Not all organisms suffer this attack; sponges for example show a strong anti-fouling reaction, rapidly destroying black coral tissue.

Figure 7: sweeper tentacles. Left column: sweeper tentacles produced after physical contact with disturbing organisms. Right column: disturbance of gorgonians and soft corals on antipatharian tissues.

The skeleton of black corals is an organic semi-precious structure known as Antipathin, made of the same chitin which makes up the cuticle of insects, and a non-fibrous scleroprotein, which differs from the gorgonin-containing collagen of gorgonians. The skeleton is organised in alternating microlayers united by organic dense material. The concentric deposition of microlayers is responsible for the growth rings visible in transversal sections, which have been related to colony age and growth rate.

The resistive and elastic properties of the skeleton, which depends on both composition and architecture, result from the current colonies face in their natural environment. This general consideration is in accordance with some observations conducted in the Indonesian antipatharian community. For example, net-like Rhipidipathes reticulata colonies living on vertical walls show thin branches which are intricately fused together, providing the skeleton with significant resistive qualities. Antipathes and Cirrhipathes colonies are flexible and resistant, while Stichopathes stems adapted to the strongest currents are thicker and more rigid, but commonly go through skeletal fractures.

It is interesting to note that unlike gorgonians, where collagen fibres determine flexibility, in black corals chitin is responsible of the elastic properties while polyphenolic proteins contribute to skeletal reinforcement. Spines play an important role in the anchorage and protection of polyps. Recent studies highlighted the role of spines as points of discontinuity in normal chitin fibre arrangements along branches, enhancing the resistance of the skeleton against torsion created by water current.

Figure 8, left: growth rings making up the circular skeleton. Right: anomalous growth of a Stichopathes whip coral after multiple fracture events.

Reproduction

Black corals are known as gonochoric organisms; generally the entire colony has the same sex, even though the literature mentions existing hermaphroditic species. Of the six primary mesenteries, only the two placed in the sagittal direction bear reproductive organs, and they are usually the longest mesenteries. Observations conducted in the field have always reported the absence of clear external morphological differences between the sexes. This seems to be the general rule, both in fertile and infertile colonies.

"Anchorages of broken fragments are not regenerated, suggesting that fragmentation is not a common reproductive strategy for black corals."

Yet some congeneric species, namely Antipathella subpinnata and Antipathella fiordensis, seem to be exceptions. In fact, in both species the pink fertile polyps are in contrast with the non-fertile white zooids. Fertile polyps are distributed in random patches in branched antipatharians, while in whip black corals the apical portion is generally always fertile in mature colonies, and fertility along the rest of the stem is more random. The quantity of eggs per polyp generally depends on the size of the zooid, for example large female polyps of Cirrhipathes spp. (2-3 mm in transverse diameter) can carry up to 400-500 eggs each and show continuous phases of fertility throughout the entire year.

Recent ultrastructural evidence of Indonesian specimens supported the origin of black coral sperm from flagellated gastrodermal cells, successively expelled from the mouth. Pro-acrosomal vesicles and a 9+2 flagellum are considered to be a feature of primitive spermatozoa, which are adapted to external insemination. This is in accordance with the general idea of antipatharians as being one of the most primitive groups of anthozoans. Another interesting feature is a cup-like body, found around the flagellum, whose function is probably related to tail movement, and whose occurrence seems to be limited to the sperm of antipatharians.

Figure 9: reproductive status of black corals. Top: sperm cysts in reproductive mesentery. Bottom: eggs in reproductive mesenteries.

The importance of asexual processes has been verified through long-term monitoring of Indonesian whip black coral meadows, where signs of apical fractures have been reported for the majority of colonies. These are likely related to water current. It seems that these species undergo frequent episodes of fracture and regrowth, which differs from the monopodial sea fan Junceella. Anchorages of broken fragments are not regenerated, suggesting that fragmentation is not a common reproductive strategy for black corals. Either way, asexual reproduction plays an important role in the reproduction of black corals. Budding is the most common strategy, and this is the reason why alternation of adult and juvenile polyps on branches is observed frequently.

Larvae have been described only for Antipathella fiordensis as negatively buoyant, non-feeding and short-lived planulae (approximately 10 days). These factors, coupled with hydrographic observations of restricted water movement in the fjords where this species lives, suggest that larval dispersal and gene flow are limited and that separate fjords may represent genetically isolated populations. Considering the habitat preferences of adults, it has been hypothesised that they tend to settle on inclined substrata, with low light intensity and high nutrient supply. Laboratory observations conducted on cut tentacles of Indonesian black coral polyps have revealed their high resilience (kept alive in cups for many days) and their ability to reorganise into independent structures. Active ciliate motion on their surface makes them move around in a peculiar fashion. It is possible that these observations may be in accordance with the existence of pseudo-larvae, representing the phenomenon of “polyp bail-out”, also described for A. fiordensis.

In part two, black coral ecology will be discussed at length. This part of the series includes their feeding behaviour and associated fauna such as shrimp and gobies.

Figure 10: A Stichopathes specimen found in a marine aquarium (photograph: Tim Wijgerde).

Acknowledgements

All pictures, unless stated otherwise, courtesy of Dr. Marzia Bo.

References

M. Bo, S. Tazioli, N. Spanò and G. Bavestrello. 2008. Antipathella subpinnata (Antipatharia, Myriopathidae) in Italian seas. Italian Journal of Zoology, 75: 185-195;

E. Gaino, M. Bo, M. Boyer and F. Scoccia. 2008. Sperm morphology in the black coral Cirrhipathes sp. (Anthozoa, Antipatharia). Invertebrate Biology, 127: 249-258;

M. Bo, M. Barucca, M. A. Biscotti, A. Canapa, H. F. N. Lapian, E. Olmo and G. Bavestrello. Description of Pseudocirrhipathes (Cnidaria: Anthozoa: Hexacorallia: Antipathidae) a new genus of whip black corals from Celebes Sea. Italian Journal of Zoology, 76: 392-402;

M. Bo, C. Di Camillo, A. M. Addamo, L. Valisano and G. Bavestrello. 2008. Growth strategies of whip black corals (Cnidaria: Antipatharia) in the Bunaken Marine Park (Celebes Sea, Indonesia). Marine Biodiversity Records, 2: 1-6;

M. Bo, G. Bavestrello, S. Canese, M. Giusti, E. Salvati, M. Angiolillo and S. Greco. Characteristics of a black coral meadow in the twilight zone of the central Mediterranean Sea. Marine Ecology Progress Series, in press;

H. F. N. Lapian, M. Barucca, G. Bavestrello, M. A. Biscotti, M. Bo, A. Canapa, S. Tazioli, E. Olmo. 2007. A systematic study of some Black Corals species (Antipatharia, Hexacorallia) based on rDNA internal transcribed spacers sequences. Marine Biology, 151: 785-792;

S. Tazioli, M. Bo, M. Boyer, H. Rotinsulu and G. Bavestrello. 2007. Ecology of some common antipatharians from the Marine Park of Bunaken (North Sulawesi, Indonesia). Zoological Studies, 46: 227-241.