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.

Few ecological studies have been dedicated to black coral ecology, which mainly focused on Hawaiian and Caribbean coral reefs. Other research has been devoted to geographical and bathymetrical distributions or to the population structure of black corals, but no large-scale studies have ever been conducted.

The Marine Park of Bunaken, North Sulawesi, has recently been a site for extensive ecological studies on black corals. This area hosts a very rich community in terms of species diversity. Strong site-dependent differences have been recorded, where steep vertical walls display high biodiversity. The only site showing low values is the one characterised by meadows of whip black coral, containing only three species which are incredibly abundant. Apart from these areas, black coral density in the park lies around 0.5 colonies per m².

Figure 1: Meadows of whip black corals belonging to Stichopathes and Cirrhipathes genera.

Habitat preferences

Antipatharians have never been found in brackish waters, although some species have adapted to low or medium salinities. They do not tolerate air exposure caused by tidal movements, which is why they have never been found in the infralittoral zone.

The bathymetric spectrum, the depth range of black corals, is extremely wide. Members of four of the seven antipatharian families (Schizopathidae, Leiopathidae, Stylopathidae and Cladopathidae) are almost all deep species. This goes especially for the Schizopathidae family, whose species show strong adaptations to bathyal soft bottoms between 200 and 2,000 m in depth, such as hook-like anchorages. The Antipathidae, Aphanipathidae and Myriopathidae families on the other hand contain more species with shallower habitats or wider bathymetric ranges. This is also true at genus level. For example, there are stenobath genera found mainly in the littoral zone such as Cirrhipathes. The superior occurrence limit of this genus is determined by tide level. Other genera are more euribath, such as Antipathes or Bathypathes, and are found at different depths depending on the location considered.

Some shallow areas are particularly suitable for massive colonization by black corals. Indonesian coral reefs for example host huge meadows of whip corals in sites with strong water current. Other areas possessing specific chemical-physical characteristics may favour the settling and growth of deep species. This is what happens in the New Zealand southern fjords or along the Colombian coasts, which are characterized by cold waters, high nutrient levels due to upwelling phenomena or moderate continental run-off, low light intensity, little water turbulence and limited competition.

In Bunaken, within the scuba diving depth limit, the number of black coral specimens increases with depth, reaching maxima at 35-45 m. Some genera harbour typical deep water corals, as in the case of Cupressopathes and Rhipidipathes. The bathymetric distributions and habitat preferences of the studied species appear to be the result of interactions among biotic and abiotic factors. Competition for space with stony corals in the shallow portion of the reef is the most probable reason why antipatharians show a trend of increasing abundance and diversity with depth, as observed on Caribbean reefs. The only way an antipatharian can compete at low depths is to settle in crevices amongst the stony corals, and in fact, only the unbranched Cirrhipathes contorta coexists with scleractinian corals. This species occupies a minimal amount of substrate surface and is able to adapt its corallum shape to the available space. Water current, in terms of intensity and direction, is a major abiotic factor. Competition and water flow therefore are important environmental constraints, limiting black coral abundance.

Figure 2: Cirrhipathes contorta specimen.

Similar to other filtering colonial organisms, black corals also tend to settle in areas of moderate current, to maximize food capture and larval dispersion. Water movement acts not only on the distribution of species, but also on their morphologies. Colony morphology is a function of age and water current. A colony may show strong phenotypic plasticity depending on the intensity of the current: strong currents lead to more numerous and thicker branches, to maximize filtration efficiency and friction resistance. Where no prevailing direction is detected, colonies display a three-dimensional bushy morphology.

In Bunaken, black coral species are adapted to conditions of moderate or strong currents. Branched corals may live exposed on vertical reefs as fan-shaped colonies, or in canyons as arborescent colonies receiving vertical currents. Some species occupy the roofs of narrow gorges and caves, scattered on the reef wall. These species have thin, delicate, bushy colonies, which avoid sedimentation on the bottom of their hole and tend to entrap everything rolling down from the reef, both living epibionts and detritus (up to 95% of their biomass).

Feeding strategies

Whip corals are adapted to strong currents: Stichopathes spp. with monoserial polyp arrangements do not orient their zooids directly towards the current, because lacking mineral sclerites, their tissues would be very fragile. Instead, their long sagittal tentacles extend perpendicularly with respect to the lateral ones, capture prey and redirect them to the mouth. In black coral meadows, the majority of colonies arranges its polyps in the same way. Cirrhipathes spp. have polyps arranged all around the stem, being able to catch food particles from every direction. Species with bottlebrush morphologies such as Cupressopathes spp. utilise the same strategy, representing a compromise between a highly branched colony and minimal frictional stress.

Figure 3: Antipathes specimen entrapping a great amount of coralline algae and other organisms with its branches.

Some species are able to completely contract their tentacles, such as Cirrhipathes and Stichopathes, whilst other never contract them, such as Rhipidipathes. Still other species only partially contract their tentacles. The observed circadian rhythms of expansion and contraction have been correlated to the energetic balances of various species. Large basket-like polyps such as those of Cirrhipathes only expand at night to reduce energetic costs, and are typical for whip corals adapted to strong currents. They direct their long tentacles upwards to capture large zooplankton. In contrast, small net-like polyps such as those of Rhipidipathes are always expanded, and are typical for fan-shaped corals adapted to moderate currents. Their tentacles are directed laterally, and they almost touch one another to increase filtration efficiency.

Figure 4: characteristics of living polyps. Top left and right: specimen of Stichopathes sp. with expanded polyps during nocturnal feeding activity and contracted tentacles during the day. Bottom left and right: expanded basket-like polyps of the whip coral Cirrhipathes anguina and the net-like ramification pattern of the branched Rhipidipathes reticulata.

Antipatharians are suspension feeders, and this is the reason why colonies tend to orient themselves in the best way possible with respect to water current. Laboratory experiments on Antipathes grandis demonstrated that polyps were able to capture amphipods, copepods and chetognats, and that capture occurred through the use of both tentacles and cilia of ectodermic cells, moving the mucous film. In Indonesia, the production of such films has never been observed. Instead, mucous is always produced copiously after touching the colony, as a defensive response.

"Large basket-like polyps only expand at night to reduce energetic costs. Small net-like polyps are always expanded, and are typical for fan-shaped corals adapted to moderate currents."

Three feeding strategies have been found for Antipathella aperta: polyp prey capture, suspension feeding with mucous nets and discharged spirocyst microfibrils, and filter feeding on unicellular and particulate food material. It has also been reported that several polyps may cooperate in the capture of large prey. A gut content analysis of basket-like polyps, such as those of Indonesian Cirrhipathes spp., demonstrated that large zooids do show a micro-predatory activity on small zooplankton. Moreover, small groups of 2-3 polyps may also collaborate to trap large polychaetes. Net-like polyps instead prefer smaller micro- and nanoplankton or particulate organic matter, entrapped with mucous nets.

Figure 5: feeding on polychaetes by Cirrhipathes anguina polyps.

Symbiosis

Since the very beginning of the literature concerning black corals, colonies of antipatharians have always been reported as true oasis for organisms, sessile, mobile and sedentary. The most common observed epibionts are commensal invertebrates: cirripeds (barnacles) are frequent inhabitants of branched antipatharians, in particular lepads of the genus Oxynapsis. The spiny skeleton of the corals typically covers these animals and at times may also generate small branches; this situation has been reported in numerous Indonesian samples. SEM photographs distinctly show the coverage, as well as anomalous deposition of skeletal spines. Interestingly, spines don not grow all over the lepad shell. For example, they tend to leave the opening for the crustacean's cirri free, allowing them to come out. In Indonesian samples gastropods are also frequently found, covered by black coral skeleton.

Within the category of epibionts with limited movement are small crustaceans and polychaetes. For example, the worm Marphysa antipathum is able to build parchment-like tubes armed with sponge spicules and is a typical black coral epibiont. It has been hypothesised that free-living polychaetes may choose the host organism. Branched antipatharians are very suitable habitats and in some cases, including some species of the family Stylopathidae, the tube-like arrangement of pinnules is used as permanent refuge. It has also been hypothesised that the commensal worm may stimulate and direct the growth of these galleries.

Many crustacean decapods, such as crab and shrimp species have been described as species-specific epibionts of tropical black corals, such as Periclimenes wirtzi. It seems that while crustaceans benefit from a protected habitat and nutrients collected by polyps, the corals gain no advantage. In some cases, when food is scarce, crabs may even start feeding on coral tissue. Finally, the presence of ophiuroids has been frequently reported in the literature.  Antipathella fiordensis hosts, at least during the adult phase, the obligate commensal brittle star Astrobrachion constrictum. This epibiont feeds on polyp mucous during the night, while it exploits captured prey by nematocysts during the day. Other epibionts reported in the literature are sponges, anemones, bryozoans, crinoids, serpulids, spirorbids, barnacles, other corals and small oysters.

Figure 6: epibionts. Top and middle left: lepads covered by the black coral's spiny skeleton. Top right: mimic Pontonides shrimp living on a colony of Pseudocirrhipathes mapia. Bottom left: crinoids holding on to a coral stem. Bottom middle: parasitic zoanthids on an Antipathes colony, gobid fish living on Cirrhipathes anguina. Bottom right: fish eggs laid on a naked antipatharian skeleton.

In Bunaken, black corals also host a highly diversified epibiontic fauna, which probably finds shelter due to the three-dimensional arborescent shape of the colonies. Generally, the diversity of the epibiontic community is related to colony shape. On unbranched colonies, usually only one epibiont type exists, often a couple of crabs or shrimp. On flabellate colonies, a wider range of species may be found.

Four functional epibiont groups can be identified: first, filter feeding organisms hanging or moving on the colonies. Second, commensal decapods often found living in specific associations with black corals, showing clear mimicries. Third, parasitic invertebrates such as the ovulid snails Phenacovolva spp., various anemones (such as Nemanthus sp.) or caprellids. At last fish, finding only refugee in the branches of the corals or carrying out a more complex relationship, as in the case of the gobids Bryaninops spp., whose reproductive cycle is totally dependent on the existence of the coral.

Together with the epibiosis of living colonies, dead black coral skeletons are very common secondary substrates for colonisation. Recently, a conservative estimate was made of the total number of living organisms occupying a single dead colony of Antipathes dendrochristos. The figure was about 2,500 individuals! It became clear that while some groups of invertebrates are found in high densities on both live and dead colonies, others appear to be mostly limited to either living or dead colonies. A similar principle is described for Mediterranean colonies of Antipathella subpinnata, found in the Strait of Messina, which are impacted by abandoned fishing lines scratching coral tissue and enhancing the colonisation of numerous encrusting epibionts.

Another important physio-ecological feature distinguishing black corals from all other groups is the complete absence of records of zooxanthellate species. Only one author (van Pesch, 1914) reported the presence of few symbiotic algae in the endoderm of some Cirrhipathes species. However, the scarcity of information made this finding doubtful and it has never been sufficient for researchers to consider the order zooxanthellate. Recently however, an Indonesian Cirrhipathes species was collected hosting up to a million zooxanthellae per mm³ in its gastroderm (unpublished data).

Growth and transplantation

Relatively few studies have taken growth strategies of black corals into consideration. The majority of authors have focused on the chemical composition, structure and architectural mechanics of black coral skeleton. Black corals are generally considered slow-growing organisms, with long life spans and older age of maturity. Literature data concerning growth rates focus mainly on radial growth rates recorded with radiometric studies using ¹⁴C. Isotopic studies on organic and carbonate coral skeletons in fact allow for palaeoclimatic reconstructions of superficial and deep water temperatures in the recent past. Concerning growth in height, observations have focused on branched antipatharians of tropical and temperate waters, highlighting rates ranging between 0.5 cm and 9.3 cm/year. Black corals are the only colonial Cnidarians which have a completely organic skeleton, made of the particulate organic carbon sinking from the surface. Excluding the zoanthid Gerardia savaglia, which reaches considerable sizes thanks to its parasitic lifestyle, black corals have comparable growth strategies to gorgonians. This is interesting because the nature and properties of their skeletons are completely different.

Figure 7: Transplanted pieces of Stichopathes sp. showing growing extremities.

The over-exploitation of shallow water black corals for commercial aims, mainly linked to the jewellery trade, led to the inclusion of the entire order in the IUCN list and in Appendix 2 of the CITES list. The most endangered reefs in this respect are those of Hawai'i, Tonga, Ecuador and numerous Caribbean localities. Indonesian reefs are under less pressure caused by the black coral trade.

In order to start restoration projects of damaged reefs, it is key to assess the feasibility of black coral transplantation. In all transplantation experiments reported in the literature, critical factors proved to be chosen habitat, light, wave action and current intensity, and substratum. Long-term experiments conducted on whip black corals in Indonesia highlight the role of these species as targets for transplantation. With their simple morphology they grow quickly, up to 13.25 cm per month, which is among the fastest rates ever recorded for colonial cnidarians. Highest survival rates are displayed by adult colonies, which can be fragmented easily. In this case the apex will show the fastest growth rate, which is especially true for Cirrhipathes cfr. anguina. The studied species clearly shows a strong phototropic growth that orients upward. Colonies which settle on substrata of different inclinations have confirmed the important role of light in black coral development.

"An important feature distinguishing black corals from all other groups is the complete absence of zooxanthellate species. Recently however, an Indonesian Cirrhipathes species was collected hosting up to a million zooxanthellae per mm³ in its gastroderm."

Information on growth rates, longevity and reproductive cycles of black corals, associated with socio-economical studies, is vital to conservation efforts. In general, the establishment of a focused conservation and management strategy for reef ecosystems is essential for the maintenance of their integrity and biodiversity.

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.