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Adam James Garthwaite 2018
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Summary | |
Clavularia corals are distributed worldwide in the Indopacifc and Atlantic. Like other genus within Octocorallia, they exhibit octoradial symmetry and use characteristic sclerites for structural support. Clavularia form encrusting colonies of monomorphic polyp zooids connected through basal stolons. Sexual reproduction occurs annually through broadcast spawning, with colonies then formed through asexual reproduction. They are important components in reef ecosystem, making up a significant proportion of benthic fauna. Secondary metabolites produced by Clavularia are used in interspecific competition and as a defence against predators. These secondary metabolites are also medically important, possessing potent anti-tumour properties. Climate change and environmental change contribute the greatest threat to Clavularia species.
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Physical Description | |
Species within genus Clavularia form encrusting colonies of monomorphic polyp zooids. The polyps are connected basally through stolons, which often form a membranous mat. This mat is often littered with algae, sponges and sediment (Bastidas et al., 2002).
Clavularia are soft corals, therefore lacking a calcareous skeleton and instead possessing calcareous sclerites which provide structural support. Sclerites cover and stiffen the entire stolon mat, including the proximal anthostele of the polyps. The soft distal anthocodia extends from the rigid anthostele, but can also be retracted, leaving only the anthostele visible. The anthocodia exhibits octo-radial symmetry, with eight filiform tentacles surrounding the mouth. Tentacles are pinnately branched with pinnules.
The colouration and size of genetic individuals in genus Clavularia varies considerably within and between species (Bastidas et al., 2002). The observed colony had a bright purple membranous mat. The anthocodia was dark purple, with light blueish purple tentacles. Pinnules were a dark purple, almost brown colour, due to an increased concentration of zooxanthellae.
Fig 1. A diagram of the general structure of a Clavularia colony. The left polyp is extended, while the right polyp has been retracted. Important structures have been labelled. This diagram was modified from Williams (2000).
Fig 2. A colony from an unidentified species of genus Clavularia. Algae and sediment can be seen covering the purple stolon mat. The pinnulate tentacles of some polyps can be seen. The anthostelle can be seen clearly in retracted polyps.
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Ecology | |
The specific ecology of Clavularia remains relatively unknown, however their ecology is similar to other soft corals. Soft corals make up a significant proportion of benthic marine fauna in many reef systems, including the Great Barrier Reef (GBR) and reefs in the Red Sea (Dinesen, 1983; Benayahu and Loya, 1977). On the GBR, soft coral cover is low on the reef flats compared to the mid-shelf and particularly the outer-shelf reef slopes (Dinesen, 1983). Similar trends are found in the Red Sea, with similar soft coral coverage on reef flats in the Red Sea (Benayahu and Loya, 1977). Another study by Alino et al. (1992) found a high proportion of Clavularia inflata on inshore reefs at the GBR. These inshore reefs were sheltered from wave action. Soft coral cover generally increases with depth and is often inversely related to hard coral cover (Dinesen, 1983). These trends are likely a result of wave action, and the more durable hard corals outcompeting soft corals (Dinesen, 1983). This hypothesis is further supported by the increasing cover of soft coral with increasing depth (Dinesen, 1983).
Competition for space plays a major role in structuring marine benthic communities (Alino et al., 1992). Many species have evolved specific adaptions due to this interspecific competition, including species in Clavularia. Clavularia inflata has adapted a high growth rate as a means of outcompeting other species (Alino et al., 1992). C. inflata was shown to outcompete many species because of this characteristic. Success of the species was also reliant on the environmental conditions (Alino et al., 1992). Secondary metabolites with cytotoxic and biotoxic properties are also used in competition for space, while also being a defence against predators (Hashimoto et al., 2003).
Clavularia corals are capable of feeding on small dissolved nutrients and food particles, however most nutrients are acquired through symbiotic relationships with zooxanthellae. Zooxanthellae associated with soft corals are dinoflagellates of the genus Symbiodinium (Hashimoto et al., 2003).
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Life History and Behaviour | |
Life History
Clavularia species follow a standard biphasic life cycle, consisting of a mobile planula larval stage, followed by a sessile polyp stage. Polyps are capable of both sexual and asexual reproduction, both of which vary slightly between species.
Species are typically dioecious, achieving sexual reproduction through synchronised broadcast spawning (Benayahu, 1989; Bastidas et al., 2002). Spawning is typically an annual occurrence as seen in Clavularia hamra (Benayahu, 1989) and Clavularia koellikeri (Bastidas et al., 2002). The time at which this occurs each year is variable between regions and species, but appears to be triggered by the lunar phase (Benayahu, 1989; Bastidas et al., 2002).
Fertilization can take place externally or internally, depending on the species. C. koellikeri and C. inflata retain their eggs, with fertilization taking place internally (Bastidas et al., 2002), while fertilization takes place externally in C. hamra (Benayahu, 1989).
Numerous methods of external brooding have developed in Clavularia. Retention of fertilised eggs on or attached to polyps has been seen in numerous species including C. crassa (Benayahu, 1989) and C. koellikeri (Bastidas et al., 2002). Mucus sheaths containing planula larvae are released from C. inflata (Bastidas et al., 2002), while C. hamra releases embryos from colonies to complete embryogenesis on nearby substrate (Benayahu, 1989).
Following brief dispersal during the planula larval stage, larvae settle and metamorphose into polyps. Genetically identical colonies are then formed through asexual reproduction. New polyps arise asexually through fragmentation and/or stoloniferous growth (Bastidas et al., 2002).
Behaviour
A study by Satterlie and Case (1980) found that stimuli can elicit a response in individual polyps or entire Clavularia colonies. When the tentacles of polyps are lightly touched on the oral side, the tentacles are bent towards the mouth. Applying beef liver extract to a tentacle produced a similar response, but the mouth was also opened, and the tentacle sometimes inserted. Seawater produced no response, suggesting that Clavularia polyps can detect potential food. The only colony wide response was the withdrawal of polyps. Repeated application of stimulus (electrical and mechanical) resulted in tentacle retraction and eventual colony wide polyp retraction.
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Anatomy and Physiology | |
Polyp Anatomy
Clavularia polyps have octo-radial symmetry, consisting of eight pinnate tentacles surrounding the oral disk and mouth. Sensory structures, along with nematocytes, are primarily located on pinnules extended off the tentacles (Satterlie and Case, 1980). A tubular pharynx extends from the mouth into the coelenteron (gastrovascular cavity). The coelenteron is compartmentalised into eight regions by complete mesenteries which extend from the body wall to the pharynx. Male and female gonads (in separate colonies) develop annually on the mesenteries (Benayahu, 1989). Mesenteries are also lined with cilia which aid in the movement and digestion of food through the coelenteron. A network of neurons run throughout the polyp and connects to the colonial nerve network (Satterlie and Case, 1980). Zooxanthellae are intimately associated with Clavularia species, being found in tissue throughout the polyp, especially concentrated in the tentacles and pinnules.
Fig 3. Longitudinal sections through Clavularia polyps. Important anatomical features have been labelled. Images show; (A) a section through the entire polyp and (B) a zoomed in view of the coelenteron in a polyp section.
Colony Structure
All polyps within a colony are physiologically connected through basal stolons. Within the stolons are entodermal tubes, called solenia, which connect the coelenterons of individual polyps within the colony. Nutrients and resources are shared amongst the colony through solenia. Species within genus Clavularia can sometimes produce new zooids through lateral stolons which extend from the body wall of other zooids. Lateral stolons are only produced once a zooid reaches a certain height. Zooids produced via lateral stolons are also connected to the rest of the colony through solenia, but their gastrovascular cavities are not directly linked to the zooid which gave rise to them.
Sclerites
Clavularia coral species are soft corals, therefore lacking a calcium carbonate skeleton as seen in scleractinian coral. The soft body is instead structurally supported by calcium carbonate sclerites. Sclerites are found over most of the coral, covering the stolon mat, forming a calyx at the top of the anthostele, and being present on the underside of tentacles. Sclerites from the stolon, tentacles and calyx are morphologically distinct from one another (Weinberg, 1986). Sclerites also differ between species and genus, allowing them to be used as a diagnostic tool in classifying an organism. Weinberg (1986) assessed the structure of sclerites from numerous species from genus Clavularia. Sclerites were similar amongst all the assessed species, with sclerites typically resembling thorned, worty spindles. These sclerites were also often branched and/or fused together.
The spicules of the observed Clavularia organism reassembled those found by Weinberg (1986). However, to obtain the spicules from the observed specimen, the tissue had to be removed with bleach, meaning that it was not possible to determine which part of the animal the spicules originated from. For this reason, it was not possible to identify the specimen down to a species level.
Fig 4. The sclerites obtained from the Clavularia specimen observed using a scanning electron microscope. It is unknown where these sclerites were located in the specimen. The magnification and scale are also shown.
Secondary Metabolites
Secondary metabolites are produced in many Clavularia species. These secondary metabolites show cytotoxic and biotoxic properties which make them useful in predator defence and interspecific competition against neighbouring sessile organisms (Hashimoto et al., 2003). It was unknown whether secondary metabolites were produced by symbiotic zooxanthellae or by the host coral itself, however studies have now shown that the coral produces these secondary metabolites (Suzuki et al., 2003; Hashimoto et al., 2003). Different types of secondary metabolites are produced in a species-specific manner, with many medically important prostanoids only being found in Clavularia viridis (Hashimoto et al., 2003).
Medical Potential of Secondary Metabolites
C. viridis specific prostanoids (clavulones) have shown promising anti-tumour properties in several studies (Honda et al., 1985; Iguchi et al., 1985; Liang et al., 2008). Clavulones have a similar structure to mammalian prostaglandin hormones, which are also a type of prostanoid (Hashimoto et al., 2003). Mammalian prostaglandin hormones have been previously associated with physiological regulation of the cell cycle (Honda et al., 1985). A break down in cell cycle regulation has been associated with the development of cancer (Hashimoto et al., 2003).
A study by Honda et al. (1985) showed a potent antileukemic effect of clavulones on human promyelocytic leukemia cells. Clavulones strongly inhibited leukemic cell growth, also showing selectively for leukemia cells over human cervical cancer cells and healthy human cells. The mechanism through which cell growth was inhibited was thought to be through blocking of the G1 phase of the cell cycle. Another study by Iguchi et al. (1985) isolated chlorovulones from C. viridis which showed an even stronger anti-tumor response to leukemia cells than previously isolated clavulones.
The action of clavulones and chlorovulones were further assessed in a study by Liang et al. (2008). The study compared the cytotoxicity of extracts from numerous soft corals on human oral squamous cell carcinoma (SCC). Of the studied species, extracts from C. viridis had the most potent effect on cell growth and cell adhesion in SCC. The mechanism of inhibition was similar to that in leukemia, however extracts were also thought to accelerate the caspase-3 stage, leading to cell apoptosis.
The above studies show promising results for the use of clavulones and chlorovulones in future cancer treatment. These compounds were effective against multiple types of cancer, however further studies need to be conducted to increase understanding of the mechanisms of inhibition before treatments are developed.
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Biogeographic Distribution | |
Clavularia coral species are widely distributed throughout the Indopacific and Atlantic. Species can be found at a range of depths; however, they are confined to shallow depths where their zooxanthellae can photosynthesise. Most often located on reef slopes and rubble zones.
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Evolution and Systematics | |
Phylum: Cnidaria
Subphylum: Anthozoa
Subclass: Octocorallia
Order: Alcyonacea
Suborder: Stolonifera
Family: Clavulariidae
Genus: Clavularia
The basal group within phylum Cnidaria is still under debate, however Anthozoa in widely considered to be basal. Within Anthozoa, Hexacorallia and Octocorallia are each considered to be monophyletic groups. The relationships within Octocorallia remain poorly understood, with few clear synapomorphies used to separate taxa within this group (Conti-Jerpe & Freshwater, 2017).
The suborder Stolonifera, and subsequent families, are a loose grouping of polyphyletic species (Conti-Jerpe & Freshwater, 2017). Evolutionary relationships amongst taxa are still unclear and groupings are bound to change with future overhauls of Stolonifera (Conti-Jerpe & Freshwater, 2017). Due to this lack of knowledge, defining characteristics such as skeletal structure and colony organisation fall on a continuum between orders, meaning that no distinct boundaries can be made between some taxa (Bayer, 1981). As a result, taxa within Stolonifera can be hard to define.
Information on the evolutionary history of Clavularia and higher taxonomic levels such as Octocorallia is limited due to infrequent appearances in the fossil record (Poliseno, 2016). The soft bodied nature of octocorals results in high post-mortem degradation, which leads to difficulty in identification of the limited fossils (Poliseno, 2016).
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Conservation and Threats | |
Little information on the conservation status of species within Clavularia is known. Two species, C. Carpediem and C. crassa, are listed on the IUCN red list, being of least concern and data deficient respectively.
While there are no known Clavularia specific threats, there are many threats to broader reef communities. These threats include climate change, invasive species, and land development. Climate change has lead to increased ocean temperatures, amongst other factors, which have been subsequently attributed to coral bleaching events (Brown, 1996; Hughes et al., 2003). The affected areas have shown a reduction in species diversity and a shift in the relative abundances of some species, due to differential responses to bleaching (Hughes et al., 2003). Invasive species further contribute to ecological shifts within reef ecosystems, often acting in synergy with climate change (Occhipinti-Ambrogi, 2007). Pollution from agriculture and land development have also been attributed as large causes in decreasing coral species richness (Hughes et al., 2003).
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References | |
Alino, P. M., Sammarco, P. W., Coll, J. C. (1992). Competitive strategies in soft corals (coelenterata, octocorallia). IV. Environmentally induced reversals in competitive superiority. Marine Ecology Progress Series, 81, 129 – 145.
Bastidas, C., Benzie, J. A. H., Fabricius, K. E. (2002). Genetic differentiation among populations of the brooding soft coral Clavularia koellikerion the Great Barrier Reef. Coral Reefs, 21, 233 – 241.
Bayer, F. (1981). Key to the genera of Octocorallia exclusive of Pennatulacea (Coelenterata: Anthozoa), with diagnoses of new taxa. Proceedings of the Biological Society of Washington, 94, 902 – 947.
Benayahu, Y. (1989). Reproductive Cycle and Developmental Processes During Embryogenesis of Clavularia hamra (Cnidaria, Octocorallia). Acta Zoologica, 70, 29 – 36.
Benayahu, Y., Loya, Y. (1977). Space partitioning by stony corals, soft corals and benthic algae on the coral reefs of the northern Gulf of Eilat (Red Sea). Helgolander wiss. Meeresunters, 30, 362 – 382.
Brown, B. E. (1996). Coral bleaching: causes and consequences. Coral Reefs, 16, 129 – 138.
Conti-Jerpe, I. E., Freshwater, D. W. (2017). Hedera caerulescens (Alcyonacea : Alcyoniidae), a new genus and species of soft coral from the temperate North Atlantic: invasive in its known range?. Invertebrate Systematics, 31, 723 – 733.
Dinesen, Z. D. (1983). Patterns in the distribution of soft corals across the central great barrier reef. Coral Reefs, 1, 229 – 236.
Hashimoto, N., Fujiwara, S., Watanabe, K., Iguchi, K., Tsuzuki, M. (2003). Localization of Clavulones, Prostanoids with Antitumor Activity, Within the Okinawan Soft Coral Clavularia viridis (Alcyonacea, Clavulariidae): Preparation of a High-Purity Symbiodinium Fraction Using a Protease and a Detergent. Lipids, 38, 991 – 997.
Honda, A., Yamamoto, Y., Mori, Y., Yamada, Y., Kikuchi, H. (1985). Antileukemic effect of coral-prostanoids clavulones from the stolonifera Clavularia viridis on human myeloid leukemia (HL-60) cells. Biochemical and Biophysical Research Communications, 130, 515 – 523.
Hughes, T. P., Baird, A. H., Bellwood, D. R., Card, M., Connolly, S. R., Folke, C., Grosberg, R., Hoegh-Guldberg, O., Jackson, J. B. C., Kleypas, J., Lough, J. M., Marshall, P., Nystrom, M., Palumbi, S. R., Pandolfi, J. M., Rosen, B., Roughgarden, J. (2003). Climate change, human impacts, and the resilience of coral reefs. Science, 301, 929 – 933.
Iguchi, K., Kaneta, S., Mori, K., Yamada, Y., Honda, A., Mori, Y. (1985). Chlorovulones, new halogenated marine prostanoids with an antitumor activity from the stolonifera Clavularia viridis Quoy and Gaimard. Tetrahedron Letters, 26, 5787 – 5790.
Liang, C. H., Wang, G. H., Liaw, C. C., Lee, M. F., Wang, S. H., Cheng, D. L., Chou, T. H. (2008). Extracts from Cladiella australis, Clavularia viridis and Klyxum simplex (soft corals) are capable of inhibiting the growth of human oral squamous cell carcinoma cells. Marine Drugs, 6, 595 – 606.
Occhipinti-Ambrogi, A. (2007). Global change and marine communities: alien species and climate change. Marine Pollution Bulletin, 55, 342 – 352.
Poliseno, A. (2016). Speciation, Evolution and Phylogeny of some Shallow-water Octocorals (Cnidaria: Anthozoa). Geobiology, Ludwig-Maximilians-University, Munich Germany.
Satterlie, R. A., Case, J. F. (1980). Neurobiology of the stoloniferan octocoral Clavularia sp. The Journal of Experimental Zoology, 212, 87 – 99.
Suzuki, M., Watanabe, K., Fujiwara, S., Kurasawa, T., Wakabayashi, T., Tsuzuki, M., Iguchi, K., Yamori, T. (2003). Isolation of peridinin-related norcarotenoids with cell growth inhibitory activity from the cultured dinoflagellate of Symbiodinium sp., a symbiont of the Okinawan soft coral Clavularia viridis, and analysis of fatty acids of the dinoflagellate. Chemical and Pharmaceutical Bulletin (Tokyo), 51, 724 – 727.
Weinberg, S. (1986). Mediterranean octocorallia: description of Clavularia carpediem n. sp. and synonymy of Clavularia crassa and C. ochracea on etho-ecological grounds. Bijdragen tot de dierkunde, 56, 232 – 246.
Williams, G. C. (2000). A new genus and species of stoloniferous octocoral (Anthozoa: Clavulariidae) from the Pacific coast of North America. Zoological medicine Leiden, 73, 333 – 343.
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