Rhodactis indosinensis Carlgren, 1943
Fig 1. Rhodactis indosinensis on the intertidal shores of Sisters' Island, Singapore. (Photography by Oh Ren Min)
Carpet corallimorphs, belonging to the species Rhodactis indosinensis1 , are a group of inconspicuous animals you would have probably missed on a walk along Singapore's intertidal shores. On first glance, these animals are commonly mistaken for sea anemones or corals. However, they belong to a seperate order - Corallimorpharia. There are approximately 51 species of corallimorphs that are distributed across the shallow to deep sea habitats worldwide. Rhodactis indosinensis is 1 of 8 corallimorph species identified in Singapore2 . Due to their vibrant colours and ease of propagation in tanks, corallimorphs are highly popular amongst aquarists. Another place you might have encountered these animals is in a saltwater aquarium shop!
Fig 2. Rhodactis indosinensis specimens from subtidal and intertidal habitats in Singapore.
(Photography by Oh Ren Min)
As little information is available publicly on the corallimorphs of Singapore, this species page serves as a general introduction to carpet corallimorphs for both hobbyists and the general public interested in learning more about these nondescript animals.
Globally, Rhodactis indosinensis is distributed across the Indo-pacific3 . In Singapore, species sightings have been recorded only on the southern shores, in both subtidal and intertidal habitats. A possible explanation for this pattern, is the differing environmental parameters on both shores. For example, the northern shores are more nutrient rich and have restricted water flow due to the Causeway linking Singapore and Malaysia4 .
Fig 4. Map of corallimorph sightings in Singapore.
Rhodactis indosinensis is represented by a red box. Acronyms for localities follow WildSingapore.
(Map designed by Neo Mei Lin, permission granted)
Rhodactis indosinensis reproduces by both sexual and asexual reproduction5 . Environmental factors such as temperature can influence asexual reproduction in this species but more detailed studies need to be conducted to ascertain this. As global temperatures are predicted to rise, such knowledge is timely and could be relevant to other closely-related species such as sea anemones6 .
In the aquarium trade, asexual reproduction in Rhodactis indosinensis allows for a method known as 'fragging' to be used for propagation. Click on the video7 below to see how it is done! *Note that the corallimorph in the video is not Rhodactis indosinensis but the method used is consistent amongst all corallimorphs.
Little is known about the diet of these animals in the wild, though it is likely that they rely on a combination of plankton and products from symbiotic zooxanthellae as a source of energy8 . In aquarium settings, Rhodactis indosinensis has been observed consuming krill flakes and other premixed aquarium food.
Corallimorph consuming food in an aquarium setting 9
Boradly, the ecological relationships of corallimorphs with other reef organisms or the habitat, has not been as well studied as scleractinians. There remains a lack of substantial body of research on Rhodactis indosinensis. However, other species from the same genus have been subject to ecological studies. Results from these studies could be suggestive of the ecological role of Rhodactis indosinensis on reefs. 2 aspects of the species ecology are particularly interesting and will be discussed here.
Fig 5. Rhodactis species occupying areas on reefs in Singapore. Red arrows indicate an individual.
Left: Rhodactis indosinensis on a subtidal reef in Singapore. (Photography by Samuel Chan, permission granted)
Right: Rhodactis inchoata (sister species of Rhodactis indosinensis) on an intertidal reef in Pulau Hantu, Singapore. (Photography by Oh Ren Min)
Phase shifts describe the phenomenon when certain species dominate a large area of a habitat by outcompeting other species, creating a new stable ecological state. In the marine environment, the most well-known example is the coral-macroalgae shift10 . Macroalgae covers most of the reef when corals succumb to poor environmental conditions. Thus, glimpses of a shift occurring serves as an indicator of a decline in reef health. Apart from the coral-macroalgae shift, the shift to a corallimorph dominated reef environment has been documented as well11 12 13 .
Some Rhodactis species exhibit competitive behaviour when in close proximity to other benthic reef organisms. Other Rhodactis species have been shown to outcompete corals in certain reefs, though this has yet to be tested for Rhodactis indosinensis. A study on the competitive success of Corallimorpharia in reefs found another Rhodactis species - Rhodactis rhodostoma, to have a damaging effect on Scleractinians14 . Scleractinians found near the R. rhodostoma had observable lesions and scars, suggesting that both groups were engaged in competition for space on the reef flat.
Fig 6. Rhodactis species in contact with a hard coral. Red arrows indicate damaged coral near the area of contact.
(Photography by Samuel Chan, permission granted)
In the marine aquarium trade, Rhodactis indosinensis is commonly known as the hairy mushroom. They remain a popular choice amongst beginner aquarists and high-end collectors due to the ease of propagation and vibrant colours15 . The ornamental value of corallimorphs has risen over the years. In 2007, the corallimorph Ricordea florida was the 12th most harvested species from the wild, compared to 1994 data where no corallimorph species was ranked in the top 1516 . The immense popularity of corallimorphs in the ornamental trade would raise concerns on the population levels in the wild. But till date, the conservation status of corallimorphs has yet to be assessed.
Fig 7. Large pink hairy mushroom in aquarium setting17 .
The species name was probably influenced by the geographic localities of syntypes examined by Carlgren. All specimens examined were collected from the Indo-Pacific region18 . The species name has underwent no subsequent revision thereafter. In a 2007 paper, Tkachenko et al.19 misspelled Rhodactis indosinensis as Discosoma indosinensis, assigning the species to the wrong genus. Fautin has since clarified this misspelling by synonymising it with the original species name20 .
No synonyms exist for this species. Common names encountered outside scientific literature include the hairy mushroom coral and carpet corallimorph (from specimens found on Singapore's intertidal shores). The former is a misnomer as corallimorphs are not corals21 .
Fig 8. Excerpt of original taxonomic description18
Rhodactis indosinensis was described in 1943 by Oskar Carlgren - one of the first few taxonomists to work extensively on Corallimorphs, based on a series of specimens collected by Dr. C Dawydoff and Professor Sixten Bock18 . The species description provided by Carlgren was done well. Detailed descriptions of both the internal and external morphology, using morphological characters such as cnidae size were included. It is worth noting that, Carlgren's taxonomic expertise is originally in Actiniaria (sea anemones). Many morphological characters he uses are similar to those in his taxonomic work on anemones and will be discussed in subsequent paragraphs. This could have also contributed to the trend of taxonomists specialising in anemones but also working concurrently corallimorphs such as Dr Daphne Fautin, amongst many others. Carlgren does not specify the species concept employed.
Fig 9. Rhodactis indosinensis syntype collected from Vietnam, Cochinchina, Poulo Condore
(Photography by Nicholas Yap, permission granted)
No holotypes have been designated for this species. Twenty-one syntypes are deposited in the Naturhistoriska Riksmuseet, Stockholm, Sweden. These were collected from 4 localities - 2 in Vietnam, 1 in Cambodia and 1 in Japan. The syntype from Japan remains reported as missing20 .
Morphological characters used overlap with those in Actiniaria, as mentioned earlier. Such a trend suggests the close resemblance in morphology between both orders, further complicating phylogenetic placement within the Hexacorallia - a group consisting of Actiniara, Scleractinia and Corallimorpharia. External morphology alone is sufficient for species identification of corallimorphs in Singapore2 . The taxonomic key below summarizes morphological characters present in all Rhodactis species.
Fig 10. Taxonomic key to genus Rhodactis 18
External morphological characters
The mouth is raised in the centre of the oral disc. Tentacles can be separated into 2 categories: marginal and discal, determined by the location on the oral disc. A distinguishing morphological character of Rhodactis indosinensis is the presence of branched discal tentacles covering most of its oral disc. Simple tentacles are present on the mound leading towards the animal's mouth. Some individuals (e.g. Fig 5.) have an empty space surrounding the mouth.
Tentacles are usually the same colour as the oral disc but the tips may be of a different colour. Colour is highly variable between individuals thus cannot be used as a species level morphological character.
Fig 11. External morphological characters (Photography by Oh Ren Min)
Internal morphological characters
Nematocysts of the following types are present in Rhodactis indosinensis: atrichs, holotrichs, microbasic b-mastigophores, microbasic p-mastigophores. Nematocyst composition and size varies between species. For example, Rhodactis inchoata lacks microbasic p-mastigophores 18 . Nematocysts are commonly used to capture prey or for defense, similar to sea anemones.
Fig 12. Internal morphology (Photography by Oh Ren Min)
The evolutionary debate on the phylogenetic placement of Corallimorpharia within the Anthozoa led to a surge in comparative genomics papers attempting to resolve the group's placement, using a range of molecular markers. Corallimorpharia like all other Cnidarians, have a much slower-evolving cytochrome-oxidase 1 (CO1) gene compared to the other Metazoans (multi-cellular organisms), thus CO1 cannot be used as a barcoding gene22 . Other common regions used for barcoding include the Internal Transcribed Spacer (ITS) of the ribosomal RNA transcription unit. These rapidly evolving regions are useful for species delineation amongst closely related species and has been successfully used to seperate Rhodactis species23 . Thus, the ITS region could possibly be used as a barcoding region for Rhodactis indosinensis. In 2014, Lin et al.21 published the corallimorph mitochondrial genome arrangement (Fig 8), providing useful information for future barcoding work on these animals.
Fig 13. Mitochondrial genome structure of Corallimorpharians. Rhodactis indosinensis corresponds to Type CII.21
The latest phylogenetic placement of corallimorphs establishes the group as a monophyletic clade, sister to scleractinians (Fig 9)24 . The tree is the most robust till date, using transcriptome data instead of relying solely traditional mitochondrial or nuclear markers which have been subject to criticism . Phylogenetic reconstruction methods used here were robust. Both maximum likelihood and Bayesian inference was used to construct the phylogeny, using concatenated and partitioned amino acid and nucleotide datasets to account for different rates of evolution. Under all reconstruction methods, corallimorphs form a monophyletic clade, sister to scleractinians (Fig 10).
Fig 14. Maximum likelihood phylogeny built using amino acid sequences of 291 nuclear genes with JTT+GAMMA+I model.
Nodes labelled 1,2,3,4 are fully supported (bootstrap support = 100, posterior probability = 1)24
Fig 15. Bootstrap support values for phylogeny24
'Naked' coral hypothesis
Prior to the use of transcriptomic data in comparative phylogenetics, the placement of corallimorphs on the tree of life has long been subject to debate. Before DNA sequencing was available, no consensus on the phylogenetic placement of corallimorphs could be reached based on inferences from morphological characters. The random or radial distribution of tentacles on the oral disc of corallimorphs and a mouth in the centre, resembled the structure observed in anemones25 . Corallimorphs have paired identical mesentries arranged radially25 . This arrangement is also similarly observed in hard corals and anemones26 . Combined with a gap in the Scleractinia fossil record suggesting that, either fossils had yet to be found, or corals had lost their skeleton hence the ability to 'fossilize', this led Stanley27 to propose the widely debated Naked Coral hypothesis
2 main lines of argument dominated the debate.
1) Corallimorphs were corals that had lost their calcium carbonate skeleton. The corresponding inference was that Scleractinia (corals) was paraphyletic since Corallimorpharia was not placed within the Scleractinia clade.
2) Corallimorphs formed a sister group to corals and Scleractinia monophyly holds.
Fig 16. The 2 lines of argument in the 'Naked Coral' debate24
As DNA sequencing was made available, the field shifted towards building a molecular phylogeny in an attempt to resolve the placement of Corallimorpharia. Initial phylogenetic analyses by Medina et al.28 using the amino acid alignment from mitochondrial protein coding genes, found support for Scleractinian paraphyly. However, as pointed out in Lin et al.24 , rates of evolution differ between each gene of the mitochondrial genome. Kitahara et al.29 also found that compositional biases of nucleotides affected phylogenetic analyses using amino acid sequence data. Other studies conducted using different molecular markers such as nuclear markers30 and transcriptomes24 31 rejected the Naked Coral hypothesis. Corallimorphs from a monophyletic sister group to Scleractinians. Thus, highlighting the importance of using multiple molecular markers for phylogenetic analyses.
For genomic data, the full mitochondrial genome by Lin et al. (2014) is available on GenBank (Accession ID: NC_027103). The mitochondrial cytochrome B (AB441349.1) and COX1 gene (AB441264.1) have been deposited in GenBank as well30 21 .
Taxonomic information is available at the Hexacorallians of the World online database curated by Dr Daphne Fautin32 .
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