Saturday, 6 June 2020

Spirobranchus spp.: Christmas Tree Worms associated with new hosts found in Puerto Rico and the Netherlands Antilles.

Caribbean Christmas Tree Worms, Spirobranchus spp., are considered host generalists in their associations with Anthozoan (Scleractinia) and Hydrozoan (Millepora) Stony Corals. As planktonic larvae, they settle on Coral surfaces and start secreting a calcareous tube to be used as a dwelling. This tube usually becomes overgrown by the host Coral (except for its opening) and may get encapsulated deep inside the Coral skeleton. In this manner, the well-protected Worms grow and survive predation and other hazards, allowing them to live for over four decades. When the host Corals are overgrown by other organisms, such as Octocorals and Sponges, these may act as secondary hosts.

In a paper published in the journal Diversity on 21 March 2020, Bert Hoeksema of the Taxonomy and Systematics Group at the Naturalis Biodiversity Center, the Groningen Institute for Evolutionary Life Sciences at the University of Groningen, and the Institute of Biology Leiden at Leiden University, Jaaziel García-Hernández of the Marine Genomic Biodiversity Laboratory at the University of Puerto Rico - Mayagüez, Godfried van Moorsel of Ecosub and the ANEMOON Foundation, Gabriël Olthof also of the Taxonomy and Systematics Group at the Naturalis Biodiversity Center, and the Institute of Biology Leiden at Leiden University, and Harry ten Hove, again of the Taxonomy and Systematics Group at the Naturalis Biodiversity Center, report two new primary hosts (Scleractinians) and two new secondary hosts (a Zoantharian Soft Coral and an Ascidian colonial Sea Squirt), discovered during recent surveys (2015–2019) in the southern and eastern Caribbean, as well as in the Greater Antilles.

The Coral–Worm associations occurred in shallow subtidal water (less than 4 m depth), with the Knobby Brain Coral, Pseudodiploria clivosa, hosting Spirobranchus giganteus at St. Eustatius in the northern Leeward Islands, and the Golfball Coral, Favia fragum, hosting both Spirobranchus giganteus and Spirobranchus polycerus at Bonaire in the southern Leeward Islands. The secondary host observations, both for Spirobranchus giganteus, involved the Zoantharian Palythoa caribaeorum at Puerto Rico and the Ascidian Trididemnum solidum at Bonaire and Curaçao. Palythoa caribaeorum represents a first record as a secondary host for a species of the order Zoantharia. Until now, the only other Anthozoan secondary hosts were species in the order Alcyonacea (subclass Octorallia), whereas Trididemnum solidum represents an entirely new host phylum, the Chordata. The only other non-Anthozoan secondary hosts known to date are Sponges (Porifera).

A Coral of Pseudodiploria clivosa at 2 m depth, Scubaqua House Reef, St. Eustatius, Eastern Caribbean (2015) hosting Spirobranchus giganteus: (a) overall view and (b) close-up. Hoeksema et al. (2020).

The two new Scleractinian hosts are both typical for shallow subtidal water near the shoreline (less than 4 m depth), where a lack of previous surveys may explain why they have not previously been reported. The new records of secondary hosts are remarkable because these encrusting Animals are known to be aggressive in competition for space with Scleractinians by allelopathy (the production of harmful biochemicals) and can be abundant on shallow reef flats and slopes, where they usually outcompete and kill Scleractinian Corals by overgrowing them. In both cases, the Christmas Tree Worms survive by withstanding this overgrowth and maintain an open space near the tube opening.

Favia fragum hosting Spirobranchus spp. at 3–4 m depth, dive site 'Front Porch', Bonaire, Southern Caribbean (2019). (a)–(c) Spirobranchus giganteus: overall view (a), overgrown tube section indicated by red arrow (b); antler-shaped opercular spines showing dark pink colouration indicated by yellow arrow (c). (d) Spirobranchus polycerus: two individuals, one showing white spines on its operculum (blue arrow). Hoeksema et al. (2020).

Hoeksema et al.'s new host records confirm two Caribbean Christmas tree worms as generalist symbionts capable of infesting a large spectrum of host Corals. They are also strong survivors when their primary hosts become overgrown by more aggressive competitors for space. Previous host records mostly concern  Spirobranchus giganteus, but Hoeksema et al. also report a new host Coral for Spirobranchus polycerus. This worm species occurs in shallow water (less than 4 m depth), whereas Spirobranchus giganteus is commonly found down to 40 m depth. Both Spirobranchus species can easily be distinguished, as Spirobranchus giganteus shows long dark pink opercular spines, whereas those of Spirobranchus polycerus are short and white. Furthermore, Spirobranchus giganteus may be larger than Spirobranchus polycerus and usually shows six to seven (maximum eight) whorls in its branchial spires, whereas Spirobranchus polycerus has two to three (maximum five).

Palythoa caribaeorum acting as a secondary host for Spirobranchus giganteus at 5 m depth, Cayo Media Luna (La Parguera Natural Reserve), Puerto Rico, Greater Antilles (2017): (a) Worm extended and (b) retracted, showing the tube opening surrounded by dead Coral; damage to the Zoantharian host caused by the operculum of the extended Worm indicated by a black arrow. Hoeksema et al. (2020).

Hoeksema et al.'s observations suggest that future surveys may discover other hosts for both Spirobranchus species with the possibility of more host overlap. Whether such host sharing is related to their phylogenetic affinities or to ecological similarities (e.g., overlapping bathymetric distributions) is an open question that merits assessment.

Trididemnum solidum acting as a secondary host for Spirobranchus giganteus in the Southern Caribbean: (a), (b) dive site 'Thousand Steps', Bonaire (2019); (c) Marie Pampoen, Curaçao, 12 m depth (2017); (d), (e) Daaibooi Bay, Curaçao (2017). Extended Worms (a), (d) and the same individuals retracted, showing an open space in front of the Worm tube mouth (b), (e). Hoeksema et al. (2020).

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