Caribbean Christmas tree worms (Annelida: Polychaeta: Serpulidae:
Spirobranchus) are considered host generalists in their associations with anthozoan (Scleractinia) and hydrozoan (
Millepora) stony corals [
1,
2,
3,
4]. 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 [
5] and other hazards, allowing them to live for over four decades [
6]. When the host corals are overgrown by other organisms, such as octocorals and sponges, these may act as secondary hosts [
7,
8].
The long lists of Caribbean host species suggest that the recorded number has reached a maximum [
1,
2,
3,
4]. However, recent surveys (2015–2019) in the southern and eastern Caribbean, as well as in the Greater Antilles, enabled us to establish new records of two primary hosts (scleractinians) and two secondary hosts (a zoantharian and an ascidian).
The coral–worm associations occurred in shallow subtidal water (<4 m depth), with
Pseudodiploria clivosa (Ellis & Solander, 1786) hosting
Spirobranchus giganteus (Pallas, 1766) at St. Eustatius (
Figure 1) and
Favia fragum (Esper, 1795) hosting both
S. giganteus (
Figure 2a–c) and
S. polycerus (Schmarda, 1861) (
Figure 2d) at Bonaire. The secondary host observations, both for
S. giganteus, involved the zoantharian
Palythoa caribaeorum (Duchassaing & Michelotti, 1860) at Puerto Rico (
Figure 3) and the ascidian
Trididemnum solidum (Van Name, 1902) at Bonaire and Curaçao (
Figure 4).
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) [
7], whereas
T. solidum represents an entirely new host phylum, viz. Chordata. The only other non-anthozoan secondary hosts known to date are sponges (Porifera) [
8].
The two new scleractinian hosts are both typical for shallow subtidal water near the shoreline (<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 [
9,
10] and can be abundant on shallow reef flats and slopes, where they usually outcompete and kill scleractinian corals by overgrowing them [
9,
10]. In both cases, the Christmas tree worms survive by withstanding this overgrowth and maintain an open space near the tube opening (
Figure 3d,
Figure 4b,e).
Our 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
S. giganteus [
1,
2,
3,
4], but here we also report a new host coral for
S. polycerus. This worm species occurs in shallow water (<4 m depth) [
5], whereas
S. giganteus is commonly found down to 40 m depth [
1]. Both
Spirobranchus species can easily be distinguished [
5], as
S. giganteus shows long dark pink opercular spines (
Figure 2c), whereas those of
S. polycerus are short and white (
Figure 2d). Furthermore,
S. giganteus may be larger than
S. polycerus [
5] and usually shows six to seven (maximum eight) whorls in its branchial spires, whereas
S. polycerus has two to three (maximum five) [
11]. Our 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.
Author Contributions
Conceptualization and supervision, B.W.H.; methodology, illustrations and funding acquisition, B.W.H., J.E.G.-H., G.W.N.M.v.M., and G.O., investigation, B.W.H., J.E.G.-H., G.W.N.M.v.M., G.O. and H.A.t.H.; writing—original draft preparation, B.W.H.; writing—review and editing, B.W.H., J.E.G.-H., G.W.N.M.v.M., G.O. and H.A.t.H. All authors have read and agreed to the published version of the manuscript.
Funding
Fieldwork at Bonaire was supported by the WWF Netherlands Biodiversity Fund, the Treub Maatschappij - Society for the Advancement of Research in the Tropics, and by the Nature of the Netherlands program of Naturalis Biodiversity Center.
Acknowledgments
We thank the staff of CARMABI (Curaçao) and CNSI (St. Eustatius) for their hospitality and assistance during the fieldwork. We thank STENAPA and Scubaqua Dive Center (Sint Eustatius), the Dive Shop (Curaçao), STINAPA, DCNA and Dive Friends (Bonaire) for logistic support. We are grateful to two anonymous reviewers for their constructive remarks on the manuscript.
Conflicts of Interest
The authors declare no conflict of interest. The funders had no role in the design of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript, or in the decision to publish the results.
References
- Hoeksema, B.W.; ten Hove, H.A. The invasive sun coral Tubastraea coccinea hosting a native Christmas tree worm at Curaçao, Dutch Caribbean. Mar. Biodivers. 2017, 47, 59–65. [Google Scholar] [CrossRef][Green Version]
- Hoeksema, B.W.; van Beusekom, M.; ten Hove, H.A.; Ivanenko, V.N.; van der Meij, S.E.T.; van Moorsel, G.W.N.M. Helioseris cucullata as a host coral at St. Eustatius, Dutch Caribbean. Mar. Biodivers. 2017, 47, 71–78. [Google Scholar] [CrossRef][Green Version]
- Martin, D.; Britayev, T.A. Symbiotic polychaetes revisited: An update of the known species and relationships (1998–2017). Oceanogr. Mar. Biol. Ann. Rev. 2018, 56, 371–448. [Google Scholar]
- Hoeksema, B.W.; Wels, D.; van der Schoot, R.J.; ten Hove, H.A. Coral injuries caused by Spirobranchus opercula with and without epibiotic turf algae at Curaçao. Mar. Biol. 2019, 166, 60. [Google Scholar] [CrossRef][Green Version]
- Hoeksema, B.W.; ten Hove, H.A. Attack on a Christmas tree worm by a Caribbean sharpnose pufferfish at St. Eustatius, Dutch Caribbean. Bull. Mar. Sci. 2017, 93, 1023–1024. [Google Scholar] [CrossRef]
- Nishi, E.; Nishihira, M. Age-estimation of the Christmas tree worm Spirobranchus giganteus (Polychaeta, Serpulidae) living buried in the coral skeleton from the coral-growth band of the host coral. Fish. Sci. 1996, 62, 400–403. [Google Scholar] [CrossRef][Green Version]
- Hoeksema, B.W.; Lau, Y.W.; ten Hove, H.A. Octocorals as secondary hosts for Christmas tree worms off Curaçao. Bull. Mar. Sci. 2015, 91, 489–490. [Google Scholar] [CrossRef]
- García-Hernández, J.E.; Hoeksema, B.W. Sponges as secondary hosts for Christmas tree worms at Curaçao. Coral Reefs 2017, 36, 1243. [Google Scholar] [CrossRef]
- Suchanek, T.H.; Green, D.J. Interspecific competition between Palythoa caribaeorum and other sessile invertebrates on St. Croix reefs, US Virgin Islands. Proc. 4th Int. Coral Reef Symp. 1981, 2, 679–684. [Google Scholar]
- Bak, R.P.M.; Sybesma, J.; van Duyl, F.C. The ecology of the tropical compound ascidian Trididemnum solidum. II. Abundance, growth and survival. Mar. Ecol. Prog. Ser. 1981, 6, 43–52. [Google Scholar] [CrossRef]
- ten Hove, H.A. Serpulinae (Polychaeta) from the Caribbean: I–The genus Spirobranchus. Stud. Fauna Curaçao Caribb. Is. 1970, 32, 1–57. [Google Scholar]
© 2020 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/).