A new association between goblet worms (Entoprocta) and xeniid corals (Cnidaria)

Short Communication
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Abstract

The phylum Entoprocta is a cryptic group of sessile, primarily marine filter-feeding invertebrates, commonly called goblet worms. During a recent survey of mesophotic reef diversity at Green Island (Ludao, Taiwan) in February 2017, zooids of the solitary entoproct Loxosomella sp. were first recorded in association with a Cespitularia-like xeniid soft coral collected at 40 m depth. This association was observed on all 14 coral colonies inspected, where their density reached 5.4 (±1.4) zooids per polyp (n = 5). This record not only constitutes the first report of entoprocts in Taiwan, but is also the first documentation of an association between entoprocts and octocorals, and highlights the importance of examining other host candidates in this taxon for a better understanding of their diversity. The exact nature of this potential symbiotic relationship needs to be elucidated, but the isolation of intact zooids suggests that Loxosomella sp. lives on the surface of coral tissues by a tight attachment of their foot. Loxosomella sp. could perhaps benefit from protection offered by soft corals against predators and competitors. The pinnate polyps and fleshy morphology of the coral colony can also assist in sediment removal, which may help entoprocts to avoid burial. Overall, the discovery of this association increases the known diversity of the associated fauna of octocorals, but possible implications in coral fitness still need to be explored.

Keywords

Entoprocta Xeniidae Soft coral Epizoitism Association Coral symbiome 

Supplementary material

12526_2017_766_Fig4_ESM.jpg (168 kb)
Online Resource 1

Distribution of Entoprocta. a. worldwide b. in East-Asia region with a focus on the distribution of the genus Loxosomella. Data from the current study and Global Biodiversity Information Facility (www.gbif.org, accessed 2017/06/27) map of the distribution of Entoprocta (a) with a focus on the Kuroshio region and the distribution of the Loxosomella (b) (JPEG 168 kb)

12526_2017_766_MOESM1_ESM.eps (2.5 mb)
High resolution image (EPS 2549 kb)
12526_2017_766_Fig5_ESM.jpg (273 kb)
Online Resource 2

Mesophotic benthic assemblage at Guiwan site (at 40 m depth) (JPEG 272 kb)

12526_2017_766_MOESM2_ESM.eps (74.6 mb)
High resolution image (EPS 76346 kb)

References

  1. Alamaru A, Brokovich E, Loya Y (2016) Four new species and three new records of benthic ctenophores (family: Coeloplanidae) from the Red Sea. Mar Biodivers 46:261–279. doi:10.1007/s12526-015-0362-4 CrossRefGoogle Scholar
  2. Benayahu Y, Loya Y (1981) Competition for space among coral-reef sessile organisms at Eilat, Red Sea. Bull Mar Sci 31:514–522Google Scholar
  3. Benayahu Y, Loya Y (1985) Settlement and recruitment of a soft coral: why is Xenia macrospiculata a successful colonizer? Bull Mar Sci 36:177–188Google Scholar
  4. Benayahu Y, Jeng MS, Perkol-Finkel S, Dai CF (2004) Soft corals (Octocorallia: Alcyonacea) from southern Taiwan: II. Species diversity and distributional patterns. Zool Stud 43:548–560Google Scholar
  5. Boero F, Bouillon J, Gravili C (2000) A survey of Zanclea, Halocoryne and Zanclella (Cnidaria, hydrozoa, Anthomedusae, Zancleidae) with description of new species. Ital J Zool 67:93–124CrossRefGoogle Scholar
  6. Borisanova AO, Chernyshev AV, Neretina TV, Stupnikova AN (2015) Description and phylogenetic position of the first abyssal solitary kamptozoan species from the Kuril-Kamchatka trench area: Loxosomella profundorum sp. nov. (Kamptozoa: Loxosomatidae). Deep-Sea Res II 111:351–356CrossRefGoogle Scholar
  7. Cheng TC (1970) Symbiosis: organisms living together. Pegasus, New YorkGoogle Scholar
  8. Cheng YR, Ho MJ, Dai CF (2016) Four anchimolgid copepods (Poecilostomatoida: Anchimolgidae) associated with the scleractinian coral Pavona explanulata (Lamarck, 1816) in Taiwan. Zootaxa 4174:274–290. doi:10.11646/zootaxa.4174.1.19 CrossRefPubMedGoogle Scholar
  9. Dai CF, Horng S (2009) Scleractinia Fauna of Taiwan I. The complex group. National Taiwan University, TaipeiGoogle Scholar
  10. Dunn CW, Hejnol A, Matus DQ, Pang K, Browne WE, Smith SA, Seaver E, Rouse GW, Obst M, Edgecombe GD, Sørensen MV, Haddock SHD, Schmidt-Rhaesa A, Okusu A, Kristensen RM, Wheeler WC, Martindale MQ, Giribet G (2008) Broad phylogenomic sampling improves resolution of the animal tree of life. Nature 452:745–749. doi:10.1038/nature06614 CrossRefPubMedGoogle Scholar
  11. Fabricius K, Alderslade P (2001) Soft corals and sea fans: a comprehensive guide to the tropical shallow water genera of the central-west Pacific, the Indian Ocean and the Red Sea. Australian Institute of Marine Science, TownsvilleGoogle Scholar
  12. FitzPatrick SK, Liberatore KL, Garcia JR, Burghardt I, Colman DR, Moquin SA, Takacs-Vesbach CD, Shepherd UL (2012) Symbiodinium diversity in the soft coral Heteroxenia sp. and its nudibranch predator Phyllodesmium lizardensis. Coral Reefs 31:895–905. doi:10.1007/s00338-012-0913-0 CrossRefGoogle Scholar
  13. Fontana S, Keshavmurthy S, Hsieh HJ, Denis V, Kuo C-Y, Hsu CM, Leung JKL, Tsai WS, Wallace CC, Chen CA (2012) Molecular evidence shows low species diversity of coral-associated hydroids in Acropora corals. PLoS One 7:e50130. doi:10.1371/journal.pone.0050130 CrossRefPubMedPubMedCentralGoogle Scholar
  14. Fox HE, Pet JS, Dahuri R, Caldwell RL (2003) Recovery in rubble fields: long-term impacts of blast fishing. Mar Pollut Bull 46:1024–1031. doi:10.1016/S0025-326X(03)00246-7 CrossRefPubMedGoogle Scholar
  15. Fuchs J, Iseto T, Hirose M, Sundberg P, Obst M (2010) The first internal molecular phylogeny of the animal phylum Entoprocta (Kamptozoa). Mol Phylogenet Evol 56:370–379. doi:10.1016/j.ympev.2010.04.009 CrossRefPubMedGoogle Scholar
  16. Gates RD, Ainsworth TD (2011) The nature and taxonomic composition of coral symbiomes as drivers of performance limits in scleractinian corals. J Exp Mar Biol Ecol 408:94–101. doi:10.1016/j.jembe.2011.07.029 CrossRefGoogle Scholar
  17. Giorgi A, Monti M, Galli P, Montano S (2016) Entoprocta-sponge associations in the Indian Ocean. Coral Reefs 35:611. doi:10.1007/s00338-016-1418-z CrossRefGoogle Scholar
  18. Harmer SF (1915) The Polyzoa of the Siboga expedition part 1. Entoprocta, Ctenostomata and Cyclostomata. Siboga-Expeditie 28a:1–180Google Scholar
  19. Hausdorf B, Helmkampf M, Meyer A, Witek A, Herlyn H, Bruchhaus I, Hankeln T, Struck TH, Lieb B (2007) Spiralian phylogenomics supports the resurrection of Bryozoa comprising Ectoprocta and Entoprocta. Mol Biol Evol 24:2723–2729. doi:10.1093/molbev/msm214 CrossRefPubMedGoogle Scholar
  20. Hoang BX, Sawall Y, Al-Sofyani A, Wahl M (2015) Chemical versus structural defense against fish predation in two dominant soft coral species (Xeniidae) in the Red Sea. Mar Ecol Prog Ser 23:129–137. doi:10.3354/ab00614 Google Scholar
  21. Hoeksema BW (2017) The hidden biodiversity of tropical coral reefs. Biodiversity 18:8-12. doi:10.1080/14888386.2017.1307787
  22. Hoeksema BW, Waheed Z, Alamaru A (2013) Out of sight: aggregations of epizoic comb jellies underneath mushroom corals. Coral Reefs 32:1065. doi:10.1007/s00338-013-1078-1 CrossRefGoogle Scholar
  23. Iseto T (2017) Review of the studies of Japanese entoprocts (Entoprocta). In: Motokawa M, Kajihara H (eds) Species diversity of animals in Japan. Springer, Japan, pp 445–467CrossRefGoogle Scholar
  24. Iseto T, Nielsen C (2016). Entoprocta. Accessed through: World Register of Marine Species at http://www.marinespecies.org/aphia.php?p=taxdetails&id=1271 on 2017–07-03
  25. Iseto T, Sugiyama N, Hirose E (2008) A new sponge-inhabiting Loxosomella (Entoprocta: Loxosomatidae) from Okinawa Island, Japan, with special focus on foot structure. Zool Sci 25:1171–1178. doi:10.2108/zsj.25.1171 CrossRefPubMedGoogle Scholar
  26. Janes MP (2013) Distribution and diversity of the soft coral family Xeniidae (coelentera: Octoccorallia) in Lembeh Strait, Indonesia. Galaxea, J Coral Reef Stud 15(Special Issue):195–200. doi:10.3755/galaxea.15.195 CrossRefGoogle Scholar
  27. Jeng MS, Huang HD, Dai CF, Hsiao YC, Benayahu Y (2011) Sclerite calcification and reef-building in the fleshy octocoral genus Sinularia (Octocorallia: Alcyonacea). Coral Reefs 30:925–933. doi:10.1007/s00338-011-0765-z CrossRefGoogle Scholar
  28. Maggioni D, Montano S, Seveso D, Galli P (2016) Molecular evidence for cryptic species in Pteroclava krempfi (hydrozoa, Cladocorynidae) living in association with alcyonaceans. Syst Biodivers 14:484–493. doi:10.1080/14772000.2016.1170735 CrossRefGoogle Scholar
  29. Maida M, Sammarco PW, Coll JC (1995) Effects of soft corals on scleractinian coral recruitment. I: directional allelopathy and inhibition of settlement. Mar Ecol Prog Ser 121:191–202. doi:10.3354/meps121191 CrossRefGoogle Scholar
  30. McFadden CS, Reynolds AM, Janes MP (2014) DNA barcoding of xeniid soft corals (Octocorallia: Alcyonacea: Xeniidae) from Indonesia: species richness and phylogenetic relationships. Syst Biodivers 12:247–257. doi:10.1080/14772000.2014.902866 CrossRefGoogle Scholar
  31. Montano S, Seveso D, Galli P, Puce S, Hoeksema BW (2015) Mushroom corals as newly recorded hosts of the hydrozoan symbiont Zanclea sp. Mar Biol Res 11:773–779. doi:10.1080/17451000.2015.1009467 CrossRefGoogle Scholar
  32. Montano S, Maggioni D, Galli P, Hoeksema BW (2017) A cryptic species in the Pteroclava krempfi species complex (hydrozoa, Cladocorynidae) revealed in the Caribbean. Mar Biodivers 47:83–89. doi:10.1007/s12526-016-0555-5 CrossRefGoogle Scholar
  33. Nielsen C (1964) Studies on Danish Entoprocta. Ophelia 1:1–76CrossRefGoogle Scholar
  34. Nielsen C (2013) Entoprocta. eLS, John Wiley and Sons, ltd, Chichester. doi: 10.1002/9780470015902.a0001596.pub2
  35. Pantos O, Bythell JC (2010) A novel reef coral symbiosis. Coral Reefs 29:761–770. doi:10.1007/s00338-010-0622-5 CrossRefGoogle Scholar
  36. Paps J, Baguñà J, Riutort M (2009) Lophotrochozoa internal phylogeny: new insights from an up-to-date analysis of nuclear ribosomal genes. Proc R Soc Lond B 276:1245–1254. doi:10.1098/rspb.2008.1574 CrossRefGoogle Scholar
  37. Ribas-Deulofeu L, Denis V, De Palmas S, Kuo CY, Hsieh JH, Chen CA (2016) Structure of benthic communities along the Taiwan latitudinal gradient. PLoS One 11:e0160601. doi:10.1371/journal.pone.0160601 CrossRefPubMedPubMedCentralGoogle Scholar
  38. Seveso D, Montano S, Pica D, Maggioni D, Galli P, Allevi V, Bastari A, Puce S (2016) Pteroclava krempfi-octocoral associations: new information from Indian Ocean and Red Sea. Mar Biodivers 46:483–487. doi:10.1007/s12526-015-0368-y CrossRefGoogle Scholar
  39. Sheppard CRC, Ateweberhan M, Chen AC, Harris A, Jones R, Keshavmurthy S, Lundin C, Obura D, Purkis S, Raines P, Riegl B, Schleyer MH, Sheppard ALS, Tamelander J, Turner JR, Visram S, Yang SY (2013) Coral reefs of the Chagos archipelago, Indian Ocean. In: CRC S (ed) Coral reefs of the UK overseas territories. Springer, Netherlands, pp 241–252CrossRefGoogle Scholar
  40. Silvestro D, Michalak I (2012) raxmlGUI: a graphical front-end for RAxML. Org Diver Evol 12:335–337. doi:10.1007/s13127-011-0056-0 CrossRefGoogle Scholar
  41. Stamatakis A (2006) RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22:2688–2690. doi:10.1093/bioinformatics/btl446 CrossRefPubMedGoogle Scholar
  42. Sugiyama N, Iseto T, Hirose M, Hirose E (2010) Reproduction and population dynamics of the solitary entoproct Loxosomella plakorticola inhabiting a demosponge, Plakortis sp. Mar Ecol Prog Ser 415:73–82. doi:10.3354/meps08747 CrossRefGoogle Scholar
  43. Vergés A, Steinberg PD, Hay ME, Poore AGB, Campbell AH, Ballesteros E, Heck KL Jr, Booth DJ, Coleman MA, Feary DA, Figueira W, Langlois T, Marzinelli EM, Mizerek T, Mumby PJ, Nakamura Y, Roughan M, van Sebille E, Gupta AS, Smale DA, Tomas F, Wernberg T, Wilson SK (2014) The tropicalization of temperate marine ecosystems: climate-mediated changes in herbivory and community phase shifts. Proc R Soc B 281:20140846. doi:10.1098/rspb.2014.084 CrossRefPubMedPubMedCentralGoogle Scholar
  44. Wanninger A, Fuchs J, Haszprunar G (2007) Anatomy of the serotonergic nervous system of an entoproct creeping-type larva and its phylogenetic implications. Invertebr Biol 126:268–278. doi:10.1111/j.1744-7410.2007.00097.x CrossRefGoogle Scholar
  45. Wasson K (2002) A review of the invertebrate phylum Kamptozoa (Entoprocta) and synopsis of kamptozoan diversity in Australia and New Zealand. Trans R Soc S Aust 126:1–20Google Scholar
  46. Wild C, Naumann MS (2013) Effect of active water movement on energy and nutrient acquisition in coral reef-associated benthic organism. Proc Natl Acad Sci U S A 110:8767–8768. doi:10.1073/pnas.1306839110 CrossRefPubMedPubMedCentralGoogle Scholar
  47. Yamano H, Sugihara K, Goto K, Kazama T, Yokoyama K, Okuno J (2012) Ranges of obligate coral-dwelling crabs extend northward as their hosts move north. Coral Reefs 31:663. doi:10.1007/s00338-012-0893-0 CrossRefGoogle Scholar
  48. Yokobori S, Iseto T, Asakawa S, Sasaki T, Shimizu N et al (2008) Complete nucleotide sequences of mitochondrial genomes of two solitary entoprocts, Loxocorone allax and Loxosomella aloxiata: implications for lophotrochozoan phylogeny. Mol Phylogenet Evol 47:612–628. doi:10.1016/j.ympev.2008.02.013 CrossRefPubMedGoogle Scholar
  49. Ziegler M, FitzPatrick SK, Burghardt I, Liberatore KL, Leffler AJ, Takacs-Vesbach C, Shepherd UL (2014) Thermal stress response in a dinoflagellate-bearing nudibranch and the octocoral on which it feeds. Coral Reefs 33:1085–1099. doi:10.1007/s00338-014-1204-8 CrossRefGoogle Scholar

Copyright information

© Senckenberg Gesellschaft für Naturforschung and Springer-Verlag GmbH Germany 2017

Authors and Affiliations

  1. 1.Institute of OceanographyNational Taiwan UniversityTaipeiTaiwan
  2. 2.Green Island Marine Research Station, Biodiversity Research CenterAcademia SinicaTaipeiTaiwan

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