Coral Reefs

, Volume 34, Issue 3, pp 899–904 | Cite as

Christmas tree worms of Indo-Pacific coral reefs: untangling the Spirobranchus corniculatus (Grube, 1862) complex

  • Demian A. Willette
  • Abril R. Iñiguez
  • Elena K. Kupriyanova
  • Craig J. Starger
  • Tristan Varman
  • Abdul Hamid Toha
  • Benedict A. Maralit
  • Paul H. Barber


Christmas tree worm is the common name of a group of colorful serpulid polychaetes from the genus Spirobranchus that are symbionts of hermatypic corals. As is increasingly common with reef-associated organisms, Spirobranchus is arranged as a complex of species with overlapping geographic ranges. Current species delimitations based largely on opercular morphology are problematic because of high intraspecific variation. Here, a multi-gene phylogeny of the Spirobranchus corniculatus complex, which tentatively includes S. corniculatus, S. cruciger, and S. gaymardi, sampled from the Coral Triangle, Australia, and Fiji, was reconstructed to test whether the complex includes three genetically distinct lineages identifiable by their opercula. Maximum-likelihood analyses of nuclear and mitochondrial markers revealed a single, monophyletic clade for the S. corniculatus complex. Furthermore, the genetic and morphological variation observed is not geographically based, indicating that the former S. corniculatus complex of three morphospecies is a single, morphologically variable species across the Central Indo-Pacific. Resolving the taxonomy of S. corniculatus presents novel opportunities to utilize this tentative bio-indicator species for monitoring reef health.


Annelida Mitochondrial DNA Nuclear DNA Polychaeta 



We thank the governments and people of Australia, Fiji, Indonesia, and the Philippines for providing research permission. Funding for the collection of samples was provided by NSF Grant OISE-0730256 to Kent Carpenter and Paul Barber, and a Conservation International support to Paul Barber. We thank Joshua Drew of Columbia University for sample collection in Fiji and Mudjie Santos, Kent Carpenter, Rachel Ravago-Gotanco, and the National Fisheries Research and Development Institute for logistics and laboratory support in the Philippines, and Harry A. ten Hove for assistance in specimen identification. We thank O. Paderanga, A. Semenov, and E. Wong for their photos.


  1. Ahrens JB, Borda E, Barroso R, Paiva PC, Campbell AM, Wolf A, Nugues MM, Rouse GW, Schulze A (2013) The curious case of Hermodice carunculata (Annelida: Amphinomidae): evidence for genetic homogeneity throughout the Atlantic Ocean and adjacent basins. Mol Ecol 22:2280–2291PubMedCrossRefGoogle Scholar
  2. Barber P, Boyce SL (2006) Estimating diversity of Indo-Pacific coral reef stomatopods through DNA barcoding of stomatopod larvae. Proc R Soc B 273:2053–2061PubMedCentralPubMedCrossRefGoogle Scholar
  3. Barroso R, Klautau M, Solé-Cava AM, Paiva PC (2010) Eurythoe complanata (Polychaeta: Amphinomidae), the cosmopolitan’ fireworm, consists of at least three cryptic species. Mar Biol 157:69–80CrossRefGoogle Scholar
  4. Boore JL, Brown WM (2000) Mitochondrial genomes of Galathealinum, Helobdella, and Platynereis: Sequence and gene arrangement comparisons indicate that Pogonophora is not a phylum and Annelida and Arthropoda are not sister taxa. Mol Biol Evol 17:87–106PubMedCrossRefGoogle Scholar
  5. Burnette AB, Struck TH, Halanych KM (2005) Holopelagic Poeobius meseres (“Poeobiidae”, Annelida) is derived from benthic flabelligerid worms. Biol Bull 208:213–220PubMedCrossRefGoogle Scholar
  6. Carr CM, Hardy SM, Brown TM, Macdonald TA, Hebert PDN (2011) A tri-oceanic perspective: DNA barcoding reveals geographic structure and cryptic diversity in Canadian polychaetes. PLoS One 6:e22232PubMedCentralPubMedCrossRefGoogle Scholar
  7. Dawson MN, Jacobs DK (2001) Molecular evidence for cryptic species of Aurelia aurita (Cnidaria, Scyphozoa). Biol Bull 200:92–96PubMedCrossRefGoogle Scholar
  8. Edgar R (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797PubMedCentralPubMedCrossRefGoogle Scholar
  9. Elwood HJ, Olsen GJ, Sogin ML (1985) The small-subunit ribosomal RNA gene sequences from the hypotrichus ciliates Oxytricha nova and Stylonchia pustulata. Mol Biol Evol 2:399–410PubMedGoogle Scholar
  10. Fiege D, ten Hove HA (1999) Redescription of Spirobranchus gaymardi (Quatrefages, 1866) (Polychaeta: Serpulidae) from the Indo-Pacific with remarks on the Spirobranchus giganteus complex. Zool J Linn Soc 126:355–364Google Scholar
  11. Halt MN, Kupriyanova EK, Cooper SJB, Rouse GW (2009) Naming species with no morphological indicators: species status of Galeolaria caespitosa (Annelida, Serpulidae) inferred from nuclear and mitochondrial gene sequences and morphology. Invertebr Syst 23:205–222CrossRefGoogle Scholar
  12. Harty M (2011) Christmas tree worms (Spirobranchus giganteus) as a potential bioindicator species of sedimentation stress in coral reef environments of Bonaire, Dutch Caribbean. Physis: J Mar Sci 9:20–30Google Scholar
  13. Kimura M (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120PubMedCrossRefGoogle Scholar
  14. Lance S (2012) Pink pigment lesions on massive Porites in Mo’orea: Distribution and Environmental Factors. Student paper.
  15. Landry C, Geyer LB, Arakaki Y, Uehara T, Palumbi SR (2003) Recent speciation into the Indo-West Pacific: rapid evolution of gamete recognition and sperm morphology in cryptic species of sea urchin. Proc R Soc Lond B Biol Sci 270:1839–1847CrossRefGoogle Scholar
  16. Lehrke J, ten Hove HA, Macdonald TA, Bartolomaeus T, Bleidorn C (2007) Phylogenetic relationships of Serpulidae (Annelida: Polychaeta) based on 18S rDNA sequence data, and implications for opercular evolution. Org Divers Evol 7:195–206CrossRefGoogle Scholar
  17. Librado P, Rozas J (2009) DnaSP v5: A software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452PubMedCrossRefGoogle Scholar
  18. Meyer A, Bleidorn C, Rouse GW, Hausen H (2008) Morphological and molecular data suggest a cosmopolitan distribution of the polychaete Proscoloplos cygnochaetus Day, 1954 (Annelida, Orbiniidae). Mar Biol 153:879–889CrossRefGoogle Scholar
  19. Nygren A (2014) Cryptic polychaete diversity: a review. Zool Scr 43:172–183CrossRefGoogle Scholar
  20. Nygren A, Norlinder E, Panova M, Pleijel F (2011) Colour polymorphism in the polychaete Harmothoe imbricata (Linnaeus, 1767). Mar Biol Res 7:54–62CrossRefGoogle Scholar
  21. Rambaut A (2002) Se-Al: Sequence alignment editor Ver. 2.0a11,
  22. Sanciangco JC, Carpenter KE, Etnoyer PJ, Moretzsohn F (2013) Habitat availability and heterogeneity and the Indo-Pacific warm pool as predictors of marine species richness n the tropical Indo-Pacific. PLoS One 8:e56245PubMedCentralPubMedCrossRefGoogle Scholar
  23. Scaps P, Denis V (2008) Can organisms associated with live scleractinian corals be used as indicators of coral reef status? Atoll Res Bull 566:1–20CrossRefGoogle Scholar
  24. Sienes PM, Willette DA, Romena L, Alvior C, Estacion J (2014) Biodiversity and the discovery of a cryptic species within a valued crab fishery in the Philippines. Philipp Sci Letters 7:317–323Google Scholar
  25. Smith R (1985) Photoreceptors of serpulid polychaetes. Ph.D. Thesis, James Cook University of North QueenslandGoogle Scholar
  26. Stella JS, Pratchett MS, Hutchings PA, Jones GP (2011) Coral-associated invertebrates: diversity, ecological importance and vulnerability to disturbance. Oceanogr Mar Biol Annu Rev 49:43–104Google Scholar
  27. Tamura K, Peterson D, Peterson N, Stecher GM, Nei M, Kumar S (2011) MEGA5: Molecular and Evolutionary Genetics Analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739PubMedCentralPubMedCrossRefGoogle Scholar
  28. ten Hove HA (1970) Serpulinae (Polychaeta) from the Caribbean: I - The genus Spirobranchus. Studies on the Fauna of Curaçao and other Caribbean Islands 32:1–57Google Scholar
  29. ten Hove HA (1994) Serpulidae (Annelida: Polychaeta) from the Seychelles and Amirante Islands. Neth Indian Ocean Progr Cruise Rep 2:107–116Google Scholar
  30. Thomas RC, Willette DA, Carpenter KE, Santos MD (2014) Hidden diversity in sardines: genetic and morphological evidence for cryptic species in the Goldstripe Sardinella Sardinella gibbosa (Bleeker, 1849). PLoS One 9:e84719PubMedCentralPubMedCrossRefGoogle Scholar
  31. Tuberville JM, Higgins DG, Gibson TJ (1994) Dueterostome phylogeny and the sister group of the chordates: evidence from molecules and morphology. Mol Biol Evol 11:648–655Google Scholar
  32. Walsh P, Metzger A, Higuchi R (1991) Chelex 100 as a medium for simple extraction of DNA for PCR based typing from forensic material. Biotechniques 10:506–513PubMedGoogle Scholar
  33. White TJ, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ (eds) PCR protocols: a guide to methods and applications. Academic Press, New York, pp 315–322Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • Demian A. Willette
    • 1
  • Abril R. Iñiguez
    • 1
  • Elena K. Kupriyanova
    • 2
  • Craig J. Starger
    • 3
  • Tristan Varman
    • 4
  • Abdul Hamid Toha
    • 5
  • Benedict A. Maralit
    • 5
    • 6
  • Paul H. Barber
    • 1
  1. 1.Department of Ecology and Evolutionary BiologyUniversity of CaliforniaLos AngelesUSA
  2. 2.Australian Museum Research InstituteSydneyAustralia
  3. 3.Science and Technology Policy Fellowships, Center of Science, Policy and Society ProgramsAmerican Association for the Advancement of ScienceWashingtonUSA
  4. 4.Department of Environmental Science and ManagementUniversity of NewcastleOurimbahAustralia
  5. 5.Fisheries DepartmentState University of PapuaManokwariIndonesia
  6. 6.Genetic Fingerprinting LaboratoryNational Fisheries Research and Development InstituteQuezon CityPhilippines

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