Abstract
Although the Galapagos are famous for their unique biodiversity, many groups of marine invertebrates from this isolated archipelago remain understudied or not investigated. One such group is the zoanthids (Order Zoantharia, =Zoanthidea, =Zoanthiniaria), anthozoans (Cnidaria) found in marine ecosystems worldwide. Zoanthid taxonomy has been in a state of disorganization and neglect due in large part to the morphological plasticity within species and questions about the accuracy of traditionally used morphological and ecological characteristics. However, recent studies utilizing molecular methodology combined with morphology have proven to be very useful in understanding zoanthid diversity. The results of a survey of zoanthids from the Galapagos and the east Pacific are reported in this study. Shallow water (<35 m) zoanthid specimens were identified using the molecular markers mitochondrial 16S ribosomal DNA (mt 16S rDNA), cytochrome oxidase subunit I (COI) gene, and the internal transcribed spacer of ribosomal DNA (ITS-rDNA). From the collected specimens seven putative zoanthid species-level clades from three known genera (Zoanthus, Palythoa, Parazoanthus) were identified at the molecular level. These identifications were further supported by morphological and ecological data. While almost all specimens belonged to known zoanthid genera, based on unique molecular and ecological data one group of specimens (designated unknown zoanthid sp. “03-103”) is potentially a novel undescribed genus. Additionally, the remaining three azooxanthellate Parazoanthus clades may also be undescribed new species, but due to the overall lack of zoanthid research and descriptions from neighboring areas (East Pacific, west coast of South America) further research is needed to clearly ascertain this. Additionally, notes on the four observed nominal azooxanthellate zoanthid species and a key to all eight nominal (seven from known genera, one from a potentially new genus) shallow water zoanthid species found thus far in the Galapagos Islands are provided.
Similar content being viewed by others
References
Beaulieu SE (2001) Life on glass houses: sponge stalk communities in the deep sea. Mar Biol 138:803–817
Breedy O, Guzman HM (2005) A new species of alcyonacean octocoral from the Galápagos archipelago. J Mar Biol Assoc UK 85:801–807
Breedy O, Guzman HM (2007) A revision of the genus Leptogorgia Milne Edwards & Haime, 1857 (Coelenterata: Octocorallia: Gorgoniidae) in the eastern Pacific. Zootaxa 1407:1–90
Breedy O, Hickman CP Jr, Williams G (in press) Octocoral research in the Galapagos Islands. Galapagos Res
Bustamante R, Collins KJ, Bensted-Smith R (2000) Biodiversity conservation in the Galápagos Marine Reserve. Bull Ins Roy Sci Natur Belg Supp 70:31–38
Bustamante RH, Wellington GM, Branch GM, Edgar GJ, Martinez P, Rivera F, Smith F, Witman J (2002) Outstanding marine features. In: Bensted-Smith R (ed) A biodiversity vision for the Galápagos Islands, Charles Darwin Foundation and World Wildlife Fund, Puerto Ayora, pp 38–67
Cairns SD (1991) A revision of the ahermatypic Scleractinia of the Galápagos and Cocos Islands. Smithson Contrib Zool 504:1–44
Cairns SD (2001) A generic revision and phylogenetic analysis of the Dendrophylliidae (Cnidaria: Scleractinia). Smithson Contrib Zool 615:1–75
Calder DR, Mallinson JJ, Collins K, Hickman CP Jr (2003) Additions to the hydroids (Cnidaria) of the Galápagos, with a list of species reported from the islands. J Nat Hist 37:1173–1218
Darwin C (1859) On the origin of species. John Murray, London
Fautin DG (2007) Hexacorallians of the world. http://geoportal.kgs.ku.edu/hexacoral/anemone2/index.cfm
Fautin DG, Hickman CP Jr, Daly M, Molodtsova T (2007) Shallow-water sea anemones (Cnidaria: Anthozoa: Actiniaria) and tube anemones (Cnidaria: Anthozoa: Ceriantharia) of the Galápagos Islands. Pac Sci 61:549–573
Glynn PW (2003) Coral communities and coral reefs of Ecuador. In: Cortes J (ed) Latin American coral reefs. Elsevier Sciences BV, Amsterdam, pp 449–472
Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52:696–704
Heath H (1906) A new species of Semper’s larva from the Galapagos Islands. Zool Anz 30:171–175
Hickman CP Jr (1998) A field guide to sea stars and other echinoderms of Galápagos. Sugar Spring Press, Lexington
Hickman CP Jr, Finet Y (1999) A field guide to marine molluscs of Galápagos. Sugar Spring Press, Lexington
Hickman CP Jr, Zimmerman TL (2000) A field guide to crustaceans of Galápagos. Sugar Spring Press, Lexington
Huang D, Meier R, Todd PA, Chou LM (2008) Slow mitochondrial COI sequence evolution at the base of the metazoan tree and its implications for DNA barcoding. J Mol Evol 66:167–174
Kimura M (1980) A simple method for estimating evolutionary rates pf base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120
Muirhead A, Tyler PA, Thurston MH (1986) Reproductive biology and growth of the genus Epizoanthus (Zoanthidea) from the north-east Atlantic. J Mar Biol Assoc UK 66:131–143
Pax F, Muller I (1962) Die Anthozoenfauna der Adria. Fauna et Flora Adriatica, III. Institut za Oceanografiju i Ribastvo, Split
Reimer JD, Ono S, Takishita K, Fujiwara Y, Tsukahara J (2004) Reconsidering Zoanthus spp. diversity: molecular evidence of conspecificity within four previously presumed species. Zool Sci 21:517–525
Reimer JD, Ono S, Iwama A, Tsukahara J, Maruyama T (2006a) High levels of morphological variation despite close genetic relatedness between Zoanthus aff. vietnamensis and Zoanthus kuroshio (Anthozoa: Hexacorallia). Zool Sci 23:755–761
Reimer JD, Ono S, Iwama A, Tsukahara J, Takishita K, Maruyama T (2006b) Morphological and molecular revision of Zoanthus (Anthozoa: Hexacorallia) from southwestern Japan with description of two new species. Zool Sci 23:261–275
Reimer JD, Ono S, Takishita K, Tsukahara J, Maruyama T (2006c) Molecular evidence suggesting species in the zoanthid genera Palythoa and Protopalythoa (Anthozoa: Hexacorallia) are congeneric. Zool Sci 23:87–94
Reimer JD, Hirano S, Fujiwara Y, Sinniger F, Maruyama T (2007a) Morphological and molecular characterization of Abyssoanthus nankaiensis, a new family, new genus and new species of deep-sea zoanthid (Anthozoa: Hexacorallia: Zoantharia) from a northwest Pacific methane cold seep. Invertebr Systemat 21:255–262
Reimer JD, Takishita K, Ono S, Maruyama T (2007b) Diversity and evolution in the zoanthid genus Palythoa (Cnidaria: Hexacorallia) utilizing nuclear ITS-rDNA. Coral Reefs 26:399–410
Reimer JD, Takishita K, Ono S, Tsukahara J, Maruyama T (2007c) Molecular evidence suggesting intraspecific hybridization in Zoanthus (Anthozoa: Hexacorallia). Zool Sci 24:346–359
Reimer JD, Ono S, Tsukahara J, Iwase F (2008) Molecular characterization of the zoanthid genus Isaurus (Anthozoa: Hexacorallia) and its zooxanthellae (Symbiodinium spp). Mar Biol 153:351–363
Reimer JD, Hickman CP Jr (in press) Preliminary survey of zooxanthellate zoanthids (Cnidaria: Hexacorallia) of the Galápagos and associated symbiotic dinoflagellates (Symbiodinium spp.). Galápagos Res
Rodriguez F, Oliver JL, Marin A, Medina JR (1990) The general stochiatic model of nucleotide substitution. J Theor Biol 142:485–501
Ronquist F, Huelsenbeck JP (2003) Bayesian phylogenetic inference under mixed models. Bioinformatics (Oxf) 19:1572–1574
Senna A (1907) Nuove larve pelagiche di Ceriantidi e di Zoanttidi, Nota preliminare. Monit Zool Ital 18:96–102
Shearer TL, van Oppen MJH, Romano SL, Worheide G (2002) Slow mitochondrial DNA sequence evolution in the Anthozoa (Cnidaria). Mol Ecol 11:2475–2487
Sinniger F (2006) Zoantharia of New Caledonia. In: Payri C, Richier De Forges B (eds) Compendium of marine species from New Caledonia. Documents scientifiques et techniques II (7). IRD Editions, Noumea. pp 127–128
Sinniger F, Montoya-Burgos JI, Chevaldonne P, Pawlowski J (2005) Phylogeny of the order Zoantharia (Anthozoa, Hexacorallia) based on mitochondrial ribosomal genes. Mar Biol 147:1121–1128
Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The ClustalX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882
Verrill AE (1869) Review of the corals and polyps of the west coast of America. Trans Conn Acad Arts Sci 1:377–558
Williams GC, Breedy O (2004) The Panamic gorgonians genus Pacifigorgia (Octocorallia: Gorgoniidae) in the Galápagos archipelago, with descriptions of three new species. Proc Calif Acad Sci 55:55–88
Acknowledgments
Graham Edgar, Angel Chiriboga, Luis Vinueza, and William C. Ober generously helped with sampling and photography. CPH is indebted to the staff of the Biomarine Laboratory of the Charles Darwin Research Station (Pto. Ayora, Santa Cruz Island) for logistical field help. The captain and crew of the Mabel (December 2004), the Flamingo (January 2003), the Golindrina (November 2003), the San Jose (May 2002), and the Beagle III (June 2001) helped make sampling possible. JDR thanks Dr. Kiyotaka Takishita, as well as Masoru Kawato and Dr. Hirokazu Kuwahara (all JAMSTEC), for research assistance. Specimen collection during the 2006 and 2007 trips were partially funded by the Darwin Initiative Project. JDR was additionally partially financed by a Japan Society for the Promotion of Science post-doctoral fellowship (#P04868) at JAMSTEC (Yokosuka, Japan), the 21st Century Center of Excellence Program (COE) at the University of the Ryukyus, and a grant from the Fujiwara Natural History Foundation (Tokyo, Japan). Three anonymous reviewers greatly helped improve this manuscript.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by: Biology Editor Dr. Ruth Gates.
Rights and permissions
About this article
Cite this article
Reimer, J.D., Sinniger, F. & Hickman, C.P. Zoanthid diversity (Anthozoa: Hexacorallia) in the Galapagos Islands: a molecular examination. Coral Reefs 27, 641–654 (2008). https://doi.org/10.1007/s00338-008-0376-5
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00338-008-0376-5