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Morphological and molecular variability of the sea anemone Phymanthus crucifer (Cnidaria, Anthozoa, Actiniaria, Actinoidea)

Published online by Cambridge University Press:  31 July 2014

Ricardo González-Muñoz*
Affiliation:
Unidad Multidisciplinaria de Docencia e Investigación en Sisal (UMDI-Sisal), Facultad de Ciencias, Universidad Nacional Autónoma de México (UNAM), Puerto de Abrigo, Sisal, C.P. 97356 Yucatán, México Posgrado en Ciencias del Mar y Limnología (PCMyL), UNAM, Instituto de Ciencias del Mar y Limnología (ICMyL), Circuito Exterior, Ciudad Universitaria, C.P. 04510, México
Nuno Simões
Affiliation:
Unidad Multidisciplinaria de Docencia e Investigación en Sisal (UMDI-Sisal), Facultad de Ciencias, Universidad Nacional Autónoma de México (UNAM), Puerto de Abrigo, Sisal, C.P. 97356 Yucatán, México
Maite Mascaró
Affiliation:
Unidad Multidisciplinaria de Docencia e Investigación en Sisal (UMDI-Sisal), Facultad de Ciencias, Universidad Nacional Autónoma de México (UNAM), Puerto de Abrigo, Sisal, C.P. 97356 Yucatán, México
José Luis Tello-Musi
Affiliation:
Laboratorio de Zoología, Facultad de Estudios Superiores Iztacala (FES-I), UNAM, Avenida de los Barrios 1, Los Reyes Iztacala, C.P. 54090 Estado de México, México
Mercer R. Brugler
Affiliation:
Division of Invertebrate Zoology, Sackler Institute for Comparative Genomics, American Museum of Natural History, Central Park West at 79th Street, New York, NY 10024, USA Biological Sciences Department, NYC College of Technology (CUNY), 300 Jay Street, Brooklyn, NY 11201, USA
Estefanía Rodríguez
Affiliation:
Division of Invertebrate Zoology, Sackler Institute for Comparative Genomics, American Museum of Natural History, Central Park West at 79th Street, New York, NY 10024, USA
*
Correspondence should be addressed to: R. González-Muñoz, Unidad Multidisciplinaria de Docencia e Investigación en Sisal (UMDI-Sisal), Facultad de Ciencias, Universidad Nacional Autónoma de México (UNAM), Puerto de Abrigo, Sisal, C.P. 97356 Yucatán, México Email: [email protected]

Abstract

The shallow water sea anemone Phymanthus crucifer exhibits three distinct morphotypes, characterized by the presence or absence of protuberances on the marginal tentacles, as well as intermediate forms. The taxonomic status of the different morphotypes and the diagnostic value of protuberances on the tentacles have been debated for this species and the family Phymanthidae. We analysed the external and internal anatomy, cnidae and three mitochondrial molecular markers for representatives of each of the three morphotypes. In addition, we address the putative monophyly of the family Phymanthidae based on molecular data. With the exception of the protuberances, our morphological and molecular results show no differences among the three morphotypes; thus, we consider this feature to be intraspecific variability within P. crucifer. Furthermore, molecular data reveal that the family Phymanthidae is not monophyletic. In addition, we discuss several diagnostic morphological features of the family Phymanthidae.

Type
Research Article
Copyright
Copyright © Marine Biological Association of the United Kingdom 2014 

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References

REFERENCES

Acuña, F.H., Excoffon, A.C. and Ricci, L. (2007) Composition, biometry and statistical relationships between the cnidom and body size in the sea anemone Oulactis muscosa (Cnidaria: Actiniaria). Journal of the Marine Biological Association of the United Kingdom 87, 415419.Google Scholar
Acuña, F.H., Excoffon, A.C., Zamponi, M.O. and Ricci, L. (2003) Importance of nematocysts in taxonomy of acontiarian sea anemones (Cnidaria, Actiniaria): a statistical comparative study. Zoologischer Anzeiger 242, 7581.CrossRefGoogle Scholar
Acuña, F.H. and Garese, A. (2009) The cnidae of the acrospheres of the corallimorpharian Corynactis carnea (Studer, 1878) (Cnidaria, Corallimorpharia, Corallimorphidae): composition, abundance and biometry. Belgian Journal of Zoology 139, 5057.Google Scholar
Acuña, F.H., Ricci, L. and Excoffon, A.C. (2011) Statistical relationships of cnidocyst sizes in the sea anemone Oulactis muscosa (Actiniaria: Actiniidae). Belgian Journal of Zoology 141, 3237.Google Scholar
Acuña, F.H., Ricci, L., Excoffon, A.C. and Zamponi, M.O. (2004) A novel statistical analysis of cnidocysts in acontiarian sea anemones (Cnidaria, Actiniaria) using generalized linear models with gamma errors. Zoologischer Anzeiger 243, 4752.CrossRefGoogle Scholar
Allcock, A.L., Watts, P.C. and Thorpe, J.P. (1998) Divergence of nematocysts of two colour morphs of the intertidal beadlet anemone Actinia equina . Journal of the Marine Biological Association of the United Kingdom 78, 821828.Google Scholar
Anderson, M.J. (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecology 26, 3246.Google Scholar
Andres, A. (1883) Le Attinie. Roma: Coi Tipi der Salviucci, 460 pp.Google Scholar
Ardelean, A. and Fautin, D.G. (2004) Variability in nematocysts from a single individual of the sea anemone Actinodendron arboreum (Cnidaria: Anthozoa: Actiniaria). Hydrobiologia 530/531, 187197.CrossRefGoogle Scholar
Bigger, C.H. (1988) The role of nematocysts in anthozoan aggression. In Hessinger, D.A. and Lenhoff, H.M. (eds) The biology of nematocysts. San Diego, CA: Academic Press, pp. 295308.Google Scholar
Brugler, M.R., France, S.C. and Opresko, D.M. (2013) The evolutionary history of the order Antipatharia (Cnidaria: Anthozoa: Hexacorallia) as inferred from mitochondrial and nuclear DNA: implications for black coral taxonomy and systematics. Zoological Journal of the Linnean Society 169, 312361.Google Scholar
Cairns, S., den Hartog, J.C. and Arneson, C. (1986) Class Anthozoa (Corals, Anemones). In Sterrer, W. and Schoepfer-Sterrer, C. (eds) Marine fauna and flora of Bermuda. New York: John Wiley & Sons, pp. 164194.Google Scholar
Carlgren, O. (1900) Ostafrikanische actinien. Mittheilungen aus dem Naturhistorischen Museum 17, 21144.Google Scholar
Carlgren, O. (1943) East-asiatic corallimorpharia and actiniaria. Kungliga Svenska Vetenskapsakademiens Handlingar 20, 143.Google Scholar
Carlgren, O. (1949) A survey of the Ptychodactiaria, Corallimorpharia and Actiniaria. Kunglia Svenska Vetenskaps—Akademiens Handlingar 1, 1121.Google Scholar
Chintiroglou, C.C. and Karalis, P. (2000) Biometric investigations on the cnidae of the Aegean colour morphs of Anemonia viridis . Journal of the Marine Biological Association of the United Kingdom 80, 543544.Google Scholar
Crowther, A.L. (2013) Character evolution in light of phylogenetic analysis and taxonomic revision of the zooxanthellate sea anemone families Thalassianthidae and Aliciidae. PhD thesis. University of Kansas, USA.Google Scholar
Daly, M. (2003) The anatomy, terminology, and homology of acrorhagi and pseudoacrorhagi in sea anemones. Zoologische Verhandenlinhen Leiden 345, 89101.Google Scholar
Dana, J.D. (1846) Zoophytes. Volume VII of the United States exploring expedition. During the years 1838, 1839, 1840, 1841, 1842. Under the command of Charles Wilkes, U.S.N. Philadelphia, PA: Lea and Blanchard, 740 pp.Google Scholar
Darriba, D., Taboada, G.L., Doallo, R. and Posada, D. (2012) jModelTest 2: more models, new heuristics and parallel computing. Nature Methods 9, 772.Google Scholar
Duchassaing, P. and Michelotti, G. (1860) Mémoire sur les Coralliaires des Antilles. Turin: Imprimerie Royale, 89 pp. doi: 10.5962/bhl.title.11388.Google Scholar
Duerden, J.E. (1895) On the genus Alicia (Cladactis), with an anatomical description of A. costae, Panc. Annals and Magazine of Natural History 15, 213218.Google Scholar
Duerden, J.E. (1897) The actiniarian family Aliciidae. Annals and Magazine of Natural History 20, 115.Google Scholar
Duerden, J.E. (1898) The Actiniaria around Jamaica. Journal of the Institute of Jamaica 2, 449465.Google Scholar
Duerden, J.E. (1900) Jamaican Actiniaria. Part II. Stichodactylinæ and Zoantheæ. Scientific Transactions of the Royal Dublin Society 7, 133208.Google Scholar
Duerden, J.E. (1902) Report of the Actinians of Porto Rico (Investigations of the aquatic resources and fisheries of Porto Rico by the U. S. Fish Commission Steamer Fish Hawk in 1899). Bulletin of the US Fish Commission 20, 323374.Google Scholar
Edmands, S. and Fautin, D.G. (1991) Redescription of Aulactinia veratra n. comb. (= Cnidopus veratra) (Coelenterata: Actiniaria) from Australia. Records of the Western Australian Museum 15, 5968.Google Scholar
Ehrenberg, C.G. (1834) Beiträge zur physiologischen Kenntniss der Corallenthiere im allgemeinen, und besonders des rothen Meeres, nebst einem Versuche zur physiologischen Systematik derselben. Abhandlungen der Königlichen Akademie der Wissenschaften zu Berlin 1, 225380.Google Scholar
Estrada-Flores, E., Peralta, L. and Rivas, P. (1982) Manual de Técnicas Histológicas. México: AGT, pp. 3265.Google Scholar
Fautin, D.G. (1988) Importance of nematocysts to actinian taxonomy. In Hessinger, D.A. and Lenhoff, H.M. (eds) The biology of nematocysts. San Diego, CA: Academic Press, Inc., pp. 487500.Google Scholar
Fautin, D.G. (1992) Cnidaria. In Adiyodi, K.G. and Rita, G. (eds) Reproductive biology of invertebrates, Volume 5 (sexual differentiation and behaviour). New Delhi: Oxford and IBH Publishing Company, pp. 3152.Google Scholar
Fautin, D.G. (2009) Structural diversity, systematics, and evolution of cnidae. Toxicon 54, 10541064.Google Scholar
Fautin, D.G. (2013) Hexacorallians of the world. Available at: http://geoportal.kgs.ku.edu/hexacoral/anemone2/index.cfm (accessed 1 July 2014).Google Scholar
Goloboff, P.A., Farris, J.S. and Nixon, K. C. (2008) TNT, a free program for phylogenetic analysis. Cladistics 24, 774786.Google Scholar
González-Muñoz, R., Simões, N., Sánchez-Rodríguez, J., Rodríguez, E. and Segura-Puertas, L. (2012) First inventory of sea anemones (Cnidaria: Actiniaria) of the Mexican Caribbean. Zootaxa 3556, 138.Google Scholar
Guindon, S., Dufayard, J.F., Lefort, V., Anisimova, M., Hordijk, W. and Gascuel, O. (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Systematic Biology 59, 307321.Google Scholar
Guindon, S. and Gascuel, O. (2003). A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Systematic Biology 52, 696704.Google Scholar
Haddon, A.C. (1898) The actiniaria of Torres Straits. Scientific Transactions of the Royal Dublin Society 6, 393520.Google Scholar
Haddon, A.C. and Shackleton, A.M. (1893) Description of some new species of actiniaria from Torres Straits. Scientific Proceedings of the Royal Dublin Society 8, 116131.Google Scholar
Haime, J. (1849) Sur le polypieroide d'un Leiopathes glaberrima . Annales des Sciences Naturelles 12, 224226.Google Scholar
Hellberg, M.E. (2006) No variation and low synonymous substitution rates in coral mtDNA despite high nuclear variation. BMC Evolutionary Biology 6, 24.Google Scholar
Jennison, B.L. (1981) Reproduction in three species of sea anemones from Key West, Florida. Canadian Journal of Zoology 59, 17081719.Google Scholar
Katoh, K., Misawa, K., Kuma, K.I. and Miyata, T. (2002) MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Research 30, 30593066.Google Scholar
Katoh, K., Kuma, K.I., Toh, H. and Miyata, T. (2005) MAFFT version 5: improvement in accuracy of multiple sequence alignment. Nucleic Acids Research 33, 511518.Google Scholar
Katoh, K. and Toh, H. (2008) Improved accuracy of multiple ncRNA alignment by incorporating structural information into a MAFFT-based framework. BMC Bioinformatics 9, 212.Google Scholar
Klunzinger, C.B. (1877) Die Korallthiere des Rothen Meeres. 1: Die Alcyonarien und Malacodermen. Berlin: Gutmann'schenBuchhandlung, 98 pp.Google Scholar
Lauretta, D., Häussermann, V., Brugler, M.R. and Rodríguez, E. (2014) Isoparactis fionae sp. nov. (Cnidaria: Anthozoa: Actiniaria) from Southern Patagonia with a discussion of the family Isanthidae. Organisms Diversity and Evolution 14, 3142.Google Scholar
Le Sueur, C.A. (1817) Observations on several species of the genus Actinia; illustrated by figures. Journal of the Academy of Natural Sciences of Philadelphia 1, 149154, 169–189.Google Scholar
Linnaeus, C. (1758) Systema Naturae. Regnum Animale. Lipsiae: Facsimile produced by the Cura Societatis Zoologiae Germanie Ed. 10.Google Scholar
Manchenko, G.P., Dautova, T.N. and Latypov, Y.Y. (2000) High level of genetic divergence between sympatric colour morphs of the littoral sea anemone Anthopleura orientalis (Anthozoa: Actiniaria). Biochemical Systematics and Ecology 28, 737750.CrossRefGoogle ScholarPubMed
McArdle, B.H. and Anderson, M.J. (2001) Fitting multivariate models to community data: a comment on distance-based redundancy analysis. Ecology 82, 290297.Google Scholar
Milne-Edwards, H. and Haime, J. (1851) Archives du Muséum d'Historie Naturelle. 5: Monographie des polypiers fossils des terrains palfozooques, pricidie d'un tableau general de la classification des polypes. Paris: Gide et J. Baudry, 502 pp.Google Scholar
Risso, A. (1826) Histoire naturelle des principales de l'Europe Méridionale. Volume 5. Paris: F. Chez, G. Levrault, Libraire, Rue de la Harpe, pp. 284290.Google Scholar
Rodríguez, E., Barbeitos, M.S., Brugler, M.R., Crowley, L.M., Grajales, A., Gusmão, L., Häussermann, V., Reft, A. and Daly, M. (2014) Hidden among sea anemones: The first comprehensive phylogenetic reconstruction of the the order Actiniaria (Cnidaria, Anthozoa, Hexacorallia) reveals a novel group of hexacorals. Plos One 9, e96998. doi: i10.1371/journal.pone.0096998.Google Scholar
Rodríguez, E., Barbeitos, M., Daly, M., Gusmão, L.C. and Häussermann, V. (2012) Toward a natural classification: phylogeny of acontiate sea anemones (Cnidaria, Anthozoa, Actiniaria). Cladistics 1, 118.Google Scholar
Rodríguez, E., Daly, M. and Fautin, D.G. (2007) Order actiniaria. In Zhang, Z.-Q. and Shear, W.A. (eds) Linnaeus Tercentenary: Progress in Invertebrate Taxonomy. Zootaxa 1668, 131–136.Google Scholar
Rüppell, E. and Leuckart, F.S. (1828) Atlas zu der Reise im Nördlicehn Afrika von Eduard Rüppell, Neue Wirbellose Thiere des Rothen Meers. Frankfurt am Main: Heinrich Ludwig Brvnner, 47 pp.Google Scholar
Scott, A. and Harrison, P.L. (2009) Gametogenic and reproductive cycles of the sea anemone, Entacmaea quadricolour . Marine Biology 156, 16591671.CrossRefGoogle Scholar
Shearer, T.L., Van Oppen, J.H., Romano, S.L. and Wörheide, G. (2002) Slow mitochondrial DNA sequence evolution in the Anthozoa (Cnidaria). Molecular Ecology 11, 24752487.Google Scholar
Stephenson, T.A. (1922) On the classification of Actiniaria. Part III. Definitions connected with the forms dealt with in Part II. Quarterly Journal of Microscopical Science 66, 247319.Google Scholar
Stoletzki, N. and Schierwater, B. (2005) Genetic and colour morph differentiation in the Caribbean sea anemone Condylactis gigantea . Marine Biology 147, 747754.Google Scholar
Tamura, K., Stecher, G., Peterson, D., Filipski, A. and Kumar, S. (2013) MEGA6: Molecular Evolutionary Genetics Analysis Version 6.0. Molecular Biology and Evolution 30, 27252729.Google Scholar
Verrill, A.E. (1900) Additions to the Anthozoa and Hydrozoa of the Bermudas. Anthozoa. Transactions of the Connecticut Academy of Arts and Sciences 10, 551572.Google Scholar
Verrill, A.E. (1905) The Bermuda Islands. Part IV. Geology and paleontology, and Part V. An account of the coral reefs. Transactions of the Connecticut Academy of Arts and Sciences 12, 45348.Google Scholar
Watts, P.C., Allcock, A.L., Lynch, S.M. and Thorpe, J.P. (2000) An analysis of the nematocysts of the beadlet anemone Actinia equina and the green sea anemone Actinia prasina . Journal of the Marine Biological Association of the United Kingdom 80, 719724.Google Scholar
Watts, P.C. and Thorpe, J.P. (1998) Phenotypic identification of three genetically differentiated morphs of the intertidal beadlet anemone Actinia equina (Anthozoa: Cnidaria). Journal of the Marine Biological Association of the United Kingdom 78, 13651368.Google Scholar
Williams, R.B. (1991) Acrorhagi, catch tentacles and sweeper tentacles: a synopsis of “aggression” of actiniarian and scleractinian Cnidaria. Hydrobiologia 216/217, 539545.Google Scholar
Williams, R.B. (1996) Measurements of cnidae from sea anemones (Cnidaria: Actiniaria): statistical parameters and taxonomic relevance. Scientia Marina 60, 339351.Google Scholar
Williams, R.B. (1998) Measurements of cnidae from sea anemones (Cnidaria: Actiniaria), II: further studies of differences amongst sample means and their taxonomic relevance. Scientia Marina 62, 361372.Google Scholar
Williams, R.B. (2000) Measurements of cnidae from sea anemones (Cnidaria: Actiniaria), III: ranges and other measures of statistical dispersion, their interrelations and taxonomic relevance. Scientia Marina 64, 4968.Google Scholar
Wilson, H.V. (1890) On a new actinia, Hoplophoria coralligens . Studies at the Biological Laboratory of the John Hopkins University (Baltimore) 6, 379387.Google Scholar