Description of Calliactis tigris sp. nov.: reconciling taxonomy and phylogeny in hermit-crab symbiotic anemones (Cnidaria: Actiniaria: Hormathiidae)

Abstract

The symbiosis between sea anemones and hermit crabs is ubiquitous in the marine environment (except in the poles), occurring from shallow to deep waters; it involves one or more anemones living on a shell inhabited by a hermit crab. The anemone-crab partnership is a mutualism in which hermit crabs provide a hard substrate, increased access to oxygenated waters and food supply, in exchange for defense by the anemone. The vast majority of the sea anemone partners belong to three genera in family Hormathiidae: Adamsia, Calliactis, Paracalliactis. Given the remarkable nature of the symbiosis, hormathiid partners have been hypothesized to represent a monophyletic group. This has been rejected by Gusmão and Daly et al. (2010) and confirmed by our phylogenetic analysis using molecular markers (12S, 16S, 18S, 28S, COIII). We expand the results of Gusmão and Daly et al. (2010) by finding a monophyletic Paracalliactis, which was left untested in their analyses. Thus, characters of taxonomic significance associated to the symbiotic habit are interpreted as functional rather than phylogenetic. We reconcile taxonomy and the present evolutionary framework to avoid defining taxonomic groups based on characters prone to convergence. We formalize the synonymy of Adamsia and Calliactis and provide updated diagnoses for the valid genera Calliactis and Paracalliactis to bring more stability to the group. Under this new framework, we describe Calliactis tigris sp. nov. from Australia based on 21 specimens collected off the coast of New South Wales and Queensland and differentiate it from congeners and other hermit crab symbionts recorded in the Pacific Ocean.

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References

  1. Ates, R. M. L. (1997). Observations on the symbiosis between Colus gracilis (Da Costa, 1778) (Mollusca: Gastropoda) and Hormathia digitata (O. F. Muller, 1776) (Cnidaria: Actiniaria). Zoologische Verhandelingen, 323, 257–262.

    Google Scholar 

  2. Bach, C. E., & Herrnkind, W. F. (1980). Effects of predation pressure on the mutualistic interaction between the hermit crab, Pagurus pollicaris Say, 1817, and the sea anemone, Calliactis tricolor (LeSueur, 1817). Crustaceana, 38, 104–108.

    Google Scholar 

  3. Balasch, J., & Mengual, V. (1973). The behavior of Dardanus arrosor in association with Calliactis parasitica in artificial habitat. Marine and Freshwater Behaviour and Physiology, 2, 251–260.

    Google Scholar 

  4. Balss, H. (1912). Paguriden. In C. Chun (Ed.), Wiss. Ergebnisse der Deutschen Tiefsee-Exp. "Valdivia" 1898–1899 (pp. 85–124). Gustav Fischer: Jena.

    Google Scholar 

  5. Brooks, W. R. (1989). Hermit crabs alter sea anemone placement patterns for shell balance and reduced predation. Journal of Experimental Marine Biology and Ecology, 132, 109–121.

    Google Scholar 

  6. Brooks, W. R., & Gwaltney, C. L. (1993). Protection of symbiotic cnidarians by their hermit crab hosts: Evidence for mutualism. Symbiosis, 15, 1–13.

    Google Scholar 

  7. Cariello, L., de Santis, A., Piccoli, R., Spagnuolo, A., Zanetti, L., & Parente, A. (1989). Calitoxin, a neurotoxic peptide from the sea anemone Calliactis parasitica: Amino acid sequence and electrophysiological properties. Biochemestry, 28, 2484–2489.

    CAS  Google Scholar 

  8. Carlgren, O. (1893). Studien über nordische Actinien. Kungliga Svenska Vetenskapsakademiens Handlingar, 25, 1–148.

    Google Scholar 

  9. Carlgren, O. (1922). Actiniaria and Zoantharia von Juan Fernandez und der osterinsel. In C. Skottsberg (Ed.), The Natural History of Juan Fernandez and Easter Island (pp. 145–160). Uppsala: Almquist & Wiksells Botryckeri-A. -B.

    Google Scholar 

  10. Carlgren, O. (1925). Zur kenntnis der Hexacorallen. Zoologischer Anzeiger, 65, 87–99.

    Google Scholar 

  11. Carlgren, O. (1927). Actiniaria and Zoantharia. In T. Odhner (Ed.), Further zoological results of the Swedish Antarctic expedition 1901–1903 (pp. 1–102). Stockholm: P.A. Norstedt & Söner.

    Google Scholar 

  12. Carlgren, O. (1928a). Zur symbiose swischen Actinien und Paguriden. Zeitschrift für Morphologie und Ökologie der Tiere, 12, 165–173.

    Google Scholar 

  13. Carlgren, O. (1928b). Ceriantharier, Zoantharier och Actiniarier. Meddelelser om Grønland, 23(Suppl), 253–308.

    Google Scholar 

  14. Carlgren, O. (1928c). Actiniaria der Deutschen Tiefsee-Expedition. Wissenschaftliche Ergebnisse der Deutschen Tiefsee-Expedition auf dem Dampfer “Valdivia” 1898–1899, 22, 125–266.

    Google Scholar 

  15. Carlgren, O. (1932). Die Ceriantharien, Zoantharien und Actiniarien des arktischen Gebietes. In F. Romer, F. Schaudinn, A. Brauer, & W. Arndt (Eds.), Eine Zusammenstellung der arktischen Tierformen mit besonderer Berücksichtigung des Spitzbergen-Gebietes auf Grund der Ergebnisse der Deutschen Expedition in das Nördliche Eismeer im Jahre (pp. 255–266). Jena: Gustav Fischer.

    Google Scholar 

  16. Carlgren, O. (1938). South African Actiniaria and Zoantharia. Kungliga Svenska Vetenskapsakademiens Handlingar, 17, 1–148.

    Google Scholar 

  17. Carlgren, O. (1940). A contribution to the knowledge of the structure and distribution of the cnidae in the Anthozoa. Kungliga Svenska Vetenskapsakademiens Handlingar, 51, 1–62.

    Google Scholar 

  18. Carlgren, O. (1943). East-Asiatic Corallimorpharia and Actiniaria. Kungliga Svenska Vetenskapsakademiens Handlingar, 20, 1–43.

    Google Scholar 

  19. Carlgren, O. (1949). A survey of the Ptychodactiaria, Corallimorpharia and Actiniaria. Kungliga Svenska Vetenskapsakademiens Handlingar, 1, 1–121.

    Google Scholar 

  20. Christidis, J., Chintiroglou, C. H., & Culley, M. B. (1997). A study of the populations of Calliactis parasitica (Couch, 1842) in symbiosis with anomuran decapods in Thermaikos Gulf (N. Aegean Sea). Crustaceana, 70, 227–238.

    Google Scholar 

  21. Couch, R. Q. (1842). An essay on the zoophytes of Cornwall. Annual Report of the Royal Cornwall Polytechnic Society, 9, 27–91.

    Google Scholar 

  22. Crowther, A. L., Fautin, D. G., & Wallace, C. C. (2011). Stylobates birtlesi sp. n., a new species of carcinoecium-forming sea anemone (Cnidaria, Actiniaria, Actiniidae) from eastern Australia. Zookeys, 89, 33–28.

    Google Scholar 

  23. Dall, W. H. (1903). A new genus of Trochidae. Nautilus, 17, 61–62.

    Google Scholar 

  24. Daly, M., Lipscomb, D. L., & Allard, M. W. (2002). A simple test: Evaluating explanations for the relative simplicity of the Edwardsiidae (Cnidaria: Anthozoa). Evolution, 56, 502–510.

    PubMed  Google Scholar 

  25. Daly, M., Ardelean, A., Cha, H., Campbell, A. C., & Fautin, D. G. (2004). A new species, Adamsia obvolva (Cnidaria: Anthozoa: Actiniaria), from the Gulf of Mexico, and a discussion of the taxonomy of carcinoecium-forming sea anemones. Bulletin of Marine Science, 74, 385–399.

    Google Scholar 

  26. Daly, M., Chaudhuri, A., Gusmão, L., & Rodríguez, E. (2008). Phylogenetic relationships among sea anemones (Cnidaria: Anthozoa: Actiniaria). Molecular Phylogenetics and Evolution, 48, 292–301.

    CAS  PubMed  Google Scholar 

  27. Daly, M., Gusmão, L. C., Reft, A. J., & Rodríguez, E. (2010). Phylogenetic signal in mitochondrial and nuclear markers in sea anemones (Cnidaria, Actiniaria). Integrative and Comparative Biology, 50(3), 371–388.

    CAS  PubMed  Google Scholar 

  28. Daly, M., Crowley, L. M., Larson, P., Rodríguez, E., Saucier, E. H., & Fautin, D. G. (2017). Anthopleura and phylogeny of Actinioidea (Cnidaria: Anthozoa: Actiniaria). Organisms, Diversity and Evolution, 17, 545–564.

    Google Scholar 

  29. Dalyell, J. G. (1848). Rare and remarkable animals of Scotland. London: John Van Voorst, Paternoster Row.

    Google Scholar 

  30. 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: Lea and Blanchard.

    Google Scholar 

  31. Dana, J. D. (1851). Conspectus crustaceorum quae in orbis terrarum circumnavigatione, Carolo Wilkes e classe reipublicae foederatae duce, lexit et descripsit. Proceedings of the Academy of Natural Sciences of Philadelphia, 5, 267–272.

    Google Scholar 

  32. Danielssen, D. C. (1890). Actinida. Christiania: Den Norske Nordhavs-Expedition.

    Google Scholar 

  33. Dechancé, M., & Dufaure, J. (1959). Une nouvelle association entre une actinie et un pagure. Comptes Rendus Hebdomadaires des Séances de l'Académie des Sciences, 249, 1566–1568.

    Google Scholar 

  34. Doumenc, D. (1975). Actinies bathyales et abyssales de l'océan Atlantique nord familles des Hormathiidae (genres Paracalliactis et Phelliactis) et des Actinostolidae (genres Actinoscyphia et Sicyonis). Bulletin du Muséum National d'Histoire Naturelle (Paris), 197(287), 157–204.

    Google Scholar 

  35. Dunn, D. F., Devaney, D. M., & Roth, B. (1980). Stylobates: A shell-forming sea anemone (Coelenterata, Anthozoa, Actiniidae). Pacific Science, 34, 379–388.

    Google Scholar 

  36. England, K. W. (1971). Actiniaria from Mururoa Atoll Tuamotu, Polynesia (Hormathiidae; Calliactis polypus Sagartiidae: Verrillactis n. gen. paguri). Cahiers du Pacifique, 15, 23–40.

    Google Scholar 

  37. Fabricius, J. C. (1775). Systema entomologiae, sistens insectorum classes, ordines, genera, species, adiectis, synonymis, locis, descriptionibus, observationibus. Officina Libraria Kortii: Flensburgi et Lipsiae.

    Google Scholar 

  38. Fautin, D. G. (1987). Stylobates loisetteae, a new species of shell-forming sea anemone (Coelenterata: Actiniidae) from western Australia. Proceedings of the California Academy of Sciences, 45(1), 1–7.

    Google Scholar 

  39. Fautin, D. G. (1988). The importance of nematocysts to actiniarian taxonomy. In D. A. Hessinger & H. M. Lenhoff (Eds.), The biology of nematocysts (pp. 487–500). New York: Academic Press.

    Google Scholar 

  40. Fautin, D. G. (1992). A shell with a new twist. Natural History, 4, 50–57.

    Google Scholar 

  41. Fautin, D. G. (2016). Catalog to families, genera, and series of orders Actiniaria and Corallimorpharia (Cnidaria: Anthozoa). Zootaxa, 4145(1), 1–449.

    PubMed  Google Scholar 

  42. Fedorov, A., Beichel, R., Kalpathy-Cramer, J., Finet, J., Fillion-Robin, J.-C., Pujol, S., Bauer, C., Jennings, D., Fennessy, F., Sonka, M., Buatti, J., Aylward, S., Miller, J. V., Pieper, S., & Kikinis, R. (2012). 3D slicer as an image computing platform for the quantitative imaging network. Magnetic Resonance Imaging, 30(9), 1323–1341.

    PubMed  PubMed Central  Google Scholar 

  43. Fischer, P. (1889). Nouvelle Contribution à l'Actinologie Française. Première Partie. Actes de la Société Linnéenne de Bordeaux, 43, 252–309.

    Google Scholar 

  44. Forbes, E. (1840). On the British Actiniadae. Annals and Magazine of Natural History, 5, 180–184.

    Google Scholar 

  45. Forsskål, P. (1775). Descriptiones Animalium Avium, Amphibiorum, Piscium, Insectorum, Vermium; Quae in Itinere Orientali Observait. Copenhagen: Molleri.

    Google Scholar 

  46. Geller, J. B., & Walton, E. D. (2001). Breaking up and getting back together: Evolution of symbiosis and cloning in sea anemones (genus Anthopleura) inferred from a molecular phylogeny. Evolution, 55, 1781–1794.

    CAS  PubMed  Google Scholar 

  47. Goloboff, P. A., Farris, J. S., & Nixon, K. C. (2008). TNT, a free program for phylogenetic analysis. Cladistics, 24, 774–786.

    Google Scholar 

  48. Gosse, P. H. (1855). Description of Peachia hastata, a new genus and species of the class Zoophyta; with observations on the family Actiniadae. Transactions of the Linnean Society (London), 21, 267–276.

    Google Scholar 

  49. Gosse, P. H. (1858). Synopsis of the families, genera, and species of the British Actiniae. Journal of Natural History, 1, 414–419.

    Google Scholar 

  50. Grajales, A., & Rodríguez, E. (2016). Elucidating the evolutionary relationships of the Aiptasiidae, a widespread Cnidarian-dinoflagellate model system (Cnidaria: Anthozoa: Actiniaria: Metridioidea). Molecular Phylogenetics and Evolution, 94, 252–263.

    PubMed  Google Scholar 

  51. Gravier, C. (1918). Note préliminaire sur les hexactiniaires recueillis au cours des croisières de la Princesse-Alice et de l'Hirondelle de 1888 à 1913 inclusivement. Bulletin de l'Institut Océanographique (Monaco), 346, 1–24.

    Google Scholar 

  52. Gusmão, L. C. (2010). Systematics and evolution of sea anemones (Cnidaria: Actiniaria: Hormathiidae) symbiotic with hermit crabs. Dissertation. The Ohio State University. https://etd.ohiolink.edu/pg_10?0::NO:10:P10_ACCESSION_NUM:osu1291150200. Accessed 20 February 2019.

  53. Gusmão, L. C., & Daly, M. (2010). Evolution of sea anemones (Cnidaria: Actiniaria: Hormathiidae) symbiotic with hermit crabs. Molecular Phylogeny and Evolution, 56, 868–877.

    Google Scholar 

  54. Gusmão, L. C., Grajales, A., & Rodríguez, E. (2018). Sea anemones through X-rays: Visualization of two species of Diadumene (Cnidaria, Actiniaria) using micro-CT. American Museum Novitates, 3907, 1–45.

    Google Scholar 

  55. Hand, C. (1975). Descriptions of two New Zealand sea anemones (Actiniaria: Hormathiidae). New Zealand Journal of Marine and Freshwater Research, 9, 493–507.

    Google Scholar 

  56. Hertwig, R. (1882). Die Actinien der Challenger Expedition. Jena: Gustav Fischer.

    Google Scholar 

  57. International Commission on Zoological Nomenclature. (1999). International code of zoological nomenclature (Fourth ed.). London: International Trust for Zoological Nomenclature. https://doi.org/10.5962/bhl.title.50608.

  58. Katoh, K., & Standley, D. M. (2013). MAFFT multiple sequence alignment software version 7: Improvements in performance and usability. Molecular Biology and Evolution, 30(4), 772–780.

    CAS  PubMed  PubMed Central  Google Scholar 

  59. Katoh, K., Rozewicki, J., & Yamada, K. D. (2017). MAFFT online service: Multiple sequence alignment, interactive sequence choice and visualization. Brief in Bioinformatics bbx108, https://doi.org/10.1093/bib/bbx108.

    PubMed Central  Google Scholar 

  60. Kearse, M., Moir, R., Wilson, A., Stones-Havas, S., Cheung, M., Sturrock, S., Buxton, S., Cooper, A., Markowitz, S., Duran, C., Thierer, T., Ashton, B., Meintjes, P., & Drummond, A. (2012). Geneious Basic: An integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics, 28(12), 1647–1649.

    PubMed  PubMed Central  Google Scholar 

  61. Kozlov, A. M., Darriba, D., Flouri, T., Morel, B., & Stamatakis, A. (2018). RAxML-NG: A fast scalable, and user-friendly tool for maximum likelihood phylogenetic inference. bioRxiv. https://doi.org/10.1101/447110.

  62. Larson, P., & Daly, M. (2016). Phylogenetic analysis reveals an evolutionary transition from internal to external brooding in Epiactis Verrill (Cnidaria: Anthozoa: Actiniaria) and rejects the validity of the genus Cnidopus Carlgren. Molecular Phylogenetics and Evolution, 94, 548–558.

    PubMed  Google Scholar 

  63. Lauretta, D., Häussermann, V., Brugler, M. R., & Rodríguez, E. (2014). Isoparactis fionae sp. n. (Cnidaria: Anthozoa: Actiniaria) from Southern Patagonia with a discussion of the family Isanthidae. Organisms, Diversity and Evolution, 14(1), 31–42.

    Google Scholar 

  64. Le Sueur, C. A. (1817). Observations on several species of the genus Actinia; illustrated by figures. Journal of the Academy of Sciences of Philadelphia, 1, 159–189.

    Google Scholar 

  65. Leach, W. E. (1815). Malacostraca Podophthalmata Britanniæ; or descriptions of such British species of the Linnean genus Cancer as have their eyes elevated on footstalks. London: B. Meredith.

    Google Scholar 

  66. Lemaitre, R. (1996). Hermit crabs of the family Parapaguridae (Crustacea: Decapoda: Anomura) from Australia: Species of Strobopagurus Lemaitre, 1989, Sympagurus Smith, 1883 and two new genera. Records of the Australian Museum, 48(2), 163–221.

    Google Scholar 

  67. Mainardi, D., & Rossi, A. C. (1969). Relations between social status and activity toward the sea anemone Calliactis parasitica in the hermit crab Dardanus arrosor. Accademia Nazionale dei Lincei, Rnma, Classe di Scienze Fisiche, Matematiche e Naturali, 47, 116–121.

    Google Scholar 

  68. Miller, M. A., Pfeiffer, W., & Schwartz, T. (2010). Creating the CIPRES Science Gateway for inference of large phylogenetic trees. Proceedings of the Gateway Computing Environments Workshop (GCE), 1–8.

  69. Müller, O. F. (1776). Zoologiae Danicae Prodromus, seu animalium Daniae et Norvegiae indigenarum characteres, nomina, et synonyma imprimis popularium. Havniae.

  70. Parry, G. (1952). The Actiniaria of New Zealand. A check-list of recorded and new species a review of the literature and a key to the commoner forms part 2. Records of the Canterbury Museum, 6, 121–141.

    Google Scholar 

  71. Parulekar, A. (1969). Neoaiptasia commensali, gen. et. sp. nov.: An actiniarian commensal of hermit crabs. Journal of the Bombay Natural History Society, 66(1), 57–62.

    Google Scholar 

  72. Paulson, O. (1875). Izsledovaniya rakoobrazykh krasnago morya s zametkami otnositel'no rakoobraznykh drugikh morei: I–XIV, 1–144, pis. 1–21. (1961, English translation: 1–164, pis. 1–21).

  73. Pei, Z. (1982). A new species of the genus Paracalliactis (Hormathiidae: Actiniaria) from the East China Sea. Studia Marina Sinica, 19, 69–71.

    Google Scholar 

  74. Pei, Z. (1996). Three new species of the genus Calliactis. Studia Marina Sinica, 37, 177–187.

    Google Scholar 

  75. Pennant, T. (1777). A British zoology (4th ed.). London: Benj White.

    Google Scholar 

  76. Presnell, J. K., & Schreibman, M. P. (1997). Humason’s animal tissue techniques. Baltimore: Johns Hopkins University Press.

    Google Scholar 

  77. Riemann-Zürneck, K. (1973). Actiniaria des Südwestatlantik I. Hormathiidae. Helgoländer Wissenschaftliche Meeresuntersuchungen, 25, 273–325.

    Google Scholar 

  78. Riemann-Zürneck, K. (1975). Actiniaria des Südwestatlantik III. Calliactis androgyna sp. n. (Hormathiidae). Veröffentlichungen des Institutes für Meeresforschung Bremerhaven, 15, 387–395.

    Google Scholar 

  79. Riemann-Zürneck, K. (1986). On some abyssal sea anemones of the North Atlantic (Actiniaria: Hormathiidae). Mitteilungen aus dem Hamburgischen Zoologischen Museum und Institut, 83, 7–29.

    Google Scholar 

  80. Rodríguez, E., & Gusmão, L. C. Case 3805: Calliactis Verrill, 1869 (Cnidaria, Anthozoa, Hexacorallia, Actiniaria): proposed precedence over Adamsia Forbes, 1840. Bull. Zool. Nomencl. (submitted).

  81. Rodríguez, E., & López-González, P. J. (2003). Stephanthus antarcticus a new genus and species of sea anemone (Actiniaria, Haloclavidae) from the South Shetland Islands, Antarctica. Helgoland Marine Research, 57, 54–62.

    Google Scholar 

  82. Rodríguez, E., Barbeitos, M., Daly, M., Gusmão, L. C., & Häussermann, V. (2012). Toward a natural classification: Phylogeny of acontiate sea anemones (Cnidaria, Anthozoa, Actiniaria). Cladistics, 28, 375–392.

    Google Scholar 

  83. Rodríguez, E., Barbeitos, M. S., Brugler, M. R., Crowley, L., Grajales, A., Gusmão, L. C., Häussermann, V., Reft, A., & Daly, M. (2014). Hidden among sea anemones: The first comprehensive phylogenetic reconstruction of the order Actiniaria (Cnidaria, Anthozoa, Hexacorallia) reveals a novel group of Hexacorals. PLoS One, 9(5), e96998.

    PubMed  PubMed Central  Google Scholar 

  84. Ross, D. M. (1971). Protection of hermit crabs (Dardanus spp.) from octopus by commensal sea anemones (Calliactis spp.). Nature, 230, 401–402.

    CAS  PubMed  Google Scholar 

  85. Ross, D. M. (1974a). Behavior patterns in associations and interactions with other animals. In L. Muscatine & H. M. Lenhoff (Eds.), Coelenterate biology: Reviews and new perspectives (pp. 281–312). New York: Academic Press.

    Google Scholar 

  86. Ross, D. M. (1974b). Evolutionary aspects of associations between crabs and sea anemones. In W. B. Vernberg (Ed.), Symbiosis in the sea (pp. 111–125). South Carolina: University of South Carolina Press.

    Google Scholar 

  87. Ross, D. M. (1975). The behavior of pagurids in symbiotic associations with actinians in Japan. Publications of the Seto Marine Biological Laboratory, 22(1–4), 157–170.

    Google Scholar 

  88. Ross, D. M., & Boletzky, S. (1979). The association between the pagurid Dardanus arrosor and the actinian Calliactis parasitica. Recovery of activity in “inactive” D. arrosor in the presence of cephalopods. Marine Behaviour and Physiology, 6, 175–184.

    Google Scholar 

  89. Ross, D. M., & Sutton, L. (1961). The response of the sea anemone Calliactis parasitica to shells of the hermit crab Pagurus bernhardus. Proceedings of the Royal Society B, 155, 266–281.

    Google Scholar 

  90. Ross, D. M., & Zamponi, M. O. (1982). A symbiosis between Paracalliactis mediterranea n. sp. (Anthozoa-Actiniaria) and Pagurus variables A. Milne-Edwards and Bouvier. Vie Millie, 32, 175–181.

    Google Scholar 

  91. Schmidt, H. (1969). Die nesselkapseln der Aktinien und ihre differentialdiagnostische Bedeutung. Helgoländer Wissenschaftliche Meeresuntersuchungen, 19, 284–317.

    Google Scholar 

  92. Schmidt, H. (1972). Die Nesselkapseln der Anthozoen und ihre Bedeutung fur die phylogenetische Systematik. Helgoländer Wissenschaftliche Meeresuntersuchungen, 23, 422–458.

    Google Scholar 

  93. Schmidt, H. (1974). On evolution in the Anthozoa. Proceedings 2nd International Coral Reef Symposium, 1, 533–560.

    Google Scholar 

  94. Simon, J. A. (1892). Ein Beitrag zur Anatomie und Systematik der Hexactinien. München: Val. Hvfling.

    Google Scholar 

  95. Smith, S. I. (1879). The stalked-eyed crustaceans of the Atlantic coast of North America north of Cape Cod. Transactions. Connecticut Academy of Arts and Sciences, 5, 27–136.

    Google Scholar 

  96. Smith, S. I. (1883). Preliminary report on the Brachyura and Anomura dredged in deep water off the south coast of New England by the United States Fish Commission in 1880, 1881, and 1882. Proceedings of the United States National Museum, 6, 1–57.

    Google Scholar 

  97. Spagnuolo, A., Zanetti, L., Cariello, L., & Piccoli, R. (1994). Isolation and characterization of two genes encoding calitoxins, neurotoxic peptides from Calliactis parasitica (Cnidaria). Gene, 138, 187–191.

    CAS  PubMed  Google Scholar 

  98. Stephenson, T. A. (1918). Coelenterata. Part I. Actiniaria. Natural History Reports on British Antarctic (“Terra Nova”) Expedition 1910, 5, 1–68.

    Google Scholar 

  99. Stephenson, T. A. (1929). A contribution to actinian morphology: The genera Phellia and Sagartia. Transactions of the Royal Society of Edinburgh, 56(6), 121–139.

    Google Scholar 

  100. Stewart, Z. K., Pavasonic, A., Hock, D. H., & Prentis, P. J. (2017). Transcriptomic investigation of wound healing and regeneration in the cnidarian Calliactis polypus. Scientific Reports, 7. https://doi.org/10.1038/srep41458.

  101. Studer, T. (1879). Zweite Abtheilung der Anthozoa polyactinia, welche während der Reise S. M. S. Corvette Gazelle um die Erde gesammelt wurden. Monatsberichte der könglich preussischen Akademie der Wissenschaften zu Berlin, 524–550.

  102. Torrey, H. B. (1902). Papers from the Harriman Alaska Expedition. XXX. Anemones, with discussion of variation in Metridium. Proceedings of the Washington Academy of Sciences, 4, 373–410.

    Google Scholar 

  103. Uchida, T. (1960). Carcinactis ichikawai, n. gen.; n. sp., an actiniaria commensal with the crab Dorippe granulata. Japanese Journal of Zoology, 12(4), 595–601.

    Google Scholar 

  104. Verrill, A. E. (1869). Review of the corals and polyps of the west coast of America. Transactions. Connecticut Academy of Arts and Sciences, 1(6), 377–567.

    Google Scholar 

  105. Verrill, A. E. (1882). Notice of the remarkable marine fauna occupying the outer banks off the southern coast of New England, No. 4. American Journal of Science, 23, 216–225.

    Google Scholar 

  106. Verrill, A. E. (1883). Reports on the Anthozoa, and on some additional species dredged by the ‘Blake’ in 1877–1879, and by the U.S. Fish Commission Steamer “Fish Hawk” in 1880–82. Bulletin of the Museum of Comparative Zoology, Harvard University, 11, 1–72.

    Google Scholar 

  107. Weill, R. (1934). Contribution à l’étude des Cnidaires et de leurs nématocystes. Paris: Les Presses Universitaires de France.

    Google Scholar 

  108. Wiedenmann, J., Ivanchenko, S., Oswald, F., & Nienhaus, G. U. (2004). Identification of GFP-like protein in nonbioluminescent, azooxanthellate Anthozoa opens new perspectives for bioprospecting. Marine Biotechnology, 6(3), 270–277.

    CAS  PubMed  Google Scholar 

  109. Williams, J. D., & McDermott, J. J. (2004). Hermit crab biocoenoses: A worldwide review of the diversity and natural history of hermit crab associates. Journal of Experimental Marine Biology and Ecology, 305, 1–128.

    Google Scholar 

  110. Williamson, M., Hauser, F., & Grimmelikhuijzen, C. J. P. (2000). Genomic organization and splicing variant of a peptidylglycine α-hydroxylating monooxygenase from sea anemones. Biochemical and Biophysical Research Communications, 277(1), 7–12.

    CAS  PubMed  Google Scholar 

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Acknowledgments

We thank Stephen Keable and Helen Stoddart (Australian Museum) for loan of specimens from Australia. We are also grateful to Stephen Cairns (United States Natural History Museum) for facilitating a first loan of the Australian material to the United States. Lily Berniker (American Museum of Natural History, AMNH) is thanked for assistance with museum loans. Morgan Hill and Andrew Smith (Microscopy and Imaging Facility, AMNH) helped us with micro-CT scanning and image processing.

Funding

This work was supported by the Lerner-Gray Fund for Marine Research Grant (AMNH) and the Fellowship for Graduate Student Travel (Society of Integrative and Comparative Biology) to LCG and a Doctoral Dissertation Improvement Grant (National Science Foundation, DEB 0808339) to MD and LCG. Janine Luke supported ER’s research program and LCG.

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Correspondence to Luciana C. Gusmão.

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Gusmão, L.C., Rodríguez, E. & Daly, M. Description of Calliactis tigris sp. nov.: reconciling taxonomy and phylogeny in hermit-crab symbiotic anemones (Cnidaria: Actiniaria: Hormathiidae). Org Divers Evol 19, 567–583 (2019). https://doi.org/10.1007/s13127-019-00414-2

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Keywords

  • Symbiosis
  • Mutualism
  • Convergence
  • Adamsia
  • Paracalliactis
  • Australia