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Type: Article
Published: 2024-09-05
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The clownfish-hosting sea anemones (Anthozoa: Actiniaria): updated nomenclature, biogeography, and practical field guide.

Department of Biological Sciences; University of Alabama; Tuscaloosa; AL; USA 35487; Dauphin Island Sea Lab; 101 Bienville Blvd; Dauphin Island; AL; USA 36528
Department of Biology; Boston University; 5 Cummington Mall; Boston; MA; USA; 02215
Department of Biological Sciences; University of Alabama; Tuscaloosa; AL; USA 35487; Dauphin Island Sea Lab; 101 Bienville Blvd; Dauphin Island; AL; USA 36528
Division of Invertebrate Zoology; American Museum of Natural History; New York; NY; USA
Coelenterata Cnidaria Hexacorallia Actinioidea symbiosis species identification

Abstract

Ten described species of sea anemones (Anthozoa: Hexacorallia: Actiniaria) serve as hosts to charismatic clownfishes (or anemonefishes) on coral reefs throughout the tropical Indo-West Pacific. Although not diverse in number, the clownfish-hosting sea anemones have large biogeographic ranges, exhibit extensive intraspecific phenotypic appearances, and have been surrounded by a great deal of historical and contemporary taxonomic and nomenclatural confusion. We believe these factors have created challenges for field scientists making real-time species-level identifications of host sea anemones. Subsequently, a surprising amount of peer-reviewed clownfish literature never accounts for the host sea anemone, omitting critical data for understanding the symbiosis ecologically and evolutionarily. Here, we leverage the revolution that has taken place in the realm of digital underwater photography over the past 30 years to provide an updated, practical field guide for the clownfish-hosting sea anemones. First however, we review and revise the nomenclature for each species to better reflect valid changes that were made in the historical literature but never broadly adopted. Next, we demonstrate that machine learning algorithms may be of limited use for automating sea anemone species IDs from digital photographs alone—highlighting the importance of organismal expertise for identifying these animals. Finally, we present high-resolution digital photographs that encompass much of the intraspecific phenotypic variation encountered underwater, discuss important characteristics useful for field IDs, and provide updated range maps for each species to better reflect the known biogeographic range of each host anemone. We hope the increased confidence in field identification provided by this guide will result in more papers incorporating the sea anemone host data into research frameworks and subsequent publications.

 

References

  1. Abadi, M., Agarwal, A., Barham, P., Brevdo, E., Chen, Z., Citro, C., Corrado, G.S., Davis, A., Dean, J., Devin, M. & Ghemawat, S. (2016) Tensorflow: Large-scale machine learning on heterogeneous distributed systems. arXiv preprint arXiv, 1603.04467. Available from: https://arxiv.org/abs/1603.04467 (accessed 17 June 2024)
  2. Assis, J., Tyberghein, L., Bosch, S., Heroen, V., Serrão, E., De Clerck, O. & Tittensor, D. (2018) Bio‐ORACLE v2.0: Extending marine data layers for bioclimatic modelling. Global Ecology and Biogeography, 27 (3), 277–284. https://doi.org/10.1111/geb.12693
  3. Barragán, Y., Sánchez, C., Hooker, Y. & Rodríguez, E. (2019) First inventory of sea anemones (Cnidaria: Actiniaria) from La Paz Bay, Southern Gulf of California (Mexico). Zootaxa, 4559 (3), 501–549. https://doi.org/10.11646/zootaxa.4559.3.4
  4. Bennett-Smith, M.F., Majoris, J.E., Titus, B.M. & Berumen, M.L. (2021) Clownfish hosting anemones (Anthozoa, Actiniaria) of the Red Sea: new associations and distributions, historical misidentifications, and morphological variability. Marine Biodiversity Records, 14 (1), 1–15. https://doi.org/10.1186/s41200-021-00216-6
  5. Bennett-Smith, M.F., Justo, M.S., Berumen, M.L., Peixoto, R. & Titus, B.M. (2022) Novel in situ observations of asexual reproduction in the carpet sea anemone, Stichodactyal mertensii (Stichodactylidae, Actiniaria). ZooKeys, 1103, 57–63. https://doi.org/10.3897/zookeys.1103.84415
  6. Buston, P.M. (2004) Territory inheritance in clownfish. Proceedings of the Royal Society of London, Series B: Biological Sciences, 271 (Supplement 4), S252–S254. https://doi.org/10.1098/rsbl.2003.0156
  7. Branconi, R., Barbasch, T.A., Francis, R.K., Srinivasan, M., Jones, G.P. & Buston, P.M. (2020) Ecological and social constraints combine to promote evolution of non-breeding strategies in clownfish. Communications Biology, 3 (1), 649. https://doi.org/10.1038/s42003-020-01380-8
  8. Brandt, J.F. (1835) Polypos, acalephas discophoras et siphonophoras, nec non echinodermata continens. Prodromus Descriptionis Animalium AB H. Mertensio in Orbis Terrarum Circumnavigatione Observatorum. Sumptibus Academiae, Petropoli, 75 pp.
  9. GBIF (2023) Derived dataset GBIF.org. 30 March 2023. Filtered export of GBIF occurrence data. https://doi.org/10.15468/dd.u2yyzx
  10. Duchassaing de Fombressin, P. & Michelotti, G. (1864) Supplément au mémoire sur les Coralliaires des Antilles. Imprimerie Royale, Turin, 112 pp. https://doi.org/10.5962/bhl.title.105196
  11. Dunn, D.F. (1981) The clownfish sea anemones: Stichodactylidae (Coelenterata: Actiniaria) and other sea anemones symbiotic with pomacentrid fishes. Transactions of the American Philosophical Society, 71 (1), 3–115. https://doi.org/10.2307/1006382
  12. England, K.W. (1987) Certain Actiniaria (Cnidaria, Anthozoa) from the Red Sea and tropical Indo-Pacific Ocean. Bulletin of the British Museum (Natural History), 53, 205–292.
  13. England, K.W. (1988) Redefinitions and systematics of Heteractis aurora, the genera Heteractis and Radianthus, and the family Heteractidae (Cnidaria: Actinaria). Indo-Malayan Zoology, 5 (1), 45–55.
  14. Ehrenberg, C.G. (1834) Beitrage 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, 225–380.
  15. Fautin, D.G. & Allen, G.R. (1992) Field guide to anemonefishes and their host sea anemones. Western Australian Museum, Perth, 78 pp.
  16. Fautin, D.G. (2016) Catalog to families, genera, and species of orders Actiniaria and Corallimorpharia (Cnidaria: Anthozoa). Zootaxa, 4145 (1), 1–449. https://doi.org/10.11646/zootaxa.4145.1.1
  17. Forsskål, P. (1775) Descriptiones Animalium. Mölleri, Hauniae, 164 pp.
  18. Gatins, R. (2014) Fine-scale population structure of two anemones (Stichodactyla gigantea and Heteractis magnifica) in Kimbe Bay, Papua New Guinea. Master’s Thesis, King Abdullah University of Science and Technology, Thuwal. [published online]
  19. Haguenauer, A., Zuberer, F., Siu, G., Cortese, D., Beldade, R. & Mills, S.C. (2021) Deep heat: A comparison of water temperature, anemone bleaching, anemonefish density and reproduction between shallow and mesophotic reefs. Fishes, 6 (3), 37. https://doi.org/10.3390/fishes6030037
  20. Haddon, A.C. & Shackleton, A.M. (1893) Description of some new species of Actiniaria from Torres Straits. Scientific Proceedings of the Royal Dublin Society, 8 (1), 116–131.
  21. Hill, R. & Scott, A. (2012) The influence of irradiance on the severity of thermal bleaching in sea anemones that host anemonefish. Coral Reefs, 31, 273–284. https://doi.org/10.1007/s00338-011-0848-x
  22. Huebner, L.K., Dailey, B., Titus, B.M., Khalaf, M. & Chadwick, N.E. (2012) Host preference and habitat segregation among Red Sea anemonefish: effects of sea anemone traits and fish life stages. Marine Ecology Progress Series, 464, 1–15. https://doi.org/10.3354/meps09964
  23. Jones, G.P., Srinivasan, M., Galbraith, G.F., Berumen, M.L. & Planes, S. (2022) Saving Nemo: Extinction Risk, Conservation Status, and Effective Management Strategies for Anemonefishes. In: Evolution, Development and Ecology of Anemonefishes. CRC Press, Boca Raton, Florida, pp. 285–298. https://doi.org/10.1201/9781003125365-30
  24. Kashimoto, R., Tanimoto, M., Miura, S., Satoh, N., Laudet, V. & Khalturin, K. (2022) Transcriptomes of giant sea anemones from Okinawa as a tool for understanding their phylogeny and symbiotic relationships with anemonefish. Zoological Science, 39 (4), 1–15. https://doi.org/10.2108/zs210111
  25. Klunzinger, C.B. (1877) Die Korallthiere des rothen Meeres. Erster Theil: Die Alcyonarien und Malacodermen. Gutmann‘schen Buchhandlung, Berlin, 98 pp.
  26. Laudet, V. & Ravasi, T. (Eds.) (2022) Evolution, development and ecology of anemonefishes: model organisms for marine science. CRC Press, Boca Raton, Florida, 328 pp. https://doi.org/10.1201/9781003125365
  27. Litsios, G., Sims, C.A., Wüest, R.O., Pearman, P.B., Zimmermann, N.E. & Salamin, N. (2012) Mutualism with sea anemones triggered the adaptive radiation of clownfishes. BMC Evolutionary Biology, 12 (1), 1–15. https://doi.org/10.1186/1471-2148-12-212
  28. Marcionetti, A. & Salamin, N. (2023) Insights into the genomics of clownfish adaptive radiation: the genomic substrate of the diversification. Genome Biology and Evolution, 15 (7), evad088. https://doi.org/10.1093/gbe/evad088
  29. Neave S.A. (1940) Nomenclator Zoologicus. Vol. III. Zoological Society of London, London, 1065 pp.
  30. Quoy, J.R.C. & Gaimard, J.P. (1833) Voyage de Découvertes de l’Astrolabe Exécuté par Ordre du Roi, Pendant les Années 1826–1827–1828–1829, sous le Commandement de M. J. Dumont D’Urville. J. Tastu, Paris, 390 pp.
  31. R Core Team (2022) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. Available from: https://www.R-project.org/ (accessed 17 June 2024)
  32. Rodríguez, E., Fautin, D. & Daly, M. (2024) World List of Actiniaria. Available from: https://www.marinespecies.org/actiniaria (accessed 7 March 2024) https://doi.org/10.14284/568
  33. Rodríguez, E., Titus, B.M. & Lauretta, D. (2024) Case 3885: Priapus giganteus Forsskål, 1775 (currently Stichodactyla gigantea) (Cnidaria, Actiniaria): proposed conservation of prevailing usage of the specific names by the designation of a non-topotypic neotype for Priapus giganteus. Bulletin of Zoological Nomenclature. [in press]
  34. Rodríguez, E., Barbeitos, M.S., Brugler, M.R., Crowley, L.M., Grajales, A., Gusmão, L., 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. https://doi.org/10.1371/journal.pone.0096998
  35. Rowlett, J. (2020) Indo-Pacific Corals. Independently Published, Rowlett, 809 pp.
  36. Rüppell, E. & Leuckart, F.S. (1828) Atlas zu der Reise im Nördlichen Afrika von Eduard Rüppell, Neue Wirbellose Thiere des Rothen Meers. Heinr. Ludw. Brvnner, Frankfurt am Main, 47 pp.
  37. Saville-Kent, W. (1893) The Great Barrier Reef of Australia; its Products and Potentialities. W. H. Allen & Co., London, 387 pp. https://doi.org/10.5962/bhl.title.58247
  38. Shick, J.M. (1991) A Functional Biology of Sea Anemones. In: Calow, P. (Ed.), Functional Biology Series. Chapman & Hall, London, New York, Tokyo, Melbourne and Madras, pp. 1–395. https://doi.org/10.1007/978-94-011-3080-6
  39. Steinberg, R.K., Dafforn, K.A., Ainsworth, T. & Johnston, E.L. (2020) Know thy anemone: A review of threats to octocorals and anemones and opportunities for their restoration. Frontiers in Marine Science, 7, 590. https://doi.org/10.3389/fmars.2020.00590
  40. Steinberg, R.K., Ainsworth, T.D., Moriarty, T., Bednarek, T., Dafforn, K.A. & Johnston, E.L. (2022) Bleaching Susceptibility and Resistance of Octocorals and Anemones at the World’s Southern-Most Coral Reef. Frontiers in Physiology, 13, 726. https://doi.org/10.3389/fphys.2022.804193
  41. Scott, A. & Hoey, A.S. (2017) Severe consequences for anemonefishes and their host sea anemones during the 2016 bleaching event at Lizard Island, Great Barrier Reef. Coral Reefs, 36 (3), 873–873. https://doi.org/10.1007/s00338-017-1577-6
  42. Titus, B.M., Benedict, C., Laroche, R., Gusmão, L.C., Van Deusen, V., Chiodo, T., Meyer, C.P., Berumen, M.L., Bartholomew, A., Yanagi, K., Reimer, J.D., Fujii, T., Daly, M. & Rodríguez, E. (2019) Phylogenetic relationships among the clownfish-hosting sea anemones. Molecular Phylogenetics and Evolution, 139, 106526. https://doi.org/10.1016/j.ympev.2019.106526
  43. Titus, B.M., Laroche, R., Rodríguez, E., Wirshing, H. & Meyer, C.P. (2020) Host identity and symbiotic association affects the taxonomic and functional diversity of the clownfish-hosting sea anemone microbiome. Biology Letters, 16 (2), 20190738. https://doi.org/10.1098/rsbl.2019.0738
  44. Wäldchen, J. & Mäder, P. (2018) Machine learning for image based species identification. Methods in Ecology and Evolution, 9 (11), 2216–2225. https://doi.org/10.1111/2041-210X.13075
  45. Yap, N.W.L., Mitchell, M.L., Quek, Z.B.R., Tan, R., Tan, K.S. & Huang, D. (2023) Taxonomy and molecular phylogeny of the sea anemone Macrodactyla (Haddon, 1898) (Cnidaria, Actiniaria), with a description of a new species from Singapore. Zoological Studies, 62, 1–25.