The first Arctic conspicuously coloured Pleusymtes (Crustacea: Amphipoda: Pleustidae) associated with sea anemones in the Barents Sea

  • Ivan N. Marin A.N. Severtsov Institute of Ecology and Evolution of RAS, Moscow 119071, Russia https://orcid.org/0000-0003-0552-8456
  • Sergey Yu. Sinelnikov I.D. Papanin Institute of Biology of Inland Waters of RAS, Borok, Russia
  • Tatiana I. Antokhina A.N. Severtsov Institute of Ecology and Evolution of RAS, Moscow 119071, Russia
Keywords: biodiversity, Pleustidae, symbiosis, Anthozoa, Arctic

Abstract

The article presents a potentially obligate association of a pleustid amphipod of the genus Pleusymtes (Crustacea: Amphipoda: Pleustidae) with the large sea anemone Urticina eques (Gosse, 1858) (Anthozoa: Actiniaria: Actiniidae) from shallow waters of the Barents Sea. The new species shows a conspicuously striped (disruptive or aposematic) colouration, unlike other Arctic species of the genus, which shows a potential for its permanent connection with anemones. It is possible that this is the first known possibly obligatory anemone-associated species, within the genus and the family Pleustidae. The article discusses the taxonomy, morphological differences from congeners and ecological features of the new species, as well as the known symbiotic associations of sea anemones (as hosts) in Arctic and sub-Arctic waters.

References

Anisimova N.A., Jørgensen L.L., Lyubin P.A. & Manushin I.E. 2010. Mapping and monitoring of benthos in the Barents Sea and Svalbard waters: results from the joint Russian-Norwegian benthic programme 2006–2008. IMR-PINRO Joint Report Series 1–2010.

Avdeev G.V. & Avdeev V.V. 1975. Copepods of the family Staurosomatidae–parasites of Actiniaria. Biologiya Morya 4: 3–12. [In Russian.]

Averincev V.G. 1990. The polychaetous fauna of the Laptev Sea. Issled Fauny Morei 37: 147–186. [In Russian with English summary.]

Azofeifa-Solano J.C., Elizondo-Coto M. & Wehrtmann I.S. 2014. Reproductive biology of the sea anemone shrimp Periclimenes rathbunae (Caridea, Palaemonidae, Pontoniinae), from the Caribbean coast of Costa Rica. In: Wehrtmann I.S. & Bauer R.T. (eds) Proceedings of the Summer Meeting of the Crustacean Society and the Latin American Association of Carcinology, Costa Rica, July 2013. ZooKeys 457: 211–225. https://doi.org/10.3897/zookeys.457.7380

Barnard J.L. 1959. Epipelagic and under-ice Amphipoda (Crustacea) of the central Arctic Basin. In: Bushnell V. (ed.) Scientific studies at Fletcher’s Ice Island T-3, 1952–1955. Geophysical Research Papers 63: 115–153.

Barnard J.L. & Given R.R. 1960. Common pleustid amphipods of southern California, with a projected revision of the family. Pacific Naturalist 1 (17): 37–48.

Bauer R.T. 2004. Remarkable Shrimps – Adaptations and Natural History of the Carideans. University of Oklahoma Press, Norman, OK.

Berge J. 2003. Influence of the physical environment on the distribution of benthic macrofauna along the coasts of Svalbard. AB-321 UNIS Publication Series.

Blake J.A., Watling L. & Scott P.V. 1995. Taxonomic Atlas of the Benthic Fauna of the Santa Maria Basin and the Western Santa Barbara Channel, Volume 12, The Crustacea Part 3. The Amphipoda. Santa Barbara Museum of Natural History, Santa Barbara, CA.

Bousfield E.L. 1973. Shallow-water Gammaridean Amphipoda of New England. Cornell University Press, Ithaca and London.

Bousfield E.L. & Hendrycks E.A. 1994. A revision of the family Pleustidae (Amphipoda: Gammaridea). Part 1. Systematics and biogeography of component subfamilies. Amphipacifica 1: 17-57.

Bousfield E.L. & Hendrycks E.A. 1995. The amphipod family Pleustidae on the Pacific coast of North America. Part III. Subfamilies Parapleustinae, Dactylopleustinae and Pleusirinae: systematics and distributional ecology. Amphipacifica 2: 65–133.

Bresciani J. & Lutzen J. 1962. Parasitic copepods from the west coast of Sweden including some new or little known species. Videnskabelige Meddelelser fra Dansk naturhistorisk Forening i Kjøbenhavn 124: 367–408.

Britayev T.A. 1991. Life cycle of the symbiotic scaleworm Arctonoe vittata (Polychaeta: Polynoidae). Ophelia Supplement 5: 305–312.

Butler T.H. 1980. Shrimps of the Pacific Coast of Canada. Bulletin 202, Department of Fisheries and Oceans, Ottawa.

Chernyshev A.V. & Polyakova N.E. 2019. Nemerteans from the deep-sea expedition KuramBio II with descriptions of three new hoplonemerteans from the Kuril-Kamchatka Trench. Progress in Oceanography 178: 102148. https://doi.org/10.1016/j.pocean.2019.102148

Dunbar M.J. 1954. The amphipod Crustacea of Ungava Bay, Canadian Eastern Arctic. Journal of Fisheries Research Board of Canada 11 (6): 709–798. https://doi.org/10.1139/f54-044

Elliott J.K. 1984. The symbiotic association of the temperate fish Oxylebius pictus and Urticina sea anemones. American Zoologist 24 (3): 24A.

Elliott J.K. 1992. The role of sea anemones as refuges and feeding habitats for the temperate fish Oxylebius pictus. Environmental Biology of Fishes 35: 381–400. https://doi.org/10.1007/BF00004991

Elmhirst R. 1925. Associations between the amphipod genus Metopa and coelenterates. Scottish Naturalist 155: 149–150.

Fenwick G.D. & Steele D.H. 1983. Amphipods of Placentia Bay, Newfoundland. Memorial University Newfoundland, Occasional Papers in Biology 7: 1–22.

Gamo S. & Shinpo Y. 1992. A new gammaridean amphipod Pleusymtes symbiotica, ectosymbiotic with a Japanese gorgonacean octocoral, Melithaea flabellifera (Kükenthal) from Sagami Bay. Scientific Reports of Yokohama State University, Section B 39: 1–11.

Gibson R. 1986. Redescription and taxonomic reappraisal of Nemertopsis actinophila Bürger, 1904 (Nemertea: Hoplonemertea: Monostilifera). Bulletin of Marine Science 39: 42–60.

Gurjanova E. 1951. Bokoplavy morei SSSR i sopredelnykh vod (Amphipoda,Gammaridea). [Amphipods of the seas of USSR and adjacent waters (Amphipoda, Gammaridea).] Opredeliteli po faune SSSR, Akademiya Nauk SSSR 41: 1–1029.

Hartnoll R.G. 1970. The relationship of an amphipod and a spider crab with the snakelocks anemone. Report of the Marine Biological Station, Port Erin 83: 37–42.

Ho J.-Sh. & Ivanenko V.N. 2003. Doridicola indistinctus n. sp. (Copepoda: Poecilostomatoida: Rhynchomolgidae) associated with the soft coral Gersemia fruticosa Sars (Octocorallia: Alcyonacea: Nephtheidae) from the White Sea. Systematic Parasitology 85 (3): 235–241. https://doi.org/10.1007/s11230-013-9419-6

Horton T., Lowry J., De Broyer C., Bellan-Santini D., Coleman C.O., Corbari L., Costello M.J., Daneliya M., Dauvin J.-C., Fišer C., Gasca R., Grabowski M., Guerra-García J.M., Hendrycks E., Hughes L., Jaume D., Jazdzewski K., Kim Y.-H., King R., Krapp-Schickel T., LeCroy S., Lörz A.-N., Mamos T., Senna A.R., Serejo C., Sket B., Souza-Filho J.F., Tandberg A.H., Thomas J.D., Thurston M., Vader W., Väinölä R., Vonk R., White K. & Zeidler W. 2021. World Amphipoda Database. Pleusymtes J.L. Barnard, 1969. Accessed through: World Register of Marine Species. Available from http://www.marinespecies.org/aphia.php?p=taxdetails&id=101732 [accessed 20 Oct. 2021].

Howard F.G. 1982. Of shrimps and sea anemones; of prawns and other things. Scottish Fisheries Bulletin 47: 39–40.

Humes A.G. 1982. A review of Copepoda associated with sea anemones and anemone-like forms (Cnidaria, Anthozoa). Transactions of the American Philosophical Society 72 (2): 1–120. https://doi.org/10.2307/1006447

Humes A.G. & Stock J.H. 1973. A revision of the family Lichomolgidae Kossmann, 1877, cyclopoid copepods mainly associated with marine invertebrates. Smithsonian Contributions to Zoology 127: 1–368. https://doi.org/10.5479/si.00810282.127

Hurt C., Silliman K., Anker A. & Knowlton N. 2003. Ecological speciation in anemone-associated snapping shrimps (Alpheus armatus species complex). Molecular Ecology 22 (17): 4532–4548. https://doi.org/10.1111/mec.12398

Jonsson L.G., Lundälv T. & Johannesson K. 2001. Symbiotic associations between anthozoans and crustaceans in a temperate coastal area. Marine Ecology Progress Series 209: 189–195. https://doi.org/10.3354/meps209189

Knowlton N. & Keller B.D. 1985. Two more sibling species of alpheid shrimps associated with the Caribbean sea anemones Bartholomea annulata and Heteractis lucida. Bulletin of Marine Science 37 (3): 893–904.

Kodama M., Hayakawa J. & Kawamura T. 2020. Aggregations of Dactylopleustes (Amphipoda: Pleustidae) on diseased areas of the host sea urchin, Strongylocentrotus intermedius. Marine Biodiversity 50: 62. https://doi.org/10.1007/s12526-020-01100-9

Krapp-Schickel T. & Vader W. 2015. Stenothoids living with or on other animals. Zoosystematics and Evolution 91 (2): 215–246. https://doi.org/10.3897/zse.91.5715

Krapp-Schickel T., Häussermann V. & Vader W. 2015. A new Stenothoe species (Crustacea: Amphipoda: Stenothoidae) living on Boloceropsis platei (Anthozoa: Actiniaria) from Chilean Patagonia. Helgoland Marine Research 69: 213–220. https://doi.org/10.1007/s10152-015-0430-y

Kumagai N. 2001. Population Persistence of Pleusymtes symbiotica (Amphipoda: Pleustidae) associated with Melithaeid Gorgonians. Unpublished Master Science thesis, University of Tsukuba.

Kutz S.J., Hoberg E.P., Polley L. & Jenkins E.J. 2005. Global warming is changing the dynamics of Arctic host-parasite systems. Proceedings of the Royal Society (B) 272: 2571–2576. https://doi.org/10.1098/rspb.2005.3285

Lincoln R.J. 1979. British Marine Amphipoda: Gammaridea. British Museum (Natural History), London.

Macnaughton M.O., Thormar J. & Berge J. 2007. Sympagic amphipods in the Arctic pack ice: redescriptions of Eusirus holmii Hansen, 1887 and Pleusymtes karstensi (Barnard, 1959). Polar Biology 30: 1013–1025. https://doi.org/10.1007/s00300-007-0260-8

Marin I.N. 2013. Atlas of Decapod Crustaceans of Russia. KMK Scientific Press, Moscow.

Marin I. & Antokhina T. 2020. Hidden burrow associates: macrosymbiotic assemblages of subtidal deep-burrowing invertebrates in the northern part of the Sea of Japan. Marine Biodiversity 50 (4): 1–22. https://doi.org/10.1007/s12526-020-01065-9

Marin I.N. & Sinelnikov S.Y. 2016. Diversity and ecological features of symbiotic communities associated with large hermit crabs along the southern part of the Russian coast of the Sea of Japan. Arthropoda Selecta 25 (2): 171–182. https://doi.org/10.15298/arthsel.25.2.04

Marin I.N. & Sinelnikov S.Y. 2017. Amphipod assemblage found on sublittoral hydroids in the White Sea with the special remarks to symbiotic association of stenothoid Metopa alderi with hydroid Tubularia larynx. Ukrainian Journal of Ecology 7 (4): 473–479. https://doi.org/10.15421/2017_146

Marin I., Sinelnikov S. & Sokolova A. 2013. Ecological remarks and re-description of the hermit crab-associated pleustid amphipod Pleusymtes japonica (Gurjanova, 1938) (Crustacea: Amphipoda: Pleustidae: Pleusymtinae) from the Russian coasts of the Sea of Japan. Zootaxa 3640 (4): 581–588. https://doi.org/10.11646/zootaxa.3640.4.6

Martin O., Macnaughton M.O., Thormar J. & Berge J. 2007. Sympagic amphipods in the Arctic pack ice: redescriptions of Eusirus holmii Hansen, 1887 and Pleusymtes karstensi (Barnard, 1959). Polar Biology 30: 1013–1025. https://doi.org/10.1007/s00300-007-0260-8

McGinitie G.E. 1955. Distribution and ecology of the marine invertebrates of Point Barrow, Alaska. Smithsonian Miscellaneous Collections 128 (9): I–IV, 1–201.

Merilaita S. & Kelley J.L. 2018. Scary clowns: adaptive function of anemonefish coloration. Journal of Evolutionary Biology 31 (10):1558-1571. https://doi.org/10.1111/jeb.13350

Merilaita S. & Ruxton G.D. 2007. Aposematic signals and the relationship between conspicuousness and distinctiveness. Journal of Theoretical Biology 245 (2): 268–277. https://doi.org/10.1016/j.jtbi.2006.10.022

Myers A.A. & Hall-Spencer J.M. 2004. A new species of amphipod crustacean, Pleusymtes comitari sp. nov., associated with gorgonians on deep-water coral reefs off Ireland. Journal of the Marine Biological Association of the United Kingdom 84 (5): 1029–1032. https://doi.org/10.1017/s0025315404010367h

Okada Y.K. 1927. Staurosoma, copepode parasite d’une actinie: description de Staurosoma caulleryi sp. n. Annotationes Zoologicae Japonenses 11: 173–183.

Pettibone M.H. 1963. Marine Polychaete Worms of the New England Region. 1. Families Aphroditidae through Trochochaetidae. Smithsonian Institution, Washington. https://doi.org/10.5479/si.03629236.227.1

Ridley H.N. 1879. On a new copepod of the genus Doridicola. The Annals and Magazine of Natural History, Series 5 4 (24): 458. https://doi.org/10.1080/00222937908679866

Sanderson J.M. 1973. A catalogue of the Amphipoda (Crustacea) in the collection of the late D.M. Reid, now in the Royal Scottish Museum, Edinburgh. Royal Scottish Museum, Information Series, Natural History 1: 1–79.

Sars G.O. 1876. Prodromus descriptionis crustaceorum ft pycnogonidarum, quae in expeditione Norvegica anno 1876, observavit. Archiv for Mathematik og Naturvidenskab 2: 227–271.

Sars G.O. 1885. Crustacea I. Den Norske Nordhavs-Expedition, 1876–1878, Zoologi (Norwegian North Atlantic Expedition 1876–1878, Zoology) 6 (14): 1–280. https://doi.org/10.5962/bhl.title.2168

Sars G.O. 1893. Amphipoda. Part XVI. Paramphitoidae, Epimeridae (part). In: An Account of the Crustacea of Norway, with Short Descriptions and Figures of all the Species 1: 343–364. https://doi.org/10.5962/bhl.title.1164

Sars M. 1857. Antheacheres Duebenii Sars, nov. gen. & spec. Forhandlinger ved de Skandinaviske Naturforskeres Möde 7 (1856): 175–181.

Sars M. 1870. Bidrag til Kundskab om Christianiafjordens Fauna. Nyt Magazin for Naturvidensk 17: 113–226. https://doi.org/10.5962/bhl.title.8730

Shimek R.L. 2004. Marine Invertebrates: 500+ Essential-to-know Aquarium Species. Microcosm/TFH.

Solyanko K., Spiridonov V.A. & Naumov A.D. 2011. Benthic fauna of the Gorlo Strait, White Sea: a first species inventory based on data from three different decades from the 1920s to 2000s. Marine Biodiversity 41 (3): 441–453. https://doi.org/10.1007/s12526-010-0065-9

Stappers L. 1911. Crustacés malacostracés. Campagne Arctique de 1907 du Duc d’Orléans Vol. 7. Imprimerie scientifique Charles Bulens, Bruxelles.

Stevens B.G. & Anderson P.J. 1999. An association between the anemone Cribrinopsis fernaldi, and shrimps of the families Hippolytidae and Pandalidae. Northwest Atlantic Fisheries Organization, Scientific Council Meeting (Serial No N4153), Dartmouth: 1–7.

Tandberg A.H.S., Schander C. & Pleijel F. 2010. First record of the association between the amphipod Metopa alderii and the bivalve Musculus. Marine Biodiversity Records 3: e5. https://doi.org/10.1017/S1755267209991102

Tarakhovskaya E.R. & Garbary D.J. 2009. Halocladius variabilis (Diptera: Chironomidae): a marine insect symbiotic with seaweeds from the White Sea, Russia. Journal of the Marine Biological Association of the United Kingdom 89 (7): 1381–1385. https://doi.org/10.1017/S0025315409000071

Taton H. 1934. Contribution à l’étude du copepode gallicole Mesoglicola delagei Quidor. Travaux de la Station biologique de Roscoff 12: 53–68.

Theel H. 1907. Om utvecklingen af Sveriges zoologiska hafsstation Kristineberg och om djur- lifvet i angransande haf och fjordar. Arkiv för Zoologi 4: 1–136.

Vader W. 1967. Notes on Norwegian amphipods 1–3. Sarsia 29 (1): 283–294. https://doi.org/10.1080/00364827.1967.10411089

Vader W. 1970a. Amphipods associated with the sea anemone Bolocera tuediae, in western Norway. Sarsia 43 (1): 87–98. https://doi.org/10.1080/00364827.1970.10411171

Vader W. 1970b. Antheacheres duebeni M. Sars, a copepod parasitic in the sea anemone Bolocera tuediae (Johnston). Sarsia 43 (1): 99–106. https://doi.org/10.1080/00364827.1970.10411172

Vader W. 1975. The sea anemone Bolocera tuediae and its copepod parasite, Antheacheres duebeni, in northern Norway. Astarte 8: 37–39.

Vader W. 1983. Associations between amphipods (Crustacea: Amphipoda) and sea anemones (Anthozoa, Actiniaria). Memoirs of the Australian Museum 18: 141–153. https://doi.org/10.3853/j.0067-1967.18.1984.380

Vader W. & Tandberg A.H.S. 2020. Amphipods and sea anemones, an update. Journal of Crustacean Biology 40 (6): 872–878. https://doi.org/10.1093/jcbiol/ruaa061

Yamaguchi A. 2006. Suctorian ciliate epibionts on calanoid copepods in the subarcticPacific. Bulletin of Plankton Society of Japan 53: 29–36. [In Japanese with English abstract.]

Zimina O., Anisimova N. & Lubina O. 2019. Species composition and peculiarities of the distribution of benthic Peracarida (Crustacea, Malacostraca) in the Barents Sea, based on surveys 2003–2008. Biology Bulletin 46 (8): 1209–1230. https://doi.org/10.1134/S1062359019080181

Published
2022-05-19
How to Cite
Marin, I. N., Sinelnikov, S. Y., & Antokhina, T. I. (2022). The first Arctic conspicuously coloured Pleusymtes (Crustacea: Amphipoda: Pleustidae) associated with sea anemones in the Barents Sea. European Journal of Taxonomy, 819(1), 166–187. https://doi.org/10.5852/ejt.2022.819.1789
Section
Research article