Hostname: page-component-76fb5796d-2lccl Total loading time: 0 Render date: 2024-04-26T06:29:47.246Z Has data issue: false hasContentIssue false

Biogeographic patterns of distribution of the mollusc Zelentia ninel (Nudibranchia, Trinchesiidae)

Published online by Cambridge University Press:  04 August 2023

Fredrik Broms*
Affiliation:
North Norwegian Humpback Whale Catalogue (NNHWC), Straumsvegen 238, N-9109 Kvaløya, Norway
Torkild Bakken
Affiliation:
NTNU University Museum, Norwegian University of Science and Technology, N-7491, Trondheim, Norway
Alexander Martynov
Affiliation:
Zoological Museum, Moscow State University, Bolshaya Nikitskaya Str. 6, 125009 Moscow, Russia
Tatiana Korshunova
Affiliation:
Koltzov Institute of Developmental Biology RAS, 26 Vavilova Str., 119334 Moscow, Russia
*
Corresponding author: Fredrik Broms; Email: fredrik.broms@gmail.com

Abstract

In the present contribution we report, for the first time, records of the nudibranch Zelentia ninel from Norway. The species is previously known only from the Barents Sea coast in northern Russia where it was described for the first time in 2017. Records of Z. ninel from six different localities in northern Norway from 2019–2023 are presented and discussed. The identity of the specimens was determined by investigation of external and internal morphology as well as molecular analysis of preserved specimens. Photographs of live specimens and radulae of preserved specimens are presented, and species delimitation is confirmed by molecular phylogenetic analysis. In order to assess the biogeographic distribution of Z. ninel based on all available information, recent unanticipated genetic data supporting a putative occurrence of Z. ninel at the Aleutian Islands, Alaska is also discussed where we provide arguments in support of occasional anthropogenic transportation outside its natural range. The present records significantly expand the known natural range of distribution for Z. ninel and demonstrate that the species is not restricted to the Russian Barents Sea coast but that the range encompasses also at least northern Norway. These data can provide important insights to the understanding of natural ranges of marine invertebrates across biogeographical regions affected by rapid ongoing climatic change.

Type
Research Article
Copyright
Copyright © The Author(s), 2023. Published by Cambridge University Press on behalf of Marine Biological Association of the United Kingdom

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Andrews, AJ, Christiansen, JS, Bhat, S, Lynghammar, A, Westgaard, J-I, Pampoulie, C and Præbel, K (2019) Boreal marine fauna from the Barents Sea disperse to Arctic Northeast Greenland. Scientific Reports 9, 5799.CrossRefGoogle ScholarPubMed
Anisimova, NA, Jørgensen, LL, Ljubin, PA and Manushin, IE (2011) Benthos. In Jakobsen, T and Ozhigin, VK (eds), The Barents Sea – Ecosystem, Resources and Management. Half a Century of Russian–Norwegian Cooperation. Trondheim: Tapir Academic Press, pp. 121160.Google Scholar
Ascanius, P (1774) Beskrivelse over en Norske sneppe og et sodyr. Det Kongelige Norske Videnskabelige Selskabs Skrifter. Trondhejm 5, 153158.Google Scholar
Bakken, T, Hårsaker, K and Daverdin, M (2023) Marine invertebrate collection NTNU University Museum. Version 1.1393. Norwegian University of Science and Technology. Occurrence dataset https://doi.org/10.15468/ddbs14 (Accessed via GBIF.org 14 March 2023).CrossRefGoogle Scholar
Berge, J, Johnsen, G, Nilsen, F, Gulliksen, B and Slagstad, D (2005) Ocean temperature oscillations enable reappearance of blue mussels Mytilus edulis in Svalbard after a 1000 year absence. Marine Ecology Progress Series 303, 167175.CrossRefGoogle Scholar
Briggs, JC (1995) Global Biogeography. Amsterdam: Elsevier.Google Scholar
Buhl-Mortensen, P, Dolan, MFJ, Ross, RE, Gonzalez-Mirelis, G, Buhl-Mortensen, L, Bjarnadóttir, LR and Albretsen, J (2020) Classification and mapping of Benthic biotopes in Arctic and Sub-Arctic Norwegian waters. Frontiers in Marine Science 7, 271.CrossRefGoogle Scholar
Chan, FT, Stanislawczyk, K, Sneekes, AC, Dvoretsky, A, Gollasch, S, Minchin, D, David, M, Jelmert, A, Albretsen, J and Bailey, SA (2018) Climate change opens new frontiers for marine species in the Arctic: current trends and future invasion risks. Global Change Biology 25, 2538.CrossRefGoogle ScholarPubMed
Derjugin, KM (1915) Fauna of the Kola Bay and the condition of its existence. Zapiski Sankt-Peterburgskoi Imperatorskoi Akademii Nauk, Fiziko-Matematicheskoe Otdelenie, Ser 8, 1929.Google Scholar
Descôteaux, R, Ershova, E, Wangensteen, OS, Præbel, K, Renaud, PE, Cottier, F and Bluhm, BA (2021) Meroplankton diversity, seasonality and life-history traits across the Barents sea polar front revealed by high-throughput DNA barcoding. Frontiers in Marine Science 8, 677732.CrossRefGoogle Scholar
Dons, C (1942) Norges strandfauna XXVII-XXIX. Bakgjellesnegler 1–3. Det Kongelige Norske Videnskabelige Selskabs Skrifter 14, 165194.Google Scholar
Evertsen, J and Bakken, T (2002) Heterobranchia (Mollusca, Gastropoda) from northern Norway, with notes on ecology and distribution. Fauna norvegica 22, 1522.Google Scholar
Evertsen, J and Bakken, T (2005) Nudibranch diversity (Gastropoda, Heterobranchia) along the coast of Norway. Fauna norvegica 25, 137.Google Scholar
Evertsen, J and Bakken, T (2013) Diversity of Norwegian sea slugs (Nudibranchia): new species to Norwegian coastal waters and new data on distribution of rare species. Fauna norvegica 32, 4552.CrossRefGoogle Scholar
Evertsen, J and Bakken, T (2023) Nudibranch sea slugs in Norway – biological diversity. Available at https://www.ntnu.edu/museum/norwegian-nudibranch (Accessed online 14 March 2023).Google Scholar
Fossheim, M, Primicerio, R, Johannesen, E, Ingvaldsen, RB, Aschan, MM and Dolgov, AV (2015) Recent warming leads to a rapid borealization of fish communities in the Arctic. Nature Climate Change 5, 16.CrossRefGoogle Scholar
Frainer, A, Primicerio, R, Kortsch, S, Aune, M, Dolgov, AV, Fossheim, M and Aschan, MM (2017) Climate-driven changes in functional biogeography of Arctic marine fish communities. Proceedings of the National Academy of Sciences 114, 1220212207.CrossRefGoogle ScholarPubMed
Friele, H and Grieg, JA (1901) Nudibranchiata. Zoologi. Mollusca. Den Norske Nordhavs-Expedition, 1876–1878 16, 1129.Google Scholar
Friele, H and Hansen, A (1876) Bidrag til Kundskaben om de norske Nudibranchier. Forhandlinger i Videnskabs-Selskabet i Christiania 1875, 6980.Google Scholar
Galkin, YI (1979) The history of bottom fauna research in the Barents Sea. In Kuznetsov, AP (ed.), Ecology of the Sea Shelf Benthic Fauna and Flora. Moscow: P.P. Shirshov Institute of Oceanology, USSR Academy of Science, pp. 112127.Google Scholar
García, FJ and Bertsch, H (2009) Diversity and distribution of the Gastropoda Opisthobranchia from the Atlantic Ocean: a global biogeographic approach. Scientia Marina 73, 153160.Google Scholar
Grieg, JA (1897) Bidrag til Kundskaben om Vestlandets mollusker. Bergens Museums Aarbog 1896, 132.Google Scholar
Grieg, JA (1913) Nudibranchiate mollusker indsamlede av den norske fiskeridamper “Michael Sars”. Det Kongelige Norske Videnskabernes Selskabs Skrifter 1912, 113.Google Scholar
Gunnerus, JE (1770) Nogle smaa rare og meestendeelen nye norske søedyr. Skrifter som udi det Kiøbenhavnske Selskab af Lærdom og Videnskabers Elskere ere fremlagte og oplæste i Aarene 1765, 1766, 1767, 1768 og 1769 10, 166176.Google Scholar
Hamilton, CD, Lydersen, C, Ims, RA and Kovacs, KM (2015) Predictions replaced by facts: a keystone species’ behavioural responses to declining arctic sea-ice. Biology Letters 11, 20150803.CrossRefGoogle ScholarPubMed
Hjort, J, Nordgaard, O and Gran, HH (1899) Report on Norwegian marine investigations, 1895–97. Bergens Museums Skrifter 6, 130.Google Scholar
Hoegh-Guldberg, O and Bruno, JF (2010) The impact of climate change on the world's marine ecosystems. Science (New York, N.Y.) 328, 15231528.CrossRefGoogle ScholarPubMed
Høisæter, T, Brattegard, T and Sneli, J-A (1997) Heterobranchia. In Brattegard, T. and Holte, T. (eds.). Distribution of marine, benthic macro-organisms in Norway. Research Report for DN 1997-1. Directorate for Nature Management, pp. 247258.Google Scholar
Johannesen, E, Jørgensen, LL, Fossheim, M, Primicerio, R, Greenacre, M, Ljubin, PA, Dolgov, AV, Ingvaldsen, RB, Anisimova, NA and Manushin, IE (2016) Large-scale patterns in community structure of benthos and fish in the Barents Sea. Polar Biology 40, 237246.CrossRefGoogle Scholar
Katoh, K, Misawa, K, Kuma, K and Miyata, T (2002) MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acid Research 30, 30593066.CrossRefGoogle ScholarPubMed
Korshunova, T, Bakken, T, Grøtan, VV, Johnson, KB, Lundin, K and Martynov, A (2020a) A synoptic review of the family Dendronotidae (Mollusca: Nudibranchia): a multilevel organismal diversity approach. Contributions to Zoology 90, 93153.CrossRefGoogle Scholar
Korshunova, T, Driessen, F, Picton, B and Martynov, A (2021a) The multilevel organismal diversity approach deciphers difficult to distinguish nudibranch species complex. Scientific Reports 11, 18323.CrossRefGoogle ScholarPubMed
Korshunova, T, Fletcher, K, Lundin, K, Picton, B and Martynov, A (2018) The genus Zelentia is an amphi-boreal taxon expanded to include three new species from the north Pacific and Atlantic oceans (Gastropoda: Nudibranchia: Trinchesiidae). Zootaxa 4482, 297321.CrossRefGoogle ScholarPubMed
Korshunova, T, Malmberg, K, Prkić, J, Petani, A, Fletcher, K, Lundin, K and Martynov, A (2020b) Fine-scale species delimitation: speciation in process and periodic patterns in nudibranch diversity. ZooKeys 917, 1550.CrossRefGoogle ScholarPubMed
Korshunova, TA and Martynov, AV (2022) Increased information on biodiversity from the neglected part of the North Pacific contributes to the understanding of phylogeny and taxonomy of nudibranch molluscs. Canadian Journal of Zoology 100, 436451.CrossRefGoogle Scholar
Korshunova, TA, Martynov, AV, Bakken, T, Evertsen, J, Fletcher, K, Mudianta, WI, Lundin, K, Schrödl, M and Picton, B (2017b) Polyphyly of the traditional family Flabellinidae affects a major group of Nudibranchia: aeolidacean taxonomic reassessment with descriptions of several new families, genera, and species (Mollusca, Gastropoda). ZooKeys 717, 1139.CrossRefGoogle Scholar
Korshunova, TA, Martynov, AV, Bakken, T and Picton, B (2017c) External diversity is restrained by internal conservatism: new nudibranch mollusk contributes to the cryptic species problem. Zoologica Scripta 46, 110.CrossRefGoogle Scholar
Korshunova, TA, Martynov, A and Picton, B (2017a) Ontogeny as an important part of integrative taxonomy in tergipedid aeolidaceans (Gastropoda: Nudibranchia) with a description of a new genus and species from the Barents Sea. Zootaxa 4324, 122.CrossRefGoogle Scholar
Korshunova, T, Picton, B, Furfaro, G, Mariottini, P, Pontes, M, Prkić, J, Fletcher, K, Malmberg, K, Lundin, K and Martynov, A (2019) Multilevel fine-scale diversity challenges the ‘cryptic species’ concept. Scientific Reports 9, 6732.CrossRefGoogle ScholarPubMed
Korshunova, TA, Sanamyan, NP, Sanamyan, KE, Bakken, T, Lundin, K, Fletcher, K and Martynov, AV (2021b) Biodiversity hotspot in cold waters: a review of the genus Cuthonella with descriptions of seven new species (Mollusca, Nudibranchia). Contributions to Zoology 90, 216283.CrossRefGoogle Scholar
Kortsch, S, Primicerio, R, Fossheim, M, Dolgov, AV and Aschan, M (2015) Climate change alters the structure of arctic marine food webs due to poleward shifts of boreal generalists. Proceedings of the Royal Society B: Biological Sciences 282, 20151546.CrossRefGoogle ScholarPubMed
Lovén, SL (1846) Index molluscorum litora Scandinaviae occidentalia habitantium. Öfversigt af Konglige Vetenskaps Akademiens Forhandlinger, Stockholm 3, 135160.Google Scholar
Martinsson, S, Malmberg, K, Bakken, T, Korshunova, T, Martynov, A and Lundin, K (2021) Species delimitation and phylogeny of Doto (Nudibranchia: Dotidae) from the Northeast Atlantic, with a discussion on food specialization. Journal of Zoological Systematics and Evolutionary Research 59, 17541774.CrossRefGoogle Scholar
Martynov, AV and Korshunova, TA (2011) Opisthobranch Molluscs of the Seas of Russia. A Colour Guide to Their Taxonomy and Biology. Moscow: Fiton Press, 231 pp.Google Scholar
Martynov, AV, Korshunova, TA and Savinkin, OV (2006) Shallow-water opisthobranch molluscs of the Murman coast of the Barents Sea, with new distributional data and remarks on biology. Ruthenica 16, 5972.Google Scholar
Miller, A and Ruiz, G (2014) Arctic shipping and marine invaders. Nature Climate Change 4, 413416.CrossRefGoogle Scholar
Müller, OF (1776) Zoologiae Danicae. Prodromus seu animalium Daniae et Norvegiae ingenarum characteres, nomina, et synonyma imprimis popularium, xxxii. 282 pp.CrossRefGoogle Scholar
Neuhaus, J, Rauch, C, Bakken, T, Picton, B, Pola, M and Malaquias, MAE (2021) The genus Jorunna (Nudibranchia: Discodorididae) in Europe: a new species and a possible case of incipient speciation. Journal of Molluscan Studies 87, eyab028.CrossRefGoogle Scholar
Nimbs, MJ, Larkin, M, Davis, TR, Harasti, D, Willan, RC and Smith, SDA (2016) Southern range extensions for twelve heterobranch sea slugs (Gastropoda: Heterobranchia) on the eastern coast of Australia. Marine Biodiversity Records 9, 27.CrossRefGoogle Scholar
Odhner, NH (1907) Northern and Arctic invertebrates in the collection of the Swedish State Museum (Riksmuseum). III. Opisthobranchia and pteropoda. Kungliga Svenska vetenskapsakademiens handlingar 41, 1118.Google Scholar
Odhner, NH (1922) Norwegian Opisthobranchiate Mollusca in the collection of the Zoological Museum of Kristiania. Nyt Magazin for Naturvidenskaberne 60, 149.Google Scholar
Odhner, NH (1929) Aeolidiiden aus dem nördlichen Norwegen. Tromsø Museums Aarshefter 1927, 122.Google Scholar
Odhner, N (1939) Opisthobranchiate Mollusca from the western and northern coasts of Norway. Det Kongelige Norske Videnskabernes Selskabs Skrifter 1, 193.Google Scholar
Pecl, GT, Araújo, MB, Bell, JD, Blanchard, J, Bonebrake, TC, Chen, I, Clark, TD, Colwell, RK, Danielsen, F, Evengård, B, Falconi, L, Ferrier, S, Frusher, S, Garcia, RA, Griffis, R, Hobday, AJ, Janion-Scheepers, C, Jarzyna, MA, Jennings, S, Lenoir, J, Linnetved, HI, Martin, VY, McCormack, PC, McDonald, J, Mitchell, NJ, Mustonen, T, Pandolfi, JM, Pettorelli, N, Popova, E, Robinson, SA, Scheffers, BR, Shaw, JD, Sorte, CJB, Strugnell, JM, Sunday, JM, Tuanmu, M, Vergés, A, Villanueva, C, Wernberg, T, Wapstra, E and Williams, SE (2017) Biodiversity redistribution under climate change: Impacts on ecosystems and human well-being. Science (New York, N.Y.) 355, 19.CrossRefGoogle ScholarPubMed
Pecuchet, L, Blanchet, M-A, Frainer, A, Husson, B, Jørgensen, LL, Kortsch, S and Primicerio, R (2020) Novel feeding interactions amplify the impact of species redistribution on an Arctic food web. Global Change Biology 26, 48944906.CrossRefGoogle Scholar
Puillandre, N, Brouillet, S and Achaz, G (2021) ASAP: assemble species by automatic partitioning. Molecular Ecology Resources 21, 609620.CrossRefGoogle ScholarPubMed
Ratnasingham, S and Hebert, PDN (2007) BOLD: the barcode of life data system (http://www.barcodinglife.org). Molecular Ecology Notes 7, 355364.CrossRefGoogle ScholarPubMed
Renaud, PE, Sejr, MK, Bluhm, BA, Sirenko, B and Ellingsen, IH (2015) The future of Arctic benthos: expansion, invasion, and biodiversity. Progress in Oceanography 139, 244257.CrossRefGoogle Scholar
Risso-Dominguez, GJ (1963) Measuring nudibranchs: a standardization for descriptive purposes. Journal of Molluscan Studies 35, 193202.Google Scholar
Ronquist, F, Teslenko, M, van der Mark, P, Ayres, D, Darling, A, Höhna, S, Larget, B, Liu, L, Suchard, M and Huelsenbeck, J (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology 61, 539542.CrossRefGoogle ScholarPubMed
Sars, M (1829) Bidrag til soedyrene naturhistorie: cand. theol. medlem af den physiographiske forening i Christiania, pt. 1, pp. 159.Google Scholar
Sars, GO (1878) Bidrag til kundskaben om Norges Arktiske fauna. I. Mollusca Regionis Arcticae Norvegiae, Oversigt Over de i Norges Arktiske Region Forekommende. Bløddyr., xiii + 466 pp., 34 pls. Universitetsprogram, Christiania.CrossRefGoogle Scholar
Sørensen, CG, Rauch, C, Pola, M and Malaquias, MAE (2020) Integrative taxonomy reveals a cryptic species of the nudibranch genus Polycera (Polyceridae) in European waters. Journal of the Marine Biological Association of the United Kingdom 100, 733752.CrossRefGoogle Scholar
Stamatakis, A, Hoover, P and Rougemont, J (2008) A rapid bootstrap algorithm for the RAxML web servers. Systematic Biology 75, 758771.CrossRefGoogle Scholar
Tamura, K, Stecher, G and Kumar, S (2021) MEGA11: molecular evolutionary genetics analysis version 11. Molecular Biology and Evolution 38, 30223027.CrossRefGoogle ScholarPubMed