Abstract
The pelagic mollusk Clione is a naked pteropod with a sympatric two-species distribution in the southern Okhotsk Sea, Japan, consisting of the morphologically and genetically distinct C. elegantissima and C. okhotensis. Clione elegantissima appears in both winter and spring, and body length differs between the winter coastal population (WCP, January to March, 10–20 mm) and the spring offshore population (SOP, April to July; up to 30 mm). This body size difference and temporal-spatial separation of the populations suggests that the SOP is either a cryptic species or C. limacine drifted from the Subarctic Atlantic Ocean or an interspecies of C. elegantissima resulting from reproductive isolation. We investigated the taxonomic positions of both populations using morphological and genetic analyses and identified both as C. elegantissima with very high genetic similarity. We explain the occurrence of spatio-temporal isolated populations using the water mass dynamics in the Okhotsk Sea. Warm water entering the southern Okhotsk Sea around Japan through the Soya Straits is divided into the Soya Warm Water (SWW: June to November) and the Forerunner of the SWW (FSWW: March to May); cold water entering the Okhotsk Sea around Japan, east of Sakhalin Island, is divided into the East Sakhalin Current Water (ESCW: November to April). The Cold Water Belt (CWB) is frequently formed off the SWW during summer and autumn and comprises upwelling cold water originating from either subsurface water of the Japan Sea off Sakhalin or Okhotsk Sea bottom water. We present the temporal-spatial isolation mechanism of WCP and SOP per the SWW, FSWW, ESCW, and CWB dynamics.
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References
Agersborg HPK (1923) Gymnosomatous Pteropoda from Friday Harbor, Washington. Ann Sci Nat 10:391–402
Aota M (1975) Studies on the soya warm current. Low Temp Sci A33:151–172
Azuma N, Yamazaki T, Chiba S (2011) Mitochondrial and nuclear DNA analysis revealed a cryptic species and genetic introgression in Littorina sitkana (Mollusca, Gastropoda). Genetica 139:1399–1408
Azuma T (1995) Biological mechanisms enabling sympatry between salmonids with special reference to sockeye and chum salmon in oceanic waters. Fisheries Research 24 (4):291-300
Chichvarkhin A (2016) Shallow water sea slugs (Gastropoda: Heterobranchia) from the northwestern coast of the Sea of Japan, north of Peter the Great Bay, Russia. Peer J 4:e2774. https://doi.org/10.7717/peerj2774
Comiso JC, Maymard NG, Smith WO, Sullivan CW (1990) Satellite ocean color studies of Antarctic ice edges in summer and autumn. J Geophys Res Oceans 95:9481–9496. https://doi.org/10.1029/JC095iC06p09481
Conover RJ, Lalli CM (1972) Feeding and growth in Clione limacina (Phipps), a pteropod mollusc. J Exp Mar Biol Ecol 9:279–302
Dall WH (1871) Descriptions of sixty new forms of mollusks from the west coast of North America and the North Pacific Ocean, with notes on others already described. Am J Conchol 7:93–160 pls. 13–16
Davis ND, Volkov AV, Efimkin AY, Kuznetsova NA, Armstrong JL, Sakai O (2009) Review of basic salmon food habits studies. North Pacific Anadromous Fish Commission Bulletin 5:197–208
Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology 3:294–299
Gilmer R, Lalli C (1990) Bipolar variation in Clione, a gymnosomatous pteropod. Am Malacol Bull 8:67–75
Haigh R, Ianson D, Holt CA, Neate HE, Edwards AM (2015) Effects of ocean acidification on temperate coastal marine ecosystems and fisheries in the Northeast Pacific. PLoS One e0117533:10. https://doi.org/10.1371/journal.pone.0117533
Hamaoka S (2002) Seasonal change and breeding season of Clione limacina in coastal Okhotsk Sea. Gekkan Kaiyo 30:172–177
Inaba Y, Okutani T (1999) Clione limacina occurred in Oarai Marine at 36°20′N. Newsl Malacol Soc Jpn 29:47–49
Jennings RM, Bucklin A, Ossenbrugger H, Hopcroft RR (2010) Species diversity of planktonic gastropods (Pteropoda and Heteropoda) from six ocean regions based on DNA barcode analysis. Deep Sea Res Part Top Stud Oceanogr 57:2199–2210. https://doi.org/10.1016/j.dsr2.2010.09.022
Kimura M (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. Journal of Molecular Evolution 16:111–120
Kuma K, Sasayama R, Hioki N, Morita Y, Isoda Y, Hirawake T, Imai K, Aramaki T, Nakamura T, Nishioka J, Ebuchi N (2014) Chemical evidence for the origin of the cold water belt along the northeastern coast of Hokkaido. J Oceanogr 70:377–387
Kumar S, Stecher G, Tamura K (2016) MEGA7: Molecular Evolutionary Genetics Analysis version 7.0 for bigger datasets. Molecular Biology and Evolution 33:1870–1874
Kunihiro Y (1995) Behaviour and fisher of Kichiji rock fish, in Okhotsk Sea No 1. Hokusuishi Latter 28:2–8
Lalli CM, Conover RJ (1976) Microstructure of the veliger shells of gymnosomatous pteropods (Gastropoda: Opisthobranchia). Veliger 18:237–240
Lalli CM, Gilmer RW (1989) Pelagic snails. The biology of holoplanktonic gastropod mollusks. Stanford University Press, Stanford
Lalli CM, Wells FE (1978) Reproduction in the genus Limacina (Opisthobranchia: Thecosomata). J Zool 186:95–108
Martens F (1675) Spitzbergische Oder Gröenlandische Reise Beschreibung Gethan im Jahr 1671. Schultze, Hamburg
Massy AL (1932) Mollusca: Gastropoda Thecosomata and Gymnosomata (Pteropoda). Discovery Repts 3:268–296
Matsuyama M, Aota M, Ogasawara I, Matsuyama S (1999) Seasonal variations of soya current. Oceanogr Jpn 8:333–338
McGowan JA (1963) Geographical variation in Limacina helicina in the North Pacific. In: Harding JP & Tebble N (eds.) Speciation in the Sea. Systematics Association, London, Publication No. 3, pp 109–128
MClintock JB, Janssen J (1990) Pteropod abduction as a chemical defence in a pelagic Antarctic amphipod. Nature 346:462–464. https://doi.org/10.1038/346462a0
Mileikovsky SA (1970) Breeding and larval distribution of the pteropod Clione limacina in the North Atlantic, Subarctic and North Pacific Oceans. Mar Biol 6:317–334
Morton JE (1958) Observations on the gymnosomatous pteropod Clione limacina (Phipps). J Mar Biol Assoc UK 37:287–297. https://doi.org/10.1017/S002531540002368
Ohshima KI, Wakatsuchi M, Fukamachi Y, Mizuta G (2002) Near-surface circulation and tidal currents of the Okhotsk Sea observed with satellite-tracked drifters. J Geophys Res 107:3195. https://doi.org/10.1029/2001JC001005
Phipps CJ (1774) A voyage towards the North Pole undertaken by HM Command 1773. London
Richter G, Seapy RR (1999) Heteropoda. In: South Atlantic zooplankton, vol. 1 (D. Boltovskoy, ed.), Backhuys, Leiden, pp. 621–647
Ruth HP, Patrick JH (1998) Oceanography of the sea of Okhotsk and the Japan/East Sea. In: The sea, Vol. 11 (RR Allan and HB Kenneth, ed.), pp. 429–481. Harvard University Press, Cambridge, MS.
Smith EA (1902) Mollusca In: Report on the collections of natural history made in Antarctic regions during the voyage of the "Southern Cross" (I. Franklin, ed.), British Museum (Natural History), London, pp. 201–213, pls. 24–25
Sromek L, Lasota R, Szymelfenig M, Wolowicz M (2015) Genetic evidence for the existence of two species of the “bipolar” pelagic mollusk Clione limacinae. Am Malacol Bull 33:118–120
Suprenand PM, Jones DL, Torres JJ (2015) Distribution of gymnosomatous pteropods in western Antarctic Peninsula shelf waters: influences of Southern Ocean water masses. Polar Rec 51:58–71. https://doi.org/10.1017/S003224741300065X
Suzuki A, Miyano Y, Mawatari K (2005) Biological features of Clione limacina Phipps (Gymnosomata: Clionidae) collected in Abashiri, Hokkaido. Newsl Malacol Soc Jpn 36:12–17
Takizawa J (1982) Characteristics of the soya warm current in the Okhotsk Sea. J Oceanogr Soc Jpn 38:281–292. https://doi.org/10.1007/BF02114532
Van Der Spoel S (1976) Pseudothecosomata, Gymnosomata and Heteropoda (Gastropoda). Bohn, Scheltema, and Holkema, Utrecht
Van Der Spoel S, Dadon JR (1999) Pteropoda. In: South Atlantic zooplankton (D. Boltovskoy, ed.), Backhuys, Leiden, pp. 649–706
Wanger N (1885) Die Wirbellosen des Weissen Meeres. Vol. 1. Zoologische Forschungen an der Küste des Solowetzkischen Meerbusens in den Sommermonaten der Jahre 1877, 1878, 1879 und 1882. W. Engelmann, Leipzig
Wrobel D, Mills C (1998) Pacific coast pelagic invertebrates: a guide to the common gelatinous animals. Sea Challengers, Monterey Bay Aquarium, Monterey, CA
Yamazaki T, Kuwahara T (2017) A new species of Clione distinguished from sympatric C. limacina (Gastropoda: Gymnosomata) in the southern Okhotsk Sea, Japan, with remarks on the taxonomy of the genus. J Molluscan Stud 83:19–26. https://doi.org/10.1093/mollus/eyw032
Acknowledgements
This work was supported by research grants to the Uminomanabi Museum Support from the Museum of Maritime Science (the Nippon Foundation), and National Institute of Polar Research (NIPR) through Project Research no. 29-39.
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Yamazaki, T., Kuwahara, T. & Takahashi, K.T. Genetic Differences in Spatially and Temporally Isolated Populations: Winter and Spring Populations of Pelagic Mollusk Clione (Mollusk: Gymnosomata), Southern Okhotsk Sea, Japan. Thalassas 34, 447–458 (2018). https://doi.org/10.1007/s41208-018-0092-z
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DOI: https://doi.org/10.1007/s41208-018-0092-z