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Systematics of North Pacific Sand Lances of the Genus Ammodytes Based on Molecular and Morphological Evidence, with the Descrip

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Systematics of North Pacific Sand Lances of the Genus Ammodytes Based on Molecular and Morphological Evidence, with the Descrip 12 9 Abstract—The systematic status Systematics of North Pacific sand lances of of North Pacific sand lances (ge- nus Ammodytes) was assessed from the genus Ammodytes based on molecular and mitochondrial DNA (cytochrome oxidase c subunit 1) sequence data morphological evidence, with the description of and morphological data to identify a new species from Japan the number of species in the North Pacific Ocean and its fringing seas. Although only 2 species, Ammodytes James W. Orr (contact author)1 hexapterus and A. personatus, have Sharon Wildes2 been considered valid in the region, Yoshiaki Kai3 haplotype networks and trees con- structed with maximum parsimony Nate Raring1 and genetic distance (neighbor- T. Nakabo4 joining) methods revealed 4 highly Oleg Katugin5 divergent monophyletic clades that 2 clearly represent 4 species of Ammo- Jeff Guyon dytes in the North Pacific region. On the basis of our material and com- Email address for contact author: [email protected] parisons with sequence data report- ed in online databases, A. personatus 1 Resource Assessment and Conservation 3 Maizuru Fisheries Research Station is found throughout the eastern Engineering Division Field Science Education and Research Center North Pacific Ocean, Gulf of Alaska, Alaska Fisheries Science Center Kyoto University Aleutian Islands, and the eastern National Marine Fisheries Service, NOAA Nagahama, Maizuru Bering Sea where it co-occurs with 7600 Sand Point Way NE Kyoto 625-0086, Japan a northwestern Arctic species, A. Seattle, Washington 98115-6349 4 The Kyoto University Museum hexapterus, that is found through- 2 Auke Bay Laboratories Kyoto University out the North American Arctic from Alaska Fisheries Science Center Yoshida, Sakyo Hudson Bay, Canada, in the east, National Marine Fisheries Service, NOAA Kyoto 606-8501, Japan through the Beaufort and Chukchi 17109 Point Lena Loop Road 5 seas, into the northern and western Pacific Research Institute of Juneau, Alaska 99801-8344 Bering Sea, and to the southern Sea Fisheries and Oceanography (TINRO-Center) of Okhotsk in the Soya Strait off 4 Shevchenko Alley Hokkaido, Japan. Two other species Vladivostok, Primorsky Kray, Russia, 690950 reside in waters around Japan: A. japonicus throughout the Sea of Ja- pan and the Seto Inland Sea and a new species in the Sea of Japan and Sand lances of the genus Ammodytes their tremendous importance in eco- the North Pacific Ocean off north- ern Honshu. We designate neotypes (family Ammodytidae) are small systems and as targets in fisheries for A. hexapterus and A. personatus silvery fishes that inhabit marine off Japan (Hamada, 1985; Han et al., because of the absence of type mate- and adjacent brackish waters of the 2012) and in the North Sea (Sher- rial and the close similarity of these Northern Hemisphere. They reside man et al., 1981; Furness, 2002), lit- 2 species. Ammodytes aleutensis is a primarily over sandy substrates, tle is known about their distribution junior synonym of A. japonicus, and where they are able to quickly bury or life history. A. alascanus is a junior synonym of themselves to avoid predators, but The family Ammodytidae com- A. personatus. are found also over bedrock, eelgrass, prises about 31 species in 7 gen- Manuscript submitted 6 February 2014. and kelp. Species of Ammodytes are era and 2 subfamilies found in the Manuscript accepted 30 January 2015. cornerstone prey items for more Arctic, Atlantic, Indian, and Pacific Fish. Bull. 113:129–156 (2015). than 100 species of marine mam- oceans (Nelson, 2006; Randall and Electronic publication date: 10 March 2015. mals, birds, and other fishes in the Heemstra, 2008; Shibukawa and Ida, doi: 10.7755/FB.113.2.3 region of the North Pacific Ocean 2013; Randall and Ida, 2014). Placed http://zoobank.org/References/29FEAF57- (Field, 1988; Willson et al.1). Despite within the subfamily Ammodytinae, 8178-45DB-8A23-76BE33BB2B0D 1 Willson, M. F., R. H. Armstrong, M. D. Willson, R. H. Armstrong, and J. F. Piatt, The views and opinions expressed or Robards, and J. F. Piatt. 1999. Sand eds.), p. 17–44. Research Paper PNW- implied in this article are those of the lance as cornerstone prey for predator RP-521. U.S. Department of Agricul- author (or authors) and do not necessarily populations. In Sand lance: a review of ture, Forest Service, Pacific Northwest reflect the position of the National biology and predator relations and anno- Research Station. Portland OR. [http:// Marine Fisheries Service, NOAA. tated bibliography (M. D. Robards, M. F. www.fs.fed.us/pnw/pubs/rp_521a.pdf] 13 0 Fishery Bulletin 113(2) which also includes the genera Gymnammodytes and ponicus of Duncker and Mohr (1939). They recognized Hyperoplus, Ammodytes is diagnosed by the presence A. aleutensis to be widely distributed from Unalaska of scales deeply embedded in dermal plicae below the in the eastern Aleutian Islands to Hokkaido in north- lateral line, a highly protrusible upper jaw (Pietsch, ern Japan and Nagasaki in southern Japan and A. 1984), and non-expanded neural and haemal spines japonicus to be only from the type locality of Otaru on the caudal vertebrae (Ida et al., 1994). Six species (=“Otaka”), Hokkaido, that also is included among currently are recognized in the genus Ammodytes: 2 in the type localities of A. aleutensis. Duncker and Mohr the eastern North Atlantic Ocean (A. tobianus Linnae- (1939) distinguished A. japonicus from A. aleutensis us, 1758, and A. marinus Raitt, 1934), 2 in the west- on the basis of its fewer dorsal-fin rays and higher ern North Atlantic Ocean (A. americanus DeKay, 1842, number of dermal plicae. In addition, they observed and A. dubius Reinhardt, 1837), and 2 in the North that, in their specimens of A. japonicus, the origin Pacific Ocean A.( hexapterus Pallas, 1814, and A. per- of the dorsal fin was farther posterior (posterior half sonatus Girard, 1856). All are very similar morpholog- versus middle of pectoral fin) and the ventrolateral ically, having an elongate body up to 280 mm in total fold was shorter (extending to mid-anal fin versus the length, scales aligned in dermal plicae for the length posterior third of the anal fin and beyond). Although of the body, long dorsal and anal fins, and no pelvic Andriashev (1954) noted the presence of significant fins. Species generally are distinguished by meristic variation among more southern forms and the need characters and relative body depth. We focus primar- for additional taxonomic work, he recognized 2 species ily on the sand lances of the North Pacific Ocean and of Ammodytes across northern seas: A. tobianus in the adjacent seas for the purpose of clarifying their sys- Atlantic Ocean and A. hexapterus from the Barents tematic status. Sea to the Baltic Sea. Within A. hexapterus, he recog- The first species recognized in this genus was col- nized the subspecies A. hexapterus marinus from the lected from Sweden to the Mediterranean and de- Barents Sea to the Baltic Sea and A. hexapterus hexa- scribed by Linnaeus (1758) as A. tobianus. Of 2 other pterus in the North Pacific region. names published in this genus in the early 1800s, A. The number of species of Ammodytes in waters alliciens Lacepède, 1800, was designated an unneed- off Japan has been in question for the last century. ed replacement name for A. tobianus, and A. cicerelus Ohshima (1950) examined the numbers of vertebrae Rafinesque, 1810, was allocated toGymnammodytes as in Ammodytes from 7 locations around Japan—in a valid species (Eschmeyer, 2013). In the North Pacific the Seto Inland Sea, southern and northern Japan region, the first species described was A. hexapterus, on the Pacific Ocean side, the northern tip of Hon- from material collected or observed from off the Ka- shu, and the northcentral Kuril Islands—and found mchatka Peninsula and Kuril Islands in Russia, the differences in vertebral numbers. Lindberg and Kra- islands “between Asia and North America,” and the syukova (1975) noted confusion in use of the names coast of North America (Pallas, 1814; Lindberg, 1937). A. hexapterus and A. personatus, as well as the un- Pallas (1814) compared it with the Atlantic species certain status of A. aleutensis and A. japonicus, and A. tobianus as described by Artedi (1738; Walbaum proposed the synonymy of all northern Ammodytes 1792), noting that A. hexapterus had more numerous within A. hexapterus, including those species in the vertebrae. western North Pacific region around Japan. Kitaguchi In his work on fishes collected during the Pacific (1979) also examined meristic data and found that 2 railroad surveys of the early 1800s, Girard (1856) de- species, which he identified asA. personatus and A. scribed A. personatus from Cape Flattery, Washing- hexapterus, occurred together in the area around Wak- ton. In 1873, Cope described A. alascanus from Sitka, kanai in the Soya Strait off northeastern Hokkaido. In Alaska, without comparing it with previously de- their study of the life history characteristics of Ammo- scribed species. Jordan (1906) referred all Ammodytes dytes, Hashimoto and Kawasaki (1981) concluded that of the North Pacific region to Ammodytes personatus, 2 populations were included in “A. personatus” col- including populations from Alaska to Monterey, Cali- lected from the Pacific Ocean coast of northern Japan fornia, and from Siberia to the Inland Sea of Japan. (Tohoku district) on the basis of meristic and allozyme He made no comments on A. hexapterus and was un- analyses. Later, Hashimoto (1984) expanded his study certain about the status of A. alascanus, as well as of of meristics within Ammodytes, examining material the northernmost populations of Ammodytes, suggest- from several localities around Japan, and concluded ing that they may be referable to a circumboreal A. that 3 genetically independent but geographically tobianus. Lindberg (1937) recognized differences be- overlapping subspecies were likely present around tween Ammodytes off the coast of Japan and species Japan.
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