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ISSN 10630740, Russian Journal of Marine Biology, 2014, Vol. 40, No. 6, pp. 447–454. © Pleiades Publishing, Ltd., 2014. Original Russian Text © S.V. Turanov, Yu.Ph. Kartavtsev, 2014, published in Biologiya Morya.

GENETICS, ICHTHYOLOGY

The Taxonomic Composition and Distribution of Sand Lances from the Genus Ammodytes (Perciformes: Ammodytidae) in the North Pacific S. V. Turanova, * and Yu. Ph. Kartavtseva, b a

Zhirmunsky Institute of Marine Biology, Far Eastern Branch, Russian Academy of Sciences, ul. Pal’chevskogo 17, Vladivostok, 690041 Russia bFar Eastern Federal University, ul. Sukhanova 8, Vladivostok, 690090 Russia *email: [email protected] Received September 19, 2013

Abstract—An analysis of the variability of 34 sequences of the 5'region of the Co1 mitochondrial gene fish of the genus Ammodytes has been performed taking the precise geographic location into account. Among them, seven sequences are original data and 27 were retrieved from the GenBank. Two hypotheses on the tax onomic composition of sand lances of North Pacific have been proposed. The first is preferable to the authors; it assumes that there are four separate species, while the second considers the presence of a complex circum polar species with four major local geographic races. Both hypotheses suppose a clear delineation and deep divergence of coldwater sand lances from warmerwater southern ones. These data and the analysis of the history of the study of the taxonomy of fareastern sand lances allowed us to consider that the use of the spe cies name A. personatus is inappropriate for sand lances from the Yellow Sea and the southern part of the Sea of Japan, as well as for some representatives of the Bering sea and the Sea of Okhotsk and adjacent waters, which form a separate monophyletic group with the current name Ammodytes hexapterus. Keywords: Ammodytes, sand lances, taxonomic structure, distribution, mitochondrial gene Co1, cryptic biodiversity DOI: 10.1134/S1063074014060212

INTRODUCTION Sand lances of the genus Ammodytes (Perciformes: Ammodytidae) inhabit temperate zone of the Pacific and Atlantic Oceans, as well as Arctic waters [21, 30, 40]. The genus, according to modern views, includes six species [16]. One striking ecological feature of sand lances is attachment to the certain type of ground (coarse sand without silt or pebbles), in which they are buried to protect themselves from predators or to rest [5, 40]. Despite their specific protection mode, sand lances still remain an important component in the diet of coastal fish fauna of the entire North Hemisphere [42] and greatly determine the population of seabirds, fishes and mammals [5, 10, 11, 40]. In the Far Eastern seas of Russia the existence of one species of sand lance, Ammodytes hexapterus Pal las, 1814, is generally recognized, whose southern boundary area extends from the coastal waters of Hok kaido Island in the Northwest to Balboa Island (South Carolina) in the Northeast Pacific; the northern boundary extends in the Arctic waters of the East Sibe rian Sea in the West to the Hudson Bay in the East [3, 7, 9, 30, 36].

In recent papers on the assessment of fish biodiver sity from the Arctics [31] and Far Eastern seas of Rus sia [45], the presence of the species Ammodytes per sonatus Girard, 1856, which was described from the Northeast Pacific off the Cape Flattery [17] and is genetically differentiable from A. hexapterus (more than 3% of the genetic distance, K2P), was suggested to inhabit the Gulf of Alaska (Semidi Islands) and in the Sea of Okhotsk. However, A. personatus, according to modern concepts, is endemic to the Yellow Sea and the southern part of the Sea of Japan [19]. This contra diction was recorded earlier [21]; to date there have been no attempts to resolve it. The study of Soldatov and Lindberg [8] was one of the first major syntheses on the taxonomic structure of fishes of the Far Eastern seas. Recognizing the exist ence in the North Pacific only the species, A. per sonatus, the authors did not exclude its possible synon ymy with Ammodytes tobianus Linnaeus, 1758, whose area extends from the Baltic Sea to the western part of Mediterranean. In this paper, the number of oblique lateral skin folds in A. personatus was taken as equal to 153. The authors did not mention the species described by Pallas, A. hexapterus, since it was synon ymized by Gunther to Ammodytes lanceolatus in 1862.

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80° N Arctic ocean Chukchi sea

70° N

60° N

Sea of Okhotsk

Bering sea

50° N Pacific ocean 40° N

30° N 120° E

Ammodytes personatus A. cf. personatus A. hexapterus A. dubius A. americanus

Sea of Japan

150° E

180° E

150° W

120° W

Atlantic ocean 90° W

60° W

Fig. 1. Sample location of sand lances that were used in the analysis.

Later, Lindberg, in the taxonomic review of Ammodytes sand lances [2] reported the existence of three species in waters of the North Hemisphere: A. personatus, A. tobianus, and A. hexapterus, which was validated by the author with a circumpolar distri bution of the latter. A. hexapterus was opposed to the other two species in the number of vertebrae (70 instead of 63). A specimen caught near Nagasaki (South of Japan) was treated as A. personatus. Lind berg did not considered the large number (160) of lat eral folds of this specimen as a reliable diagnostic char acter when taking Cope’s data [13] into account on A. alascanus of the Northeast Pacific (182 folds), which later became synonymous to A. hexapterus. Based on this, we can assume that Lindberg’s study [2] was the starting point for the inappropriate use of the species name A. personatus pertaining to sand lances that inhabit the southern part of the Sea of Japan. Later, Lindberg and Krasyukova [3] considered additional data [39] and recognized the existence of only one species, A. hexapterus, in the North Pacific with a wide range of variation in the number of verte brae (from 61 to 73) and again determined its possible circumpolar distribution. This work was not men tioned in the latest review on the taxonomy of fishes of Japan [19], but another [2] was cited. The basis for the compilation of data on the fauna of Japanese sand lances [19] was obviously Kitaguchi’s paper [27], who recorded the existence of two species in the waters of Japan, A. hexapterus and A. personatus; their numbers of vertebrae were 68 and 65–66, respectively (see the summary in [40]). This suggests that the author was not familiar with Lindberg and Krasyukova’s paper

[3]; as well, he possibly is a proponent of the hypothe sis of the amphypacific distribution of A. personatus. Available nomenclature contradictions, as well as new information that implies the presence of cryptic biodiversity of sand lances in the North Pacific, enabled the authors of this work to consider the history of the study of sand lances in the Far East in more detail, and, with the use of molecular data, to deter mine the limits of distribution of genetically separate lineagess of this group. Moleculargenetics techniques have proven themselves in taxonomic studies thanks to a new area, viz., socalled DNA barcoding, which is a comprehensive approach to the species identification of organisms using standard molecular markers of mitochondrial DNA (mDNA) and the maintenance of biological collections [20]. In the study of the taxo nomic structure of the North Pacific sand lances we used personal and literature data that were accumu lated during the analysis of the biological diversity of marine fishes in the Northern Hemisphere, using the nucleotide sequences of cytochrome oxidase c subunit I, Co1 mDNA, or DNA barcodes. This study is intended to clarify the number of genetically distinguishable species of sand lances that inhabit the North Pacific and determine their areas, as well as the validity of the specific name A. personatus as it pertains to the sand lances of the Yellow Sea and the southern part of the Sea of Japan. MATERIALS AND METHODS We analyzed the nucleotide sequences of the 5' region of the Co1 gene (hereinafter, the sequences)

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THE TAXONOMIC COMPOSITION AND DISTRIBUTION OF SAND LANCES

of sand lances of the Ammodytes genus that were sam pled in the Bering (2008, 2 ind.) and Okhotsk Seas (2011, five ind.) (Fig. 1). Individuals that show diver gence values less than 2% of the K2P distances [26] relative to A. cf. personatus from Mecklenburg [30] were identified as A. cf. personatus. The rest of the sand lances in our sample (the divergence relative to A. cf. personatus was more than 3% on the K2P scale) were attributed to A. hexapterus. Furthermore, additional Co1 gene sequences of the Atlantic sand lances, Ammodytes americanus DeKay, 1842 and A. dubius Reinhardt, 1837 were retrieved from the GenBank, NCBI (http://www.ncbi.nlm.nih.gov/). The species Siganus vulpinus (Schlegel et Müller, 1845), and Scombrops gilberti (Jordan et Snyder, 1901) were used (table) as external taxa for molecular–phylogenetic reconstructions. Each captured specimen was placed in the fish col lection of the Zhirmunsky Institute of Marine Biology, Far Eastern Brach, Russian Academy of Sciences (IMB FEB RAS) (curator A.A. Balanov), was individ ually photographed, and a small piece of skeletal mus cle tissue (fixed in 95% ethanol) was taken. Isolation of total DNA from muscle tissue was carried out by the standard procedure [4], with phenol exclusion at the deproteinization stage. Amplification of the 5' region of the Co1 gene, which consisted of approximately 650 base pairs (bp) for each sample, was carried out using a cocktail of universal primers COI3 [22]. A reaction mixture in a 10 µL volume contained 6.4 µL of deionized H2O, 0.5 µL of 10 µM deoxynucleotide triphosphate mix (dNTPs), 1 µL of 10× PCR buffer (Evrogen), 0.4 µL of 50 µM MgCl2, 10 µM 0.6 µL primer cocktail mix, 0.1 µL Taq polymerase (Evro gen), and 1 µL of the total DNA solution. The poly merase chain reaction (PCR) protocol included 2 min of preliminary heating at 94°C followed by 35 cycles according the following pattern: denaturation at 94°C, 30 s, hybridization at 52°C, 40 s, elongation at 72°C— 1 min; and final elongation was carried for 10 min. To check the results of PCR, the amplicons were run in a 1% agarose gel (Helicon). The amplified products were used for cycle sequencing with a BigDye Termi nator v. 3.1 Cycle Sequencing Kit (Applied Biosys tems) and further forward and reverse sequencing using an ABI Prism DNA sequencer in the IMB FEB RAS. The consensus sequences based on the obtained chromatograms were built applying the ChromasPro program (http://www.technelysium.com.au/chromas. html). The sets of sequences were aligned in the MEGA v. 5 software environment [44] using the MUSCLE algorithm [15]. During the alignment, the Lycodes palearis sequence (GenBank Accession no. FJ164794) [43] was used to verify the correctness of the reading frame of the Co1 gene. Sequences with their chromatograms and photographs of sample fish, as well as other biological data, were placed in the BOLD dataset [38] at the page of our “FERU” project, as well as in GenBank, NCBI under their RUSSIAN JOURNAL OF MARINE BIOLOGY

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respective numbers (table). Analysis and visualization of the results of the variability of nucleotide sequences variation were carried out using MEGA v. 5 software. The phylogenetic trees were constructed based on the maximum likelihood algorithms (ML) and neighbor joining (NJ) [32] using the Kimura twoparameter model (K2P) [26], as well as the method of maximum parsimony (MP). The genetic distances between sequences, which were calculated by the K2P model, were also used in the argumentation. Assessment of the stability of the tree topology was carried out using 1000 replicates of the bootstrap test. Beyond the vari ation of Co1 gene sequences, the following morpho logical characters were recorded for sand lances in our sample: vert., the total number of vertebrae; A, the number of rays in the anal fin; D, the number of rays in the dorsal fin; and pl. str., the number of lateral oblique skin folds. RESULTS AND DISCUSSION The gene tree that reveals the phylogenetic rela tionships of Ammodytes sand lances (Fig. 2) shows two monophyletic macroclusters, where the basal group consists of Siganus vulpinus and Scombrops gilberti. Coldwater sand lances, including those from the southeast of the Sea of Japan (NFRDI2005052411 and NFRDI2005052430), which is under influence of branches of the cold Oyashio Current, form a poly tomic macrocluster. The sequences A. personatus formed two clusters belonging to different areas of the Sea of Japan and the Yellow Sea. A. americanus and A. dubius from the Northeast Atlantic form a single cluster. In addition, A. hexapterus and A. cf. personatus isolated into two paraphyletic clusters. The first cluster combined sequences of individuals from areas of the Okhotsk and Bering Seas, as well as sand lances in the Gulf of Alaska (Semidi Islands) and Puget Sound. The second cluster does contain the sequences of sand lances collected in the Chukchi, Bering, and Okhotsk seas and one sequence of an individual that was caught at Cape Söya, Soya, Hokkaido Isl. The distribution of values of genetic distances within and between phy letic lineages in general is consistent with the tree topology. Thus, the distance between the sequences within separate clusters did not exceed 1.51% (mean 0.46 ± 0.034%); the minimum distance between the sequences from different clusters was 3.25% (mean 8.06 ± 0.22%). The distance between the sand lances from the Yellow Sea and the southern part of the Sea of Japan, where the effect of the warm Kuroshio Current was manifested, and the northern representatives var ied from 6.55 to 8.84%. The maximum difference between coldwater sand lances reached 6.32%. The main diagnostic characters of sand lances in our sam ple were: A 2830/2930, D 5561/5863, vert. 66 70/6972, and pl. str. 142160/140150. The slash sep arates characters for individuals with identifiers: No. 6

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Data on samples of Ammodytes sand lances whose sequences were considered in the study Sampling area

Reference

Species

1

06566

KC015153

The Atlantic, Labrador

McCusker et al., 2013

2

Ammodytes americanus A. americanus

06140GeoB1b7

KC015156

McCusker et al., 2013

3

Ammodytes dubius

07389

KC015161

4

A. dubius

06195

KC015160

5

Okh 1

KF019327

6 7 8 9 10 11 12

Ammodytes hexapterus A. hexapterus A. hexapterus A. hexapterus A. hexapterus A. hexapterus A. hexapterus A. hexapterus

YPK308 YPK309 RUSALCA09142 RUSALCA09143 PKU1512 PKU1513 WTU:UW116054

HQ704752 HQ704753 HM421764 HM421765 FJ666920 FJ666921 JQ353965

13

A. hexapterus

WTU:UW116055

JQ353966

14 15

A. hexapterus Ammodytes personatus A. personatus A. personatus A. personatus A. personatus A. personatus A. personatus A. personatus

Complete genome KC422441 NFRDI2005052430 FJ666916

The Atlantic, New Scot land area The Atlantic, Flemish Cap Bank The Atlantic, New Scot land area The Pacific, Sea of Okhotsk The Pacific, Bering Sea The Pacific, Bering Sea The Pacific, Chukchi Sea The Pacific, Chukchi Sea The Pacific, Bering Sea The Pacific, Bering Sea The Pacific, Pudget Sound The Pacific, Pudget Sound The Pacific, Soya Cape The Pacific, Sea of Japan

NFRDI2005052411 PKU1476 PKU1474 NFRDI200703262 PKU1475 NFRDI200504276 No name

FJ666915 FJ666905 FJ666903 FJ666911 FJ666904 FJ666906 HQ711864

F00099 F00101 F00133 F00132 Okh 2

JQ738549 JQ738551 JQ738429 JQ738428 KF019325

28

A. personatus A. personatus A. personatus A. personatus Ammodytes cf. personatus A. cf. personatus

Okh 3

KF019324

29

A. cf. personatus

Okh 4

KF019323

30

A. cf. personatus

Okh 5

KF019326

31 32 33

A. cf. personatus A. cf. personatus Scombrops gilberti

SMMOCI200719 SMMOCI200769 KURM8

HQ712264 HQ712265 JF952851

34

Siganus vulpinus

BIOUG HLC10739

FJ584118

16 17 18 19 20 21 22 23 24 25 26 27

Vaucher number

NCBI GenBank accession no.

No

The Pacific, Sea of Japan The Pacific, Yellow Sea The Pacific, Yellow Sea The Pacific, Sea of Japan The Pacific, Yellow Sea The Pacific, Yellow Sea The Pacific, China Waters The Pacific, Yellow Sea The Pacific, Yellow Sea The Pacific, Yellow Sea The Pacific, Yellow Sea The Pacific, Sea of Okhotsk The Pacific, Sea of Okhotsk The Pacific, Sea of Okhotsk The Pacific, Sea of Okhotsk The Pacific, Semidi Isls The Pacific, Semidi Isls The Pacific, Honshu Isl., Sizuoka The Pacific, Manila Bay


McCusker et al., 2013 McCusker et al., 2013 Turanov et al., 2014 Turanov et al., 2014 Turanov et al., 2014 Mecklenburg et al., 2011 Mecklenburg et al., 2011 Kim et al., 2010 Kim et al., 2010 GenBank, NCBI GenBank, NCBI Li et al., 2013 Kim et al., 2010 Kim et al., 2010 Kim et al., 2010 Kim et al., 2010 Kim et al., 2010 Kim et al., 2010 Kim et al., 2010 GenBank, NCBI GenBank, NCBI GenBank, NCBI GenBank, NCBI GenBank, NCBI Turanov et al., 2014 Turanov et al., 2014 Turanov et al., 2014 Turanov et al., 2014 Mecklenburg et al., 2011 Mecklenburg et al., 2011 GenBank, NCBI Steinke et al., 2009

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72/74/76 95/91/99

60/79/62

62/68/⎯

95/99/99

99/99/100

99/99/100 85/86/86 99/99/100 55/55/52

100/−/100

451

Ammodytes hexapterus voucher PKU1512 Ammodytes cf. personatus Okh 3 Ammodytes cf. personatus DS2011 voucher SMMOCI200719 Ammodytes cf. personatus Okh 2 Sea of Okhotsk, Ammodytes cf. personatus DS2011 voucher SMMOCI200769 Bering sea, Ammodytes cf. personatus Okh 4 Semidi islands, Ammodytes hexapterus voucher WTU:UW 116055 Pudget Sound Ammodytes cf. personatus Okh 5 Ammodytes hexapterus voucher PKU1513 Ammodytes hexapterus voucher WTU:UW 116054 Ammodytes hexapterus mitochondrion complete genome Chukchi sea, Ammodytes hexapterus YPK309 Bering sea, Ammodytes hexapterus voucher RUSALCA09142 Sea of Okhotsk, Ammodytes hexapterus Okh 1 Soya Cape Ammodytes hexapterus voucher RUSALCA09143 (Hokkaido) Ammodytes hexapterus YPK308 Ammodytes ammericanus voucher 06566 Ammodytes dubius voucher 07389 Northwest Atlantic Ammodytes ammericanus voucher 06140GeoB1b7 Ocean Ammodytes dubius voucher 06195 Ammodytes personatus voucher NFRDI2005052411 Sea of Japan Ammodytes personatus voucher NFRDI2005052430 Ammodytes personatus voucher PKU1474 Ammodytes personatus HQ711864 Ammodytes personatus voucher PKU1476 Ammodytes personatus voucher NFRDI200504276 Yellow Sea and Ammodytes personatus voucher PKU1475 Inner Sea of Japan Ammodytes personatus isolate F00132 Ammodytes personatus isolate F00101 Ammodytes personatus isolate F00099 Ammodytes personatus isolate F00133 Ammodytes personatus voucher NFRDI200703262 Siganus vulpinus voucher BIOUGCAN:HLC10739 Outgroup Siganus vulpinus voucher KURM8

Fig. 2. A phylogenetic tree displaying the molecular phylogenetic relationships of the Ammodytes species based on nucleotide sequences of the Co1 gene. In the nodes, assessments for the stability of the topology, which are expressed as a percentage (boot strap test, 1000 replicates; ML/MP/NJ), are recorded. The explanation of the abbreviations ML, MP and NJ is given in the Mate rials and Methods.

Okh 2, Okh 3, Okh 4, and Okh 5 are the first values and Okh 1, YPK308, and YPK309 are the second values. According to published data on the variation of the 5' region of the Co1 mitochondrial gene (DNA bar code) in birds and fishes, sequences that differ by at least 2% are more likely to belong to different species [46]. Based on this, each separate cluster on our phy logenetic tree can be considered as a separate species. This is the basic concept on which we relied. Thus, the sand lances are thought to have four taxa of species rank in the North Pacific and one in the Atlantic. However, given the lack of clear diagnostics of mor phological characters and the circumpolar distribu tion of the Ammodytes, an alternative hypothesis RUSSIAN JOURNAL OF MARINE BIOLOGY

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should be proposed, according to which the waters of the Northeast Atlantic, the East Siberian and Chukchi seas, as well as the North Pacific, excepting areas under the influence of the warm waters of the Kuro shio Current, are inhabited by one amphiboreal spe cies with a complex genetic structure. This species may include a number of local geographical races (subspe cies), which are separated genetically. This hypothesis is theoretically consistent with the views of Lindberg and Krasyukova [3], who believed that the North Pacific is inhabited by a single species, A. hexapterus. As an example of such a species genetic structure, the capelin Mallotus villosus (Müller, 1776) may be con sidered. Despite the fact that independent genetic data No. 6

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revealed at least four species in the species composi tion [6, 12, 14, 29, 37] and taking the material from hardtoreach areas into account, even for five highly divergent and geographically separated lineages [31], taxonomic treatment above the subspecies level based on morphology characters is considered unreasonable. The capelin, which is distributed in the pelagic zone at depths to 300 m and deeper, comes to the coast only to spawn. In contrast to this species, mature sand lances are rather conservative in selecting their habitat and have not been recorded at depths deeper than 100 m. In this case, the “centers” of reproduction with unsteady areas of dispersal, which may disappear within a few years under unfavorable conditions, are considered as the main source of sandlance diversity [1, 5]. These centers are characterized by specific grounds (see Introduction), which in the Far Eastern seas are often connected with areas of intense water mixing at depths from 10 to 70–80 m that function as a barrier to gene flows. The clearly defined geographi cal location of individual clusters in the gene tree also supports this idea. In our opinion, polytomy in the macrocluster of coldwater sand lances implies their onetime origin and subsequent dispersal in the North Pacific and North Atlantic. Polyphyletic allocation of taxa within the specified macrocluster once again cor roborates the lack of clearly defined diagnostic char acters, which may cause misidentification of sand lances. It was determined that the two phyletic lines that were isolated in our sand lance sample (Bering and Okhotsk seas) (Fig. 2) are rather poorly supported by the main diagnostic characters. However, the number of oblique lateral skin folds points to their unambigu ous separation from sand lances of the Sea of Japan. Based on the tree topology, we can assume that our sequence from the Sea of Okhotsk (Okh 2, Okh 3, Okh 4, and Okh 5), as well as all the rest that occurred in the corresponding cluster, belong to A. personatus. Thus, the Puget Sound, Salish Sea can be considered as the southeastern edge of the A. personatus area and the coastal waters of the southwestern Kamchatka would be the western one. The range of A. hexapterus covers the Chukchi, Bering, and Okhotsk seas and the Sea of Japan in the North Pacific; its southern bound ary is at the Soya Cape, which is the northern extrem ity of Hokkaido Island (the sequence from: [28]). Two endemic populations other than A. personatus and A. hexapterus are assumed to inhabit the Yellow Sea and the southern part of the Sea of Japan [18]. In the study on the phylogeography of sand lances of the Sea of Japan and the Yellow Sea, which the authors attributed to A. personatus, based on the variation of the mitochondrial control region, clear separation into the northern and southern populations was revealed. The northern boundary of the gene pool of the population from the east coast of the Honshu Isl. is confined by the temperature gradient that resulted from the collision of the Kuroshio and Oyashio Cur

rents and at the west coast it does not move to the south of the northern extremity of the Honshu Island, which is under the influence of a branch of the Tsushima Current. The gene pool of the southern population from the area of secondary contact with the northern form widely juts out into the latter, moving further north along Hokkaido Island [18]. Unfortunately, the authors left the taxonomic status of these populations unclear. However, taking the allocation on the gene sequence of Lee et al. [28] in their gene tree into account, we can assume that the northern population is nothing more than representatives of A. hexapterus from the southern end of its area, which introgress with the southern form in the zone of the secondary contact but do not propagate into the warm waters of the Kuroshio Current. Some authors have tentatively distinguished (with no description) at least one taxon of the species rank in the Sea of Japan and the Yellow Sea [34, 35, cit. by 23, 24, 25]. The essence of the argument reduces to the separation of populations of A. personatus without specific indicators of their taxo nomic status. Kim et al. [26], when performing species identification of sand lance larvae in the Northwest Pacific, found that A. personatus inhabits the south of the Sea of Japan. Comparison of the larvae in the Sea of Japan with larvae in the Bristol Bay, Bering Sea revealed their considerable divergence. As a result, the larvae from this bay were attributed to A. hexapterus. Based on the overall data (Fig. 2), we can conclude that in the Bering Sea [25] the larvae of A. personatus, which diverged from the both, A. hexapterus and endemics of the Sea of Japan, were sampled. This is indicated by the genetic proximity of the sequences of the larvae from the Bristol Bay [25] and from the Northeast Pacific. McCusker et al. [29] left the problem of the taxo nomic status of the Atlantic sand lances A. americanus and A. dubius unresolved. The inconsistency of the genetic and morphological descriptors in this case is significant, because, according to the literature, these species can be attributed morphologically; moreover, they form their areas with different distances from the coast [33]. The genetic dissociation of the Atlantic and Pacific sand lances, according to our data, is slight, supporting a recent divergence of their evolutionary lineages. Summing up the study, we give preference to the first of the proposed hypotheses, viz., that the North Pacific is inhabited by four species of sand lance that are welldefined genetically, but poorly recognized by external characters. In this case, both hypotheses, as has been noted, point to the incorrect use of the spe cies name A. personatus in relation to warmwater sand lances of the Yellow Sea and the southern part of the Sea of Japan. Since A. personatus from the Northeast Pacific is a pronouncedly divergent and geographically strictly localized group, the species name A. per sonatus, according to the priority, is saved only for the sand lances in that region. The warmwater species of


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the Sea of Japan require redescription using compre hensive approaches; a reserve in this field already exists [34, 35, cit. by 25, 23, 24, 25]. ACKNOWLEDGMENTS The authors are highly grateful to their colleagues from the Laboratory of Ichthyology, Institute of Marine Biology, Far Eastern Branch, Russian Acad emy of Sciences, Dr. A.A. Balanov, for consultation in the field of applied taxonomy and critical remarks in the preparation of this work, and Dr. P.A. Savelyev, for assistance in obtaining radiographs of sand lances. REFERENCES 1. Velikanov, A.Ya. and Stominok, D.Yu., Occurrence, distribution, and some aspects of the biology of the Pacific sand lance (Ammodytes hexapterus Pallas, 1811) in the Tatar Strait (Sea of Japan), Izv. Tikhookean. NauchnoIssled. Inst. Rybn. Khoz. Okeanogr., 2001, vol. 128, pp. 737–750. 2. Lindberg, G.U., Concerning the taxonomy and distri bution of sand lances of the Ammodytes genus (Pisces), Vestn. Dalnevost. Otd., Akad. Nauk SSSR, 1937, no. 27, pp. 85–93. 3. Lindberg, G.U. and Krasyukova, Z.V., Ryby Yapon skogo morya i sopredel’nykh chastei Ohotskogo i Zheltogo morei (Fishes the Sea of Japan and adjacent areas of the Sea of Okhotsk and Yellow Sea) Leningrad: Nauka, 1975, pt. 4. 4. Maniatis, T., Fritsch, E., and Sambrook, J., Metody geneticheskoi inzhenerii. Molekulyarnoe klonirovanie (Molecular Cloning: a Laboratory Manual), New York: Cold Spring Hrabor Lab., 1982. 5. Mel’nikov, I.V. and Hudya, V.N., The Far East sand lance (Ammodytes hexapterus Pallas) in the Sea of Okhotsk and the western part of the Bering Sea, Izv. Tikhookean. NauchnoIssled. Inst. Rybn. Khoz. Okean ogr., 1998, vol. 124, pp. 344–359. 6. Skurikhina, L.A., Kukhlevsky, A.D., Oleinik, A.G. and Kovpak, N.E., Phylogenetic relationships of smelt fish (Osmeridae) according to the data on variability of cytochrome b, Genetika, 2010, vol. 46, no. 1, pp. 79–91. 7. Sokolovsky, A.S., Dudarev, V.A., Sokolovskaya, T.G., and Solomatov, S.F., Ryby rossiiskikh vod Yaponskogo morya (Fishes of Russian Waters of the Sea of Japan), Vladivostok: Dal’nauka, 2007. 8. Soldatov, V.K. and Lindberg, G.U., Review of fishes of Far East seas, Izv. Tikhookean. NauchnoIssled. Inst. Rybn. Khoz. Okeanogr., 1930, vol. 5. 9. Fedorov V.V., Chereshnev, I.A., Nazarkin, M.V., et al., Katalog morskikh i presnovodnykh ryb severnoi chasti Okhotskogo morya (Catalogue of Marine and Freshwa ter Fishes of the North of the Sea of Okhotsk), Vladi vostok: Dal’nauka, 2003. 10. Chereshnev, I.A., Volobuev, V.V., Khovansky, I.E., and Shestakov, A.V., Pribrezhnye ryby severnoi chasti Okhotskogo morya (Coastal Fishes of the North of the Sea of Okhotsk), Vladivostok: Dal’nauka, 2001. RUSSIAN JOURNAL OF MARINE BIOLOGY

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Translated by L. Dolgov

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