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Article

Walleye Pollock Gadus chalcogrammus, a Species with Continuous Range from the Norwegian Sea to Korea, Japan, and California: New Records from the Siberian Arctic

by
Alexei M. Orlov
1,2,3,4,5,6,*,
Maxim O. Rybakov
7,
Elena V. Vedishcheva
2,
Alexander A. Volkov
8 and
Svetlana Yu. Orlova
8,9
1
Laboratory of Oceanic Ichthyofauna, Shirshov Institute of Oceanology of the Russian Academy of Sciences, 117218 Moscow, Russia
2
Department of Marine Fishes of the Russian Far East, Russian Federal Research Institute of Fisheries and Oceanography, 107140 Moscow, Russia
3
Laboratory of Behaviour of Lower Vertebrates, A.N. Severtsov Institute of Ecology and Evolution of the Russian Academy of Sciences, 119071 Moscow, Russia
4
Department of Ichthyology and Hydrobiology, Tomsk State University, 634050 Tomsk, Russia
5
Department of Ichthyology, Dagestan State University, 367000 Makhachkala, Russia
6
Laboratory of Marine Biology, Caspain Institute of Biological Resourses of Dagestan Federal Research Center of the Russian Academy of Sciences, 367000 Makhachkala, Russia
7
Laboratory of Marine Bioresources, Polar Branch of the Russian Federal Research Institute of Fisheries and Oceanography, 183038 Murmansk, Russia
8
Laboratory of Molecular Genetics, Russian Federal Research Institute of Fisheries and Oceanography, 107140 Moscow, Russia
9
Laboratory of Ecology of Coastal Bottom Communities, Shirshov Institute of Oceanology of the Russian Academy of Sciences, 117218 Moscow, Russia
*
Author to whom correspondence should be addressed.
J. Mar. Sci. Eng. 2021, 9(10), 1141; https://doi.org/10.3390/jmse9101141
Submission received: 3 October 2021 / Accepted: 13 October 2021 / Published: 17 October 2021
(This article belongs to the Special Issue Deepwater Fishes)
Browse Figures
Versions Notes

Abstract

:
The first records of walleye pollock Gadus chalcogrammus Pallas, 1814 in the seas of the Siberian Arctic (the Laptev Sea, the Kara Sea, the southeastern Barents Sea), are documented. Information about the external morphology (morphometric and meristic characters), photos of sagittal otoliths and fish, and data on the sequences of the CO1 mtDNA gene are presented. The results of a comparative analysis indicate that walleye pollock caught in the Siberian Arctic do not differ in principle from North Pacific and North Atlantic individuals. Previous conclusions about the conspecificity of the walleye and Norwegian pollock Theragra finnmarchica are confirmed. New captures of walleye pollock in the Siberian Arctic allow us to formulate a hypothesis about its continuous species’ range from the coasts of Norway in the North Atlantic to the coasts of Korea, Japan, and California in the North Pacific. The few records of walleye pollock in the North Atlantic originate from the North Pacific due to the transport of early pelagic juveniles to the Arctic by currents through the Bering Strait and further active westward migrations of individuals which have switched to the bentho-pelagic mode of life.

1. Introduction

Walleye pollock Gadus chalcogrammus Pallas, 1814 is the most widespread bentho-pelagic fish species of the North Pacific [1,2]. Its range extends from the Chukchi Sea in the north to the waters of Korea, Japan, and California in the south [3,4,5]. There are also occasional records of this species in the North Atlantic and adjacent Arctic, including the Norwegian and Barents seas [6,7]. Walleye pollock is a valuable commercial species, occupying a leading position in terms of catch both in the North Pacific and in world fisheries as a whole [8,9,10,11,12]. In addition, it plays an important role in the ecosystems of the North Pacific, participating in various trophic chains from invertebrates as consumer to predatory fish, marine mammals and birds as prey [1,2,13].
For more than a century since the description of walleye pollock as a species, its taxonomic position has been repeatedly revised. Thus, it was originally described by Pallas [14] within the genus Gadus from a specimen from the Sea of Okhotsk off the coast of Kamchatka as G. chalcogrammus. About sixty years later, from the waters of Alaska near the Unalaska Island, Cope [15] described the species Gadus periscopus. Afterwards, Steindachner and Döderlein [16] described a new species Gadus minor from the waters of Japan near Tokyo. A few years later, Jordan and Gilbert [17] described a subspecies Pollachius chalcogrammus fucensis from the waters of Puget Sound (near Tacoma, Washington, USA), which Jordan and Evermann [18] subsequently placed in the genus Thergara and provided it with the status of a valid species Theragra fucensis. All these taxa were described from the waters of the North Pacific and are now recognized as junior synonyms of Gadus chalcogrammus [3,19,20]. In the mid-1950s, the Norwegian pollock Theragra finnmarchica Koefoed, 1956, was described from the waters of northern Norway (near Berlevåg) [21], which was long considered a valid species. Since its description, several dozen captures have been recorded in the Norwegian and Barents Seas [7,22,23,24]. Only with the widespread use of genetic analysis methods in ichthyology did it become possible to show the conspecificity of the walleye and Norwegian pollocks [25,26,27,28,29] and restore the validity of the Gadus chalcogrammus species.
Along with the change in taxonomic status, the ideas about the range of walleye pollock also changed. After the description of the Norwegian pollock, it was long believed that the genus Theragra is represented by two species (T. chalcogramma and T. finnmarchica) with ranges, respectively, in the North Pacific and the North Atlantic off the coast of Norway [30,31]. After the recognition of the Norwegian pollock as a junior synonym of the walleye pollock, it became clear that the range of this species is interrupted in the Siberian Arctic. At the same time, it is believed that there is an independent population in the Norwegian and Barents seas [6], which can be replenished by individuals from the North Pacific. However, there is another point of view [5], according to which the few records of walleye pollock in the North Atlantic are the result of the transport of its pelagic progeny by currents from the North Pacific to the Arctic through the Bering Strait and further active migrations into the Norwegian and Barents Seas. Thus, until now, there were no data on the occurrence of walleye pollock in the Siberian Arctic, so that it was not possible to draw reliable conclusions about the status of this species in the waters of the Northeast Atlantic. Meanwhile, this problem is important for understanding such evolutionary processes as speciation, distribution, population formation, etc.
The purpose of this paper is to document the first records of walleye pollock in the Siberian Arctic (southeastern Barents Sea, Kara Sea and Laptev Sea) testified with the data on external morphological characters, sequences of the CO1 mtDNA gene, X-rays of fish, and photos of fish and sagittal otoliths.

2. Materials and Methods

This paper is based on new records of walleye pollock individuals in the southeastern Barents Sea in 2018, the Kara Sea in 2008, and the Laptev Sea in 2019 (Table 1) on board various Russian research and commercial fishing vessels. A total of 14 specimens were caught. New records of walleye pollock in the Siberian Arctic were obtained outside of its known range. One individual was caught in the southeastern Barents Sea to the north of the Kolguev Island (Figure 1). The capture of 9 more specimens was first recorded in the Kara Sea between the Franz Josef Land and Severnaya Zemlya archipelagos. Also, for the first time, this species was registered in the Laptev Sea to the northeast of the Taimyr Peninsula.
Walleye pollock captures in the Siberian Arctic were recorded in a wide range of depths from 42 to 603 m. The shallowest catch (42 m) was recorded in the southeastern Barents Sea, and the deepest (603 m) in the Laptev Sea. According to the capture depth, the Kara Sea (383 m) occupies an intermediate position.
All biological work was carried out in accordance with generally accepted methods [32,33]. In all fish, the total length (TL) and body weight were measured. In individuals from the Barents and Kara seas, the sex, the stages of gonad maturity, the weight of the liver, gonads, and stomach contents were additionally determined, and the age was examined by sagittal otoliths. Sagittae were extracted from freshly caught fish during the biological analyses onboard. The age determinations were carried out in the laboratory. Sagittae were broken transversely in half with a lancet and baked, then polished if necessary. They were burned in the flame of an alcohol burner. For the preparation of polished cross-sections of the sagittae, abrasive discs with aluminum-oxide- or silicon-carbide-coated grit of 0.1−0.9 μm (Buehler, Inc., Lake Bluff, IL, USA) were used. The readiness of each sagitta for further analysis was determined individually on the basis of visual observations. We used a trinocular microscope (Olympus SXZ12) with a DFPLAPO 1 × PF lens to view the cross-sections at 1 × 20–40 magnification. Otolith cross-sections were coated with glycerin and illuminated with reflected light [34,35]. The ratio between otolith length and otolith width [36] are based on the measurements made using digital caliper.
Gonadal maturity state of walleye pollock specimens were examined at macroscopic level based on a six-stage scale [37].
Four individuals from the Laptev Sea (specimens from the Kara and Barents Seas were discarded after dissection, examination of biological characteristics, and extraction of sagittae) were subjected to morphometric analysis with the measurement of characteristics previously used by various authors in the study of specimens from the North Pacific and the North Atlantic [23,24,28,30,38,39,40,41]. The following morphometric characteristics were measured: predorsal and preanal lengths, pectoral and pelvic fin lengths, body depth, depth of caudal peduncle, head length, upper jaw length, interorbital length, horizontal and vertical eye diameters, preorbital and postorbital lengths, lengths of D1, D2 and D3 bases, lengths of A1 and A2 bases. All measurements were carried out on individuals preserved in a 6% formalin solution using digital calipers. Counts of the number of D1, D2, D3, A1, A2, pectoral, pelvic, and caudal fin rays, and number of vertebrae were carried out according to radiographs produced on an EcoRay Orange 1040 HF Portable X-Ray Generator (EcoRay, Seoul, Republic of Korea). Individuals from the Laptev Sea were deposited in the ichthyological collection of the Shirshov Institute of Oceanology of the Russian Academy of Sciences under the catalog numbers IORAS 04464-04467.
The pectoral fins clips of walleye pollock specimens, preserved in alcohol, were registered and deposited in the Russian National Collection of Genetic Reference Materials in the Russian Federal Research Institute of Fisheries and Oceanography (VNIRO, Moscow, Russia) (Table 2). All tissue samples were fixed in volumes of 96% ethanol at least 5 times larger than sample volume. Fixed samples were stored at −20 °C; ethanol was changed approximately a month after collection, and again in a year.
DNA was extracted with Wizard SV 96 Genomic DNA Purification System (Promega Corporation, Madison, WI, USA) according to the manufacturer’s manual.
All molecular genetic studies (DNA extraction, polymerase chain reaction (PCR), PCR product purification, and nucleotide sequencing) were performed using standard molecular genetic techniques [42]. Cytochrome oxidase subunit I (CO1) fragment of 510 b.p. was amplified with a primer complex of VF2_t1, FishF2_t1, FishR2_t1, FR1d_t1 [42,43]. Amplification was conducted in a volume of 15μL with 90 ng total DNA, buffer 1x, 2.5 mM MgCl2, 0.2 mM dNTP, 0.5 mM of each primer, and 0.75 U μL−1 Color Taq polymerase. Cycling consisted of 5 min at 95 °C, followed by thirty-five cycles of 30 s each at 95 °C, 45 s at 52 °C, 60 s at 72 °C, and a final extension for 12 min at 72 °C. All resulting amplicons were purified by ethanol precipitation [44].
Purified fragments were sequenced from both strands by Applied Biosystems BigDye Terminator v3.1. kit (Applied Biosystems, Foster City, CA, USA) with capillary electrophoresis on ABI3500 Genetic Analyzer in VNIRO Laboratory of Molecular Genetics.
Resulting sequences were assembled in Geneious 6.5.0 (Biomatters, Auckland, New Zealand) [45] and aligned with “ClustalW” built in algorithm. They were subsequently translated into the necessary format for constructing a haplotype network in the PopArt program (Allan Wilson Centre Imaging Evolution Initiative, Otago, New Zealand) [46]. The FaBox 1.41 converter was used to convert the fasta file to the format required for calculation [47]. A network of haplotypes was constructed on the basis of the maximum parsimony method using TCS v. 1.21 software (Computational Science Laboratory, Provo, UT, USA). DnaSP v. 5.10.01 software (University of Barcelona, Barcelona, Spain) was used for the analysis of the average number of nucleotide substitutions and number of haplotypes in samples [48].
Data processing was performed, and a molecular genetic tree was constructed by using Geneious 6.0.5 software (Biomatters, Auckland, New Zealand) based on the Neighbor–Joining method with European hake Merluccius merluccius as an outgroup [49] with the use of Genetic Distance HKY model and 1000 bootstrap replicates [50].
Data on CO1 sequences of walleye pollock from various parts of species’ range and its congeners represented by Greenland cod Gadus ogac, Atlantic cod G. morhua and Pacific cod G. macrocephalus (sister groups involved in the analysis for comparative purposes [51]) were taken from the open BOLD (https://www.boldsystems.org/) (accessed on 24 September 2021) and NCBI (https://www.ncbi.nlm.nih.gov/) (accessed on 24 September 2021) databases.

3. Results

The records considered were represented by individuals of various lengths and physiological state (Figure 2). The smallest walleye pollock with a length of 32–35 cm (on average 33.3 cm) was recorded in the Laptev Sea. In the Kara Sea, the fish was noticeably larger with a length of 33–43 cm (on average, 38.4 cm). The largest individual with a length of 77 cm was caught in the Barents Sea. The body weight of walleye pollock varied between 195–272 g (on average 232.5 g) in the Laptev Sea and from 230 to 530 g (on average 391.2 g) in the Kara Sea. The weight of an individual from the Barents Sea was 2930 g.
Walleye pollock catches in the Barents and Kara Seas were mainly represented by females with gonads at various stages of maturity from immature (stage 2) to maturing (stage 3) and mature (stage 4).
The age of walleye pollock in the Kara Sea ranged from 4+ to 7+ years (on average 5.7 years). The age of the largest fish from the Barents Sea was 13+ years. At the same time, walleye pollock in the Kara Sea actively fed, and the stomach of a large male from the Barents Sea was empty.
Walleye pollock specimens from the Laptev Sea were characterized by the following (Table 3) external morphological characteristics (average values in percent of standard length, % SL): predorsal length 44.9, preanal length 29.0, pectoral fin length 17.5, pelvic fin length 14.9, body depth 17.0, depth of caudal peduncle 4.3, pectoral fin length 25.0, upper jaw length 10.5, interorbital length 6.3, horizontal eye diameter 6.3, vertical eye diameter 5.7, preorbital length 7.9, postorbital length 11.9, length of D1 base 10.4, length of D2 base 15.8, length of D3 base 15.0, length of A1 base 18.3, length of A2 base 15.1. The average values of the meristic characteristics of these individuals were as follows (Figure 3): number of D1 fin rays 12.8, number of D2 fin rays 16.3, number of D3 fin rays 19.0, number of A1 fin rays 20.8, number of A2 fin rays 20.0, number of pectoral fin rays 18.5, number of pelvic fin rays 6.8, number of caudal fin rays 50.5, number of vertebrae 51.5.
The sagittal otoliths of walleye pollock caught in the Kara Sea (Figure 4) have the following morphological characteristics. The lateral surface (side opposite the sulcus) is distinctly concave. It is flat or almost flat. Otolith width is less than 44% of otolith length and usually less than 40%. Lobulations on ventral margin do not extend up to the longitudinal midline.
The results of a comparative genetic analysis of the sequences of walleye pollock mtDNA CO1 gene fragment (Figure 5) from different regions show that there were no principal differences between various samples. European hake Merluccius (outgroup) represented a separate branch from all representatives of Gadus genus. Individuals of Greenland cod Gadus ogac, Atlantic cod G. morhua and Pacific cod G. macrocephalus (sister groups), which formed independent clusters, were well differentiated from walleye pollock samples. Nine substitutions with site positions 69, 84, 123, 219, 270, 324, 399, 408 and 486 were found within the walleye pollock samples, all of them were synonymous. No non-synonymous substitutions were found within the group of walleye pollock and cod sequences. Only four non-synonymous substitutions were found in the European hake sample in relation to all other samples in positions 56, 209, 272 and 368. At the same time, walleye pollock samples did not form separate clusters according to the geographical principle and were mixed with each other. Thus, the nucleotide sequences of samples from the North Atlantic (Barents and Norwegian Seas and waters of Svalbard) were close to those from the Beaufort, Chukchi and Laptev Seas, and the Pacific waters of the United States and Canada. At the same time, samples from the Laptev Sea were close to those from the Beaufort and Chukchi Seas, the North Atlantic and the waters of the Pacific coast of the United States and Canada.
The results of the genetic analysis reveal 12 different haplotypes among the walleye pollock samples studied (Table 4). The haplotype H2 was the most frequent among them, which was found in 15 walleye pollock samples from the Bering, Beaufort, Chukchi, and Laptev Seas, the waters of British Columbia, Puget Sound, Norway, Svalbard and the Aleutian Islands. The remaining haplotypes were observed in 1–3 cases. At the same time, haplotype H1 was found in walleye pollock from the waters of Japan and the Chukchi Sea, i.e., in remote areas from each other.
The CO1 haplotype network, constructed on the basis of all walleye pollock samples, its congeners and outgroup (Figure 6), demonstrates that walleye pollock haplotypes form a star-shaped structure with the main central haplotype H2, from which the remaining haplotypes are separated by 1–2 mutations. At the same time, various haplogroups are formed by haplotypes belonging to individuals from different geographical areas.

4. Discussion

Until recently, nothing was known about the occurrence of walleye pollock in the Siberian Arctic. It was believed that walleye pollock could not be found in the Chukchi Sea [3,52,53]. Its presence in this area was only recently reported, but the abundance of this species was considered insignificant [6]. In August 2019, adult walleye pollock were found in large amounts in the western Chukchi Sea, and in September 2019 several specimens were caught in the Laptev Sea [5,54,55,56,57]. However, there was no detailed description of the records in the latter area.
The depths of walleye pollock captures in the Siberian Arctic (42–603 m) fit into the known range of its occurrence in the North Pacific, which is 0–1280 m [58] and well corresponds to the range of their preferred habitat depths (30–590 m).
Walleye pollock can reach a total length of 91 cm [53,59], but fish of this length are extremely rare in catches. The catches are usually dominated by medium-sized individuals, and the size composition depends on the geographical area, season, depth, and fishing gear [1,52]. Our catches of walleye pollock by bottom trawls in the Kara and Laptev Seas were mainly represented by medium-sized individuals, which is typical for trawl catches in other areas [52,60,61,62]. A large male in the Barents Sea was caught by the bottom longline that is associated with the feeding habits of an adult walleye pollock, which, as it grows, turns to a predatory lifestyle [1,63].
The body weight of walleye pollock can reach 3.9 kg [64]. The body weight of walleye pollock individuals caught in the Siberian Arctic did not differ in principle from that of individuals from the eastern Bering Sea [63]. Thus, the eastern Bering Sea walleye pollock with a length of 33 cm has an average body weight of 250 g, with a length of 39 cm—410 g, with a length of 43.5 cm—565 g and with a length of 72 cm—2537 g. These values are quite comparable to those of our specimens.
The maximum age of walleye pollock is estimated to be from 15 years [63] to 28 years [65]. At the same time, the catches in the Bering Sea are dominated by fish aged from 2+ to 5+ years, which account for about 90% in the western Bering Sea and more than half of the catches in the eastern Bering Sea [66]. Fish under the age of 7+ years predominate in other parts of the range [60,61,62]. In this respect, the age composition of our catches does not principally differ from that in the native range, since a significant part of the individuals from the Kara Sea were over the age of 5+ years, and the individual from the Barents Sea was 13+ years old.
The predominance of females in our samples may be due to a small sample size, although there is information about the prevalence of females in catches at spawning grounds, for example, in the Korean waters of the Sea of Japan [67]. In the eastern Bering Sea, 50% of the females and males become sexually mature at a length of 35 and 32 cm, respectively [63]. Off the coast of Hokkaido, the southern Kuril Islands and the western Kamchatka, the corresponding values are 40.7–45.3 cm and 37.5–43.1 cm [68]. All females and males become sexually mature depending on the area at a length of 41–53 cm [66]. In our samples from the Kara Sea, all walleye pollock individuals with a length of 34 cm or more were sexually mature, which fully corresponds to the published data for the northern parts of its range.
Walleye pollock spawning lasts for 2–7 months [3]. In the northern parts of the range, it occurs in the winter–spring period, while in the southern regions it is shifted to the winter [1,52]. The period of walleye pollock captures in the Kara Sea (September) fell on the feeding period, when the fish actively feeds, which explains the good filling of their stomach with food. In the Barents Sea, a large male with an empty stomach was caught in December, during the pre-spawning period, when the feeding activity of this species decreases [1,52]. Unfortunately, the analysis of the diet composition of walleye pollock individuals caught in the Siberian Arctic was not carried out. Nevertheless, through the X-ray of a single specimen from the Laptev Sea (no. 3, Figure 3), sagittal otoliths are clearly visible in the stomach. In shape, they certainly belong to a representative of the family Gadidae [69], most likely to the polar cod Boreogadus saida, which is the most abundant fish in this area [55,70,71,72,73].
The data on morphometric characteristics of individuals from the Laptev Sea, as a whole, are within the limits of intraspecific variability of walleye pollock from the waters of the North Atlantic and North Pacific [23,24,28,30,38,39,40,41]. Minor differences in our data from previously published research may be related to the shorter length of our fish, since walleye pollock is characterized by age-related variability of external morphological features [74,75]. As for the meristic characters, the overwhelming majority of them also are within the limits of intraspecific variability. The only exception is the number of rays in the pectoral fin, which in one case (20) slightly exceeds the known range (16–19) from published sources [23,24,28,39,40].
Walleye pollock sagittal otoliths from the Kara Sea had a typical shape for sagittae of gadid fishes [61] and did not differ in any way in shape or proportions from those of North Pacific walleye pollock individuals [69,76,77].
The results of our genetic analysis (composition of haplotypes, haplotype network, and tree topology reconstruction) clearly show that throughout the vast range from the Norwegian and Barents Seas to waters of Japan, Korea and California, including the Arctic, there is a single species, walleye pollock Gadus chalcogrammus. This is in good agreement with the results of previous studies [25,26,27,28,29], which indicate the conspecificity of the walleye and Norwegian pollocks and do not support the opinion of individual scientists [23,24] about the validity of the latter species.
The new data obtained by us on the records of walleye pollock in the Siberian Arctic allow us to present a hypothetical scheme of its dispersion from the North Pacific. The distribution of walleye pollock in the North Atlantic is limited to the coastal waters of the Norwegian Sea from the west, to the north of the Kolguev Island from the east, and to the waters north of the Svalbard from the north [6,78], according to our data. At the same time, records of this species in this area are extremely rare [7] and are mainly represented by large adult fish [22,23,24,28]. Until recently, there was no information about the occurrence of adult walleye pollock in the Chukchi Sea [52,53]. Only recently there was information about its presence in this area, but the abundance of this species was considered insignificant here [6]. In recent years, adult pollock has been found in large numbers in the western Chukchi Sea [5,54,55,56,57]. New captures of medium-sized walleye pollock in the Laptev and Kara Seas suggest that individuals of this species at the early life stages from the Bering Sea through the Bering Strait with Pacific inflow [79] are transported to the Chukchi and East Siberian Seas. This possibility is evidenced by the appearance in recent years, along with adult walleye pollock, of a noticeable number of juveniles in the Chukchi Sea [54]. It can be further assumed that, after reaching a certain length, walleye pollock can perform active lengthy migrations, which are an integral part of its lifecycle [5,80,81,82]. At the same time, shifting gradually westward as it grows, it moves against the currents that in the Laptev, Kara and Barents Seas have a general eastward direction [83,84]. This assumption is supported by the size composition of walleye pollock, which in the Laptev Sea is represented by individuals with a length of 32–35 cm, in the Kara Sea by fish with a length of 33–43 cm, and in the Barents and Norwegian Seas reaches a length of over 43 cm, on average over 50 cm [22,23,24,28]. Judging by the age of the fish in the samples, such migrations can take several years. However, it should be noted that recently a walleye pollock with a length of 36.5 cm was caught in the waters north of Svalbard [78], which does not quite fit into the hypothesis we proposed. Nevertheless, based on the morphological features, the authors assume the North Pacific origin of this individual. It can be assumed that this specimen was transported to Svalbard by another way, namely, by a current that carries surface waters from the Laptev Sea to Svalbard through the central Arctic [83,84]. It is possible that with the warming in the Arctic basin, the survival of early walleye pollock progeny became possible, and the record of this specimen is the result of the spawning of large-sized walleye pollock individuals migrated to the Barents and Norwegian Seas from the North Pacific. This possibility is indicated by the physiological state of specimens caught in the Barents Sea, whose gonads were in a pre-spawning or post-spawning condition [23,24], according to our data. In any case, their abundance here is very low and therefore there are no reasons to assume the presence of a self-reproducing population in this area yet. Thus, the waters of the North Atlantic and the adjacent Arctic should probably be considered as a zone of sterile walleye pollock eviction.

5. Conclusions

The data presented here clearly indicate that the few records of walleye pollock in the North Atlantic have their origin from the North Pacific, and its range extends almost continuously from the coast of Norway in the North Atlantic to the coasts of Korea, Japan, and California in the North Pacific. Walleye pollock has not yet been found in the East Siberian Sea, since research there is extremely rare and limited in that area [85,86]. However, the discovery of walleye pollock in the East Siberian Sea, in our opinion, is a matter of the near future. The warming in the Arctic, accompanied by a decrease in the ice cover, provides good opportunities for the intensification of scientific research both in terms of expanding the geographical coverage of water areas previously closed by ice, and of the seasonal duration of work.
Undoubtedly, research in the seas of the Siberian Arctic and the northeastern Atlantic will continue in the future, accompanied by new records of walleye pollock. In this regard, the comparison of individuals from different geographical areas in order to determine their macro- and microevolutionary histories and relationships seems very promising. This requires carrying out research in the following areas:
-
comparative analysis of fossil records, modern distribution and variability of mtDNA genes (see e.g., [87]);
-
comparative analysis of the shape of otoliths (see e.g., [88,89]);
-
comparison of the chemical composition of otoliths (see e.g., [90]);
-
comparative analysis of the diet composition and feeding habits (see e.g., [91]), including evaluation of microplastic, macroplastic and other marine litter content in the stomach and its impact on the biological condition of fish (see e.g., [92,93,94]) since pollution of the Siberian Arctic in recent years become a serious ecological problem [95,96].

Author Contributions

Conceptualization, A.M.O.; methodology, A.A.V., M.O.R., E.V.V., S.Y.O.; software, A.M.O., A.A.V., S.Y.O.; validation, M.O.R., A.A.V., S.Y.O.; formal analysis, A.M.O., S.Y.O.; investigation, A.M.O., M.O.R., E.V.V., S.Y.O.; resources, M.O.R., E.V.V., A.A.V., S.Y.O.; data curation, A.M.O., M.O.R., E.V.V., A.A.V., S.Y.O.; writing–original draft preparation, A.M.O.; writing–review and editing, A.M.O., M.O.R., E.V.V., A.A.V., S.Y.O.; supervision, A.M.O. All authors have read and agreed to the published version of the manuscript.

Funding

Preparation of this paper was funded by the Ministry of Science and Higher Education, Russian Federation (grant No. 13.1902.21.0012, contract No. 075-15-2020-796).

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Not applicable.

Acknowledgments

The authors are grateful to their colleagues from VNIRO (Moscow, Russia), Vasily Ulchenko for providing the data on the capture, a tissue sample, and photo of sagittal otolith and fish caught in the Barents Sea, and Kristina Zhukova for determining the age of this specimen. Special thanks to Tatyana Prokhorova (Polar Branch of VNIRO-PINRO, Murmansk, Russia) for determining the age of walleye pollock from the Kara Sea. The authors are also grateful to their colleagues from VNIRO, PINRO and TINRO (Pacific Branch of VNIRO, Vladivostok, Russia) for their assistance in collecting material at sea. The authors thank two anonymous reviewers for their valuable comments and suggestions which allowed for considerable improvement of the manuscript.

Conflicts of Interest

The authors declare no conflict of interest.

References

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Figure 1. Map of walleye pollock Gadus chalcogrammus range (green shading) and its new records in the Barents Sea (★), Kara Sea (▲), and Laptev Sea (⊕).
Figure 1. Map of walleye pollock Gadus chalcogrammus range (green shading) and its new records in the Barents Sea (★), Kara Sea (▲), and Laptev Sea (⊕).
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Figure 2. Photographs of walleye pollock Gadus chalcogrammus caught outside of native range (from the Laptev Sea (a,b), the Kara Sea (c,d), the Barents Sea (e)) and viscera of specimen from the Barents Sea (f).
Figure 2. Photographs of walleye pollock Gadus chalcogrammus caught outside of native range (from the Laptev Sea (a,b), the Kara Sea (c,d), the Barents Sea (e)) and viscera of specimen from the Barents Sea (f).
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Figure 3. X-ray images of walleye pollock Gadus chalcogrammus from the Laptev Sea: (1): IORAS 04464, (2): IORAS 04465, (3): IORAS 04466, (4): IORAS 04467.
Figure 3. X-ray images of walleye pollock Gadus chalcogrammus from the Laptev Sea: (1): IORAS 04464, (2): IORAS 04465, (3): IORAS 04466, (4): IORAS 04467.
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Figure 4. Walleye pollock Gadus chalcogrammus whole sagittal otoliths of from the Kara Sea (a,b) and sagitta cross-section of the specimen from the Barents Sea (c).
Figure 4. Walleye pollock Gadus chalcogrammus whole sagittal otoliths of from the Kara Sea (a,b) and sagitta cross-section of the specimen from the Barents Sea (c).
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Figure 5. Tree topology reconstruction of 35 selected walleye pollock Gadus chalcogrammus specimens from the entire species range based on the Neighbor–Joining method, Kimura 2-parameter model and 1000 bootstrap replicates for mitochondrial cytochrome oxidase subunit I (CO1) genes. Numbers beside each branch indicate bootstrap values above 50%. Numbers to the right of the tree correspond to the number of specimens in Table 2.
Figure 5. Tree topology reconstruction of 35 selected walleye pollock Gadus chalcogrammus specimens from the entire species range based on the Neighbor–Joining method, Kimura 2-parameter model and 1000 bootstrap replicates for mitochondrial cytochrome oxidase subunit I (CO1) genes. Numbers beside each branch indicate bootstrap values above 50%. Numbers to the right of the tree correspond to the number of specimens in Table 2.
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Jmse 09 01141 g006 550
Figure 6. CO1 haplotype network of walleye pollock, its congeners and outgroup. Numbers of haplotypes correspond to Table 4, numbers of substitutions are given in brackets, Mmer = European hake, Gmor = Atlantic cod, Gog = Greenland cod, Gmac = Pacific cod, numbers before species acronyms correspond to number of samples in Table 2. The diameters of the circles are proportional to the number of samples, smallest circle corresponds to single sample.
Figure 6. CO1 haplotype network of walleye pollock, its congeners and outgroup. Numbers of haplotypes correspond to Table 4, numbers of substitutions are given in brackets, Mmer = European hake, Gmor = Atlantic cod, Gog = Greenland cod, Gmac = Pacific cod, numbers before species acronyms correspond to number of samples in Table 2. The diameters of the circles are proportional to the number of samples, smallest circle corresponds to single sample.
Jmse 09 01141 g006
Table
Table 1. Data on new captures of walleye pollock Gadus chalcogrammus in the Siberian Arctic (M = male, F = female, na = not available).
Table 1. Data on new captures of walleye pollock Gadus chalcogrammus in the Siberian Arctic (M = male, F = female, na = not available).
Vessel/GearDateLatitude, NLongitude, EDepth, mTotal
Length, cm		Weight, gSexMaturity StageLiver Weight, gGonad Weight, gFood Weight, gAge, Years
Barents Sea
FV “Kotoyarvi”/longline06.12.201869°31′50″47°25′30″42772930M3–412090013+
Kara Sea
RV “Obva”/bottom trawl02.09.200882°00′00″77°08′00″38335310F3188125+
43530F42116177+
41452F314886+
41495F4163457+
40474F4362746+
42420F4121426+
37360M41813195+
34250F312405+
33230F29244+
Laptev Sea
RV “Professor Levanidov”/bottom trawl12.09.201977°18′54″122°44′12″60332195nananananana
34247nananananana
77°20′06″120°12′18″45235272nananananana
13.09.201977°54′06″115°52′36″40832216nananananana
Table
Table 2. Information about CO1 sequences and respective samples used for genetic analysis to identify walleye pollock Gadus chalcogrammus from various areas of species’ range, its congeners and outgroup (na = not available).
Table 2. Information about CO1 sequences and respective samples used for genetic analysis to identify walleye pollock Gadus chalcogrammus from various areas of species’ range, its congeners and outgroup (na = not available).
No.
Sample		Number in
VNIRO Genetic
Database		Genbank
Accession
Number		Sampling
Date		LocalityCountrySource
European hake Merluccius (outgroup)
1naKX78281511.06.2013 GermanyNCBI
Greenland cod Gadus ogac (sister group 1)
2naLC14670726.07.2016 GreenlandNCBI
Atlantic cod Gadus morhua (sister group 2)
3naKJ2048792010–2012North SeanaNCBI
4naKJ2048802010–2012North SeanaNCBI
Pacific cod Gadus macrocephalus (sister group 3)
5naABCBF117-10nanaCanadaBOLD Systems
6naABCBF118-10nanaCanadaBOLD Systems
Walleye pollock Gadus chalcogrammus (main group)
7naABFJ129-0609.10.2005HachinoheJapanBOLD Systems
8naDSFAL234-0712.09.2007N Bering SeaUSABOLD Systems
9naDSFAL479-0809.08.2008W Beaufort SeaUSABOLD Systems
10naDSFAL480-0809.08.2008W Beaufort SeaUSABOLD Systems
11naDSFAL481-0809.08.2008W Beaufort SeaUSABOLD Systems
12naFHAK128-1902.08.2018British ColumbiaCanadaBOLD Systems
13naFHAK129-1902.08.2018British ColumbiaCanadaBOLD Systems
14naFMV085-0829.04.2003Puget Sound, WashingtonUSABOLD Systems
15naFMV086-0829.04.2003Puget Sound, WashingtonUSABOLD Systems
16naFMV441-0902.02.2009Puget Sound, WashingtonUSABOLD Systems
17naGBGC4810-08naFinnmarkNorwayBOLD Systems
18naGBGC4811-08naFinnmarkNorwayBOLD Systems
19naGBGC4812-08naFinnmarkNorwayBOLD Systems
20naNBMF027-1514.08.2011SvalbardNorwayBOLD Systems
21naSDP113001-1303.08.2012Aleutian IslandsUSABOLD Systems
22naSDP113002-1303.08.2012Aleutian IslandsUSABOLD Systems
23naSDP131037-1403.08.2012Aleutian IslandsUSABOLD Systems
24THE5962MZ75095011.09.2019E Chukchi SeaUSANCBI
25THE5980MZ75095111.09.2019E Chukchi SeaUSANCBI
26lapLevArk88MZ75094212.09.2019Laptev SeaRussiaNCBI
27lapTHE5897MZ75094313.09.2019Laptev SeaRussiaNCBI
28LevArk89MZ75094412.09.2019Laptev SeaRussiaNCBI
29THE5896MZ75094813.09.2019Laptev SeaRussiaNCBI
30THE5898MZ75094913.09.2019Laptev SeaRussiaNCBI
31barTHE2842MZ75093806.12.2018SE Barents SeaRussiaNCBI
32chuk1THE5881MZ75093923.08.2019W Chukchi SeaRussiaNCBI
33chuk1THE5884MZ75094023.08.2019W Chukchi SeaRussiaNCBI
34chuk2THE5983MZ75094111.09.2019W Chukchi SeaRussiaNCBI
35THE5882MZ75094523.08.2019W Chukchi SeaRussiaNCBI
36THE5885MZ75094623.08.2019W Chukchi SeaRussiaNCBI
37THE5889MZ75094723.08.2019W Chukchi SeaRussiaNCBI
Table
Table 3. Morphometric and meristic characteristics of walleye pollock Gadus chalcogrammus from various parts of species’ range.
Table 3. Morphometric and meristic characteristics of walleye pollock Gadus chalcogrammus from various parts of species’ range.
Character/SourceNorth AtlanticNorth PacificLaptev Sea
1234567891011
Min.Max.Mean
Total length (TL), mm620585 422 322352333.0
Standard length (SL), mm550555 507309 292320302.5
Morphometrics
% TL
Predorsal length40.042.6 40.7 40.4–44.1 39.641.240.8
Preanal length27.129.9 29.4 27.3–29.2 25.028.626.3
Pectoral fin length16.115.0 17.5–21.4 15.016.315.9
Pelvic fin length14.715.6 9.5–11.8 12.615.113.6
Body depth15.522.616.7–18.2 9.8–15.2 15.215.915.5
Depth of caudal peduncle4.04.24.4–4.5 3.0–3.5 3.64.23.9
Head length21.824.625.0–26.7 21.8–24.2 22.223.422.7
% SL
Predorsal length 47.245.7 43.945.344.9
Preanal length 31.232.4 27.531.429.0
Pectoral fin length20.0 18.417.7 16.618.017.5
Pelvic fin length18.7 15.715.9 13.816.614.9
Body depth 16.717.417.0
Depth of caudal peduncle4.5 4.24.6 4.04.64.3
Pectoral fin length24.5 25.726.4 24.525.825.0
Upper jaw length11.1 9.711.110.5
Interorbital length29.6 5.76.86.3
Horizontal eye diameter 4.95.8 5.96.66.3
Vertical eye diameter 5.36.05.7
Preorbital length 8.48.6 7.58.57.9
Postorbital length 12.912.6 11.412.911.9
Length of D1 base 12.112.1 9.011.510.4
Length of D2 base 17.517.6 14.816.815.8
Length of D3 base 16.015.9 13.815.615.0
Length of A1 base 20.721.4 17.220.218.3
Length of A2 base 16.816.6 11.417.215.1
Meristics
Number of D1 fin rays13121312.812.5 12–1412–1412–1413–14121412.8
Number of D2 fin rays161516–1716.116.3 12–1812–1812–1815–19141816.3
Number of D3 fin rays171618–2018.418.117.520–2117–2120–2118–23182019.0
Number of A1 fin rays172019–2019.720.8 19–2319–2319–2319–24182220.8
Number of A2 fin rays2019 (21)19–2018.919.4 21–2320–2321–2320–23192120.0
Number of pectoral fin rays19161918.818.8 18–19 162018.5
Number of pelvic fin rays67 6.16.2 5–6 676.8
Number of caudal fin rays 45.542.2 50 *52 *50.5
Number of vertebrae 5050–525050–52515251.5
*—total number of caudal fin rays (principal and procurrent); sources: 1—Barents Sea [24]; 2—Barents Sea [23]; 3—North Atlantic [40]; 4—Norwegian and Barents seas [28]; 5—waters off Alaska [28]; 6—Bering Sea [23]; 7—North Pacific [39]; 8—North Pacific [41]; 9—North Pacific [30]; 10—North Pacific [38]; 11—Laptev Sea (our data).
Table
Table 4. Composition of CO1 haplotypes in the studied walleye pollock Gadus chalcogrammus samples. Numbers of samples correspond to Table 2.
Table 4. Composition of CO1 haplotypes in the studied walleye pollock Gadus chalcogrammus samples. Numbers of samples correspond to Table 2.
No. SampleNo. HaplotypeCountry, Locality
123456789101112
7 Japan, Hachinohe
8 USA, Bering Sea
9 USA, Beaufort Sea
10 USA, Beaufort Sea
11 USA, Beaufort Sea
12 Canada, British Columbia
13 Canada, British Columbia
14 USA, Puget Sound
15 USA, Puget Sound
16 USA, Puget Sound
17 Norway, Finnmark
18 Norway, Finnmark
19 Norway, Finnmark
20 Norway, Svalbard
21 USA, Aleutians
22 USA, Aleutians
23 USA, Aleutians
24 USA, Chukchi Sea
25 USA, Chukchi Sea
26 Russia, Laptev Sea
27 Russia, Laptev Sea
28 Russia, Laptev Sea
29 Russia, Laptev Sea
30 Russia, Laptev Sea
31 Russia, Barents Sea
32 Russia, Chukchi Sea
33 Russia, Chukchi Sea
34 Russia, Chukchi Sea
35 Russia, Chukchi Sea
36 Russia, Chukchi Sea
37 Russia, Chukchi Sea
Total number of particular haplotype3152211111121
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Orlov, A.M.; Rybakov, M.O.; Vedishcheva, E.V.; Volkov, A.A.; Orlova, S.Y. Walleye Pollock Gadus chalcogrammus, a Species with Continuous Range from the Norwegian Sea to Korea, Japan, and California: New Records from the Siberian Arctic. J. Mar. Sci. Eng. 2021, 9, 1141. https://doi.org/10.3390/jmse9101141

AMA Style

Orlov AM, Rybakov MO, Vedishcheva EV, Volkov AA, Orlova SY. Walleye Pollock Gadus chalcogrammus, a Species with Continuous Range from the Norwegian Sea to Korea, Japan, and California: New Records from the Siberian Arctic. Journal of Marine Science and Engineering. 2021; 9(10):1141. https://doi.org/10.3390/jmse9101141

Chicago/Turabian Style

Orlov, Alexei M., Maxim O. Rybakov, Elena V. Vedishcheva, Alexander A. Volkov, and Svetlana Yu. Orlova. 2021. "Walleye Pollock Gadus chalcogrammus, a Species with Continuous Range from the Norwegian Sea to Korea, Japan, and California: New Records from the Siberian Arctic" Journal of Marine Science and Engineering 9, no. 10: 1141. https://doi.org/10.3390/jmse9101141

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