Structure and Assessment of Beluga Whale, Delphinapterus Leucas, Populations in the Russian Far East

Structure and Assessment of Beluga Whale, Delphinapterus leucas, Populations in the Russian Far East OLGA V. SHPAK, ILYA G. MESCHERSKY, DMITRY M. GLAZOV, DENIS I. LITOVKA, DARIA M. KUZNETSOVA and VIATCHESLAV V. ROZHNOV Introduction Far-Eastern waters were recognized: of marine resources in Russia, includ- Western Chukchi-East Siberian Sea ing belugas, is not based on the spe- In the Russian Far East, the belu- (stock no. 25), Anadyr Gulf (26); She- cies population structure, but rather on ga, Delphinapterus leucas, or white likhov (27); Sakhalin-Amur (28), and geographically defined fishing zones. whale, occurs in the Okhotsk Sea and Shantar (29). The delineation of Stock Our studies in the Okhotsk Sea have along the coastline of the Chukotka 25 was questioned by some experts, led to the Russian Federal Agency of Autonomous Region in the western who, based on satellite tracking data, Fisheries and the Ministry of Agricul- Bering, western Chukchi, and eastern suggested belugas migrating along ture recognizing the necessity to con- East Siberian seas (Fig. 1). From late Chukotka Peninsula coast belonged sider stock distribution when issuing 1920’s to the dissolution of the So- to United States or Canadian stocks total allowable takes (TAT) in this re- viet Union in 1991, Soviet scientists (i.e., Eastern Bering Sea (stock no. 3), gion (Ministry of Agriculture, Order conducted extensive studies on this Eastern Chukchi Sea (4), or Beaufort N 533, 27 October 2017). An updated species’ abundance and distribution, Sea (or Eastern Beaufort) (5)). For assessment of beluga population struc- mainly because belugas were hunt- stocks 25 and 26, no abundance esti- ture would be important for effective ed commercially (Kleinenberg et al., mates were provided, and the Okhotsk and sustainable management. 1964; Matishov and Ognetov, 2006). Sea beluga population (comprised of Here, we review and summarize our In 2000, scientific information on be- stocks 27, 28, and 29) was estimated previously published research results lugas in Russian waters was reviewed at 18,000–20,000 (IWC, 2000). and present updated genetic results and summarized for the global assess- Apart from nonexistent or method- on the Far Eastern beluga population ment of the species by the Scientific ologically poor abundance estimates, structure and status, to provide a basis Committee of the International Whal- no genetic information was available for effective conservation and sustain- ing Commission (IWC, 2000). At that at that time, and migration routes and able management. A working version time, five beluga stocks in Russian winter grounds remained mostly un- of this paper was originally presented known. Stock delineation was based and discussed at the Global Review of Olga Shpak ([email protected]), Ilya Me- solely on summer distribution and lo- Monodontids (GROM)1 meeting held schersky, Dmitry Glazov, Daria Kuznetsova, and Viatcheslav Rozhnov are with A. N. Sev- cal movement patterns. in March 2017 (Hobbs et al., 2019, ertsov Institute of Ecology and Evolution of the Since the IWC (2000) assessment, provide an overview of the meeting Russian Academy of Sciences, Str. Leninsky and a break in research in the 1990’s outcomes). Prospect, 33, Moscow, Russia 119071. Denis following the dissolution of the So- Litovka is currently with the Office of Governor Methods and Government of the Chukotka Autonomous viet Union, extensive beluga studies Region, Str. Bering 20, Anadyr, Russia 689000. have been resumed in the Russian Far Genetics doi: https://doi.org/10.7755/MFR.81.3–4.3 East in 2005. Currently management Our use of the term “biological population,” or population, is defined ABSTRACT—In 2000, the International Siberian seas. Published results of genetic as a group of individuals who inter- Whaling Commission conducted a global analysis are updated with our original un- assessment of beluga whales, Delphin- published data. Based on information avail- breed and are genetically isolated apterus leucas. Following this assessment, able to date, we propose recognizing seven from other biological populations due five beluga stocks were recognized in Rus- beluga stocks in the Russian Far East. Five to geographical, behavioral, or any sian Far East waters: Western Chukchi- stocks in the Okhotsk Sea: 1) Sakhalin- other reasons. In summer months, East Siberian Sea, Anadyr Gulf, Shelikhov, Amur, 2) Ulbansky, 3) Tugursky, 4) Udska- Sakhalin-Amur, and Shantar. This paper ya, 5) Shelikhov, and two stocks in the CAR: many beluga populations seasonally provides a revised assessment of beluga 6) Anadyr, and 7) Bering-Chukchi-Beaufort break into discrete, relatively resident abundance, distribution, and population (BCB). Natural and anthropogenic threats “nursery aggregations” (a synonym to structure in the Russian Far East. This re- to these stocks are described and include the term “reproductive aggregation” gion encompasses the Okhotsk Sea, and ice entrapment, over-fishing of key prey, live the coastline of the Chukotka Autonomous captures for aquaria, bycatch in fisheries, 1GROM (https://nammco.no/topics/report-glob- Region (CAR), which includes the western exposure to effluent, and seismic and mili- al-review-monodontids-now-available/ accessed Bering, western Chukchi, and eastern East tary activities. 9 Aug. 2018). 72 Marine Fisheries Review Figure 1.—Russian Far East with toponyms mentioned in the text. sometimes used in the Russian litera- units should be split until evidence is ellite loci: (Cb1, Cb2, Cb4, Cb5, Cb8, ture), and small groups, comprised available to justify combining them.” Cb10, Cb11, Cb13, Cb14, Cb16, Cb17 mostly of males, which are more no- A “pool” is defined as a large beluga – Buchanan et al., 1996; Ev37Mn, madic. A “stock” (also see Hobbs whale unit of an unknown demograph- Ev94Mn – Valsecchi and Amos, 1996; et al., 2019, under “Identification of ic status (presumably made up of mul- 415/416, 417/418, 464/465, 468/469 Stocks”), is a population unit which tiple stocks or even multiple biological – Schlötterer et al., 1991; Fullard et can be defined as discrete and sea- populations), within which we cannot al., 2000). The methods of genotyp- sonally stable and should be managed delineate stocks or populations due to ing and sex determination were anal- separately from other equivalent units the lack of information on their distri- ogous to those previously described (synonym of “management unit”). bution ranges, movement patterns, and in Meschersky et al. (2013). Sample Thus, a summer nursery aggregation is genetics. comparison was performed using the considered a stock if its geographical For the genetic analyses presented allele frequency based Fst-criterion (spatiotemporal) separation from the herein, we have combined our pub- (Arlequin 3.1 software, Excoffier et neighboring aggregations of the same lished (Meschersky et al., 2013, 2018) al., 2005) and a clustering method biological population can be proved and unpublished data to delineate each (LOCPRIOR-Admixture model, 5 by genetics, photo-identification, or stock, population, or pool. The level of runs of 50,000 MCMC iterations of other methods. Following the guidance population isolation was evaluated us- burn-in and 200,000 iterations of main in IWC (2000:244), “possible stock ing allele frequencies of 17 microsat- analysis) using Structure 2.3.4 soft- 81(3–4) 73 Figure 2.—The results of K = 3 hypothesis tested by clustering analysis based on 17 microsatellite loci alleles frequencies. LOCPRIOR-Admixture model. Samples = 1–Sakhalinsky Bay, 2–Nikolaya Bay, 3–Ulbansky Bay, 4–Tugursky Bay, 5–Udskaya Bay, 6–Western Kamchatka coast, 7–Gizhiginskaya Bay, 8–Anadyr Estuary, and 9–Chukotka coast. Light gray shaded area = western-Okhotsk population, dark gray shaded area = northeast Okhotsk population, and black shaded area = Anadyr-Chukotka pool. ware (Pritchard et al., 2000). Patterns Results and frequencies were found between of spatial distribution within regions the two Okhotsk Sea regions. Okhotsk Sea and populations were evaluated using Isolation of the Okhotsk Sea belu- maternal lineage (mtDNA haplotypes) Two multi-year projects were con- gas from whales inhabiting the Anadyr distribution (Fst-criterion—haplotypes ducted in the Okhotsk Sea during the Estuary (in the Bering Sea) was dem- frequency only, Arlequin 3.1 soft- period 2007–16. Genetic analyses onstrated earlier (Meschersky et al., ware). In most cases, a fragment of (Meschersky et al., 2013), together 2013; Borisova et al.2). With the cur- 559 bp (see Genbank JQ716342, for with geographic distribution studies rent sample size, we unambiguously instance) was used. Where appropri- (Shpak et al., 2010; Solovyev et al., confirmed isolation of the Okhotsk ate, results from O’Corry-Crowe et al. 2015), delineated two biological pop- Sea belugas from Bering Sea belu- (1997) were included to expand the ulations: 1) Western Okhotsk, which gas. The combined Anadyr-Chukotka dataset. The original samples (skin bi- includes belugas summering in the coast sample (n = 83) microsatellite opsies or tissues of dead animals) were Sakhalin-Amur and Shantar regions, allele distance was estimated at 4.78% collected during the period 2008–16 and 2) Northeast Okhotsk (or Shelik- for the western Okhotsk population, (and for Sakhalinsky Bay since 2004). hov), which spends the summer in the 4.30% for the Northeast Okhotsk Gizhiginskaya and Penzhinskaya bays (Shelikhov) population, or 4.15% for Distribution of Shelikhov Gulf and along the west- the combined Okhotsk Sea

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