Distribution, Abundance, Harvest, and Status of Western Alaska Beluga Whale, Delphinapterus Leucas, Stocks

Distribution, Abundance, Harvest, and Status of Western Alaska Beluga Whale, Delphinapterus leucas, Stocks

LLOYD F. LOWRY, JOHN J. CITTA, GREG O’CORRY-CROWE, LORI T. QUAKENBUSH, KATHRYN J. FROST, ROBERT SUYDAM, RODERICK C. HOBBS, and TOM GRAY

Introduction sink2), Norton Sound and the Yukon ed that these occurrences represented Delta (Nelson, 1887; Zagoskin, 1967), long established migration routes and Beluga whales, Delphinapterus leu- and in the Chukchi Sea in Kotzebue summer concentration areas, and that cas (also called white whales), are a Sound and along lagoons near Point belugas were an important subsistence conspicuous and important component Lay (Nelson, 1887; Foote and Wil- resource harvested at many coastal vil- of the marine mammal fauna of west- liamson, 1966; Childs3). Traditional lages (Huntington et al., 1999; Neakok ern Alaska. Early reports indicated knowledge of Alaska Natives indicat- et al.4; Chythlook and Coiley5). regular spring, summer, and fall oc- Research on belugas in Alaska ini- currences of belugas in the Bering Sea 2Lensink, C. J. 1961. Status report: beluga stud- tially focused on competition with in Bristol Bay (Brooks et al.1; Len- ies. Alaska Dep. Fish Game, Div. Biol. Res., commercial fisheries but later in- Unpubl. Rep., Juneau (avail. at http://www.adfg. alaska.gov/static/home/library/pdfs/wildlife/re- cluded potential impacts of proposed 1Brooks, J. W., A. S. Mossman, and H. Z. Han- search_pdfs/status_report_beluga_studies_1961. oil and gas leasing. Belugas in Bris- sen. 1955. Predator control and investigation: pdf). tol Bay were the subject of early sci- beluga investigation. In 1955 annual report, p. 3Childs, H. E., Jr. 1969. Birds and mammals of entific attention mostly because the 98–106. Alaska Fish. Board, Alaska Dep. Fish., the Pitmegea River Region, Cape Sabine, north- Rep. 7, Juneau (avail. at http://www.arlis.org/ western Alaska. Biol. Pap. No. 10, Univ. Alaska, largest commercial sockeye salmon, docs/vol1/A/31110164etc/31110164etc-1955. Fairbanks, 76 p. (avail. at https://scholarworks. Oncorhynchus nerka, fishery in the pdf#page=97). alaska.edu/handle/11122/1432). world occurs there (Jones et al.6) and

4Neakok, W., D. Neakok, W. Bodfish, D. Libbey, Lloyd Lowry was with the Alaska Beluga Whale Whale Committee. Kathryn J. Frost is with the E. S. Hall, Jr., and the Point Lay elders. 1985. Committee and submitted this manuscript prior Alaska Beluga Whale Committee, 73-4388 Paia- To keep the past alive: the Point Lay cultural re- to his passing on 25 November 2018. John Citta ha Street, Kailua Kona, HI 96740. Robert Suy- source site survey. North Slope Borough, Bar- is with the Alaska Department of Fish and Game, dam is with North Slope Borough Department of row, AK, 111 p. 1300 College Road, Fairbanks, AK 99701 and Wildlife Management, Box 69, Utqiag;vik, AK 5 the Alaska Beluga Whale Committee (email: 99723 and the Alaska Beluga Whale Commit- Chythlook, M., and P. Coiley 1994. The subsis- [email protected]). Greg O’Corry-Crowe tee. Roderick Hobbs is retired from the Marine tence use of beluga whale in Bristol Bay by Alas- is with the Harbor Branch Oceanographic Insti- Mammal Laboratory, Alaska Fisheries Science ka Natives, 1993. Tech. Paper No. 231. Alaska tute, Florida Atlantic University, Fort Pierce, FL Center, National Marine Fisheries Service, Dep. Fish Game, Div. Subsistence, Juneau, AK, 34946. Lori Quakenbush is with the Alaska De- NOAA, and currently affiliated with the North 29 p. partment of Fish and Game, 1300 College Road, Atlantic Marine Mammal Commission, 6130 6Jones, M., T. Sands, S. Morstad, P. Salomone, Fairbanks, AK 99701 and the Alaska Beluga NE 204th Street, Kenmore, WA 98028. Tom G. Buck, F. West, C. Brazil, and T. Krieg. 2013. Gray is Chair of the Alaska Beluga Whale Com- 2012 Bristol Bay area annual management re- doi: https://doi.org/10.7755/MFR.81.3–4.2 mittee, P.O. Box 306, Nome, AK 99762. port. Alaska Dep. Fish Game, Fish. Manage.

ABSTRACT—The Alaska Beluga Whale now be stable. Survey results and a genet- any decrease in abundance or availability. Committee co-manages three western Alas- ics mark-recapture study indicate a popu- The eastern Chukchi Sea stock is migratory, ka beluga whale Delphinapterus leucas, lation of approximately 2,000 whales. The wintering in the northern Bering Sea, mov- stocks with the National Marine Fisheries average annual Alaska Native subsistence ing north through the eastern Chukchi Sea Service, NOAA, and has conducted stud- harvest over the past decade (23) is below in spring, and summering in the Beaufort ies on stock identity, distribution, abun- the calculated potential biological removal Sea and Arctic Ocean. It is large, estimated dance, and subsistence harvests. Studies (PBR; 39-43). The eastern Bering Sea be- at approximately 20,000 animals based on of mitochondrial DNA revealed substan- luga stock concentrates in summer off the 2012 aerial surveys. The average annual tial differentiation among belugas that use Yukon River Delta and in Norton Sound and subsistence harvest (57) is well below PBR summering areas in Bristol Bay, the east- in winter moves offshore in the eastern Ber- (293). Few significant threats to persistence ern Bering Sea, and the eastern Chukchi ing Sea. Abundance has been estimated at of western Alaska beluga stocks have been Sea, and there is little overlap in their sea- approximately 9,242 based on aerial survey identified, although climate warming and sonal distributions. The Bristol Bay stock data collected in 2017. The average annual declines in sea ice and industrial activities summers in bays in inner Bristol Bay and subsistence harvest, plus the estimated num- related to resource development and in- winters in outer Bristol Bay. Abundance ber of struck and lost belugas, is 215 and creases in commercial shipping are of con- estimates from aerial surveys increased by exceeds the PBR calculated from this abun- cern and could pose challenges in the future. more than 4% per year during 1994–2005. dance estimate (201), but the abundance es- Continued monitoring of population size Survey counts in 2016 were similar to 2004– timate is thought to be biased low and local and trend, subsistence harvest, and health 2005 indicating that the population may and traditional knowledge does not indicate of western Alaska belugas is warranted.

54 Marine Fisheries Review salmon stocks were depleted. Stud- When the ABWC was formed, there that are co-managed by the ABWC in ies began in Bristol Bay in the 1950’s was no consistently funded research western Alaska (i.e., Bristol Bay, east- because of concern that belugas were or management program for belu- ern Bering Sea, and eastern Chukchi consuming enough salmon smolt to gas in Alaska. With its formation, the Sea stocks). Using recent abundance limit salmon populations (Brooks et ABWC brought together representa- and harvest information, we calcu- al.1; Lensink2) and there was pressure tives from beluga hunting communi- late the Potential Biological Removal by commercial fisheries to reduce be- ties in Alaska; federal, state, tribal, (PBR) (Wade and Angliss, 1997) and luga predation on salmon (Fish and and local governments; and beluga comment on sustainability of current Vania, 1971). researchers to develop and implement anthropogenic removals. To facilitate Research throughout western Alaska a program to provide the data needed the use of this information for NOAA began in 1977 to assess potential im- for sound beluga management. Goals Stock Assessment Reports (SAR’s), pacts of oil and gas exploration and of the ABWC were to identify man- we follow the format found in those development in the Bering, Chukchi, agement stocks in western Alaska, es- reports. and Beaufort seas (Burns and Sea- timate abundance and trends of those man7). Compilations of observational stocks, and monitor the number of Identity of Management Stocks data confirmed the widespread distri- belugas harvested from those stocks To understand the relationship of bution and common occurrence of be- for subsistence by Alaska Natives. In belugas summering in different re- lugas in western Alaska (Seaman et furtherance of these goals and with gions of western Alaska, the ABWC al.8). When all available sightings were funding from NMFS and other coop- sponsored genetic studies. A total of plotted, a non-uniform distribution of erators, the ABWC has conducted a 1,212 beluga skin samples were col- belugas in coastal waters during the total of 23 multi-day aerial surveys of lected from this region, many by Alas- summer was evident and suggestive belugas in three areas, Bristol Bay (N ka Native beluga hunters. Differences of population subdivisions (Frost and = 7), Norton Sound/Yukon Delta (N = in mitochondrial DNA (mtDNA; Fig. Lowry, 1990). This summer distribu- 7), and the eastern Chucki Sea (N = 9) 1) from different regions led to the tion pattern formed the basis for provi- since 1990. The ABWC began satel- identification of four genetically dis- sional stock designations recognizing lite tracking studies of beluga move- tinct stocks (Fig. 2) in the eastern Ber- that genetic studies would be required ments and habitat use in 1996, and has ing, Chukchi, and Beaufort seas: 1) to confirm underlying patterns of relat- facilitated and collaborated in beluga Bristol Bay (BB), 2) eastern Bering edness among the seasonal groupings tracking studies, including the train- Sea (EBS), 3) eastern Chukchi Sea (O’Corry-Crowe and Lowry, 1997). ing of hunters to attach transmitters, (ECS), and 4) Beaufort Sea (Muto et The Alaska Beluga Whale Commit- in Bristol Bay (N = 69), Norton Sound al., 2018). All of these stocks are ge- tee (ABWC) was formed in 1988 to (N = 7), and the eastern Chukchi Sea netically distinct from the stock in conserve beluga whales and manage (N = 30). In 1989, the ABWC initiated Cook Inlet. These genetic differences beluga subsistence hunting in western a pioneering genetics study of beluga likely reflected long-established pat- Alaska in cooperation with NOAA’s stock identity and by 2017 had facili- terns of female-mediated philopatry National Marine Fisheries Service tated the collection of more than 2,000 and group isolation (O’Corry-Crowe (NMFS) (Adams et al., 1993; Fernan- beluga skin samples. It supported a et al., 1997, 2002, 2018; Brown-Glad- dez-Gimenez et al., 2006; ABWC9). genetics-based mark-recapture study den et al., 1997, 1999; Meschersky et to estimate beluga abundance in Bris- al., 2008, 2013). Data from aerial sur- Rep. 13-20, Div. Commer. Fish., Anchorage, AK tol Bay and to validate aerial survey veys and satellite-linked depth record- (avail. at www.adfg.alaska.gov/FedAidPDFs/ estimates. The ABWC has collected ers (SDR’s) attached to whales have FMR13-20.pdf). subsistence harvest data during 1987– shown that each stock has distinct sea- 7Burns, J. J., and G. A. Seaman. 1988. Investi- gations of belukha whales in coastal waters of 2017 from more than fifty Alaska sonal distribution patterns (see Dis- western and northern Alaska. II. Biology and communities where beluga hunting oc- tribution and Movements below and ecology. U.S. Dep. Commer., Outer Continen- tal Shelf Environ. Assess. Prog. Fin. Rep. 56: curs. The ABWC stands as a model of Fig. 2). The three stocks, BB, EBS, 221-357 (avail. at https://www.boem.gov/ES- what can be achieved when scientists, and ECS, that have summer concen- PIS/0/81.pdf). Alaska Native hunters, and managing tration areas in western Alaska are the 8Seaman, G. A., K. J. Frost, and L. F. Lowry. agencies work together. subject of this review. We do not con- 1988. Investigations of belukha whales in coastal waters of western and northern Alaska. Part The goal of this manuscript is to sider Gulf of Anadyr belugas, because I. Distribution and abundance. U.S. Dep. Com- update what is known about the stock they summer in eastern Russia and are mer., Outer Continental Shelf Environ. Assess. identity, distribution, abundance, sub- not known to range into Alaska waters Prog. Fin. Rep. 56:153-220 (avail. at https:// 10 www.boem.gov/ESPIS/0/82.pdf). sistence harvest, and fisheries bycatch (Citta et al., 2016; Litovka et al. ; Fig. 9Alaska Beluga Whale Committee (ABWC). of the three stocks of beluga whales 1999. Agreement between the National Marine 10Litovka, D. I., R. C. Hobbs, K. L. Laidre, G. Fisheries Service and the Alaska Beluga Whale M. O’Corry-Crowe, J. R. Orr, P. R. Richard, R. Committee for co-management of the western North Slope Borough, Dep. Wildl. Manage., S. Suydam, and A. A. Kochnev. 2002. Research Alaska beluga whale population. Avail. from Box 69, Barrow, AK 99723, 8 p. of belugas Delphinapterus leucas in Anadyr

81(3–4) 55 2, 3). Beaufort Sea belugas winter in the Bering Sea (Citta et al., 2016; Fig. 3), are harvested at some locations in Alaska during spring migration (see Point Hope in Fig. 1), and spend summers near and offshore of the Mack- enzie estuary, Canada (Hauser et al., 2014; Fig. 2). We do not review the Beaufort Sea stock in this paper because research has been conducted primarily by Canadian researchers and the majority of removals occur in Canada. Belugas found in Kotzebue Sound deserve special mention. Studies conducted in the 1970’s and early 1980’s reported belugas entering Kotzebue Sound in mid- to late-June every year, during or shortly following ice break- up (Frost and Lowry, 1990; Seaman et 8 Figure 1.—Frequency distribution of the distinct mtDNA lineages found in the al. ). Traditional knowledge confirmed five major geographic regions used by summering beluga whales in Alaskan and this was a long-established summer northwestern Canadian waters: Cook Inlet, Bristol Bay, eastern Bering Sea, east- concentration area (Huntington et ern Chukchi Sea, and the Beaufort Sea, as well as one spring migration location, al., 1999). The number of whales re- Point Hope, Alaska (adapted from O’Corry-Crowe et al., 1997, 2002, 2018). Each mtDNA lineage, or haplotype, is denoted by a different color. The location of the turning to Kotzebue Sound declined summer aggregation, stock identity, and sample size are given at the bottom of the substantially after 1983 and has not figure. recovered; however, belugas have en- tered the Sound intermittently in summer in some subsequent years (Frost 11 stocks remain unclear. These are cur- variety of prey, including salmonids, and Lowry, 1990; Seaman et al. ). rent topics of research, and because of other fishes, and invertebrates (Quak- MtDNA characteristics of belugas the uncertainty described above we do enbush et al., 2015; Brooks et al.1; harvested before the decline showed not consider Kotzebue Sound belugas Lowry et al.13). After the salmon runs that those taken by Kotzebue Sound further in this paper. end in late summer, belugas widen hunters in the early 1980’s differed their distribution, but remain mostly from the other western Alaska stocks Distribution and Movements within Nushagak and Kvichak bays (O’Corry-Crowe et al., 2016, 2018). Bristol Bay (Fig. 4c; Citta et al., 2016). In winter, O’Corry-Crowe et al. (2018) also de- BB belugas range into outer Bristol termined that belugas recently harvest- Telemetry studies using SDR’s in- Bay as far as Cape Newenham (Fig. ed in Kotzebue Sound, at least in years dicate that BB belugas are typically 4d; Citta et al., 2016) and frequent the with adequate sample sizes, were ei- found in Nushagak and Kvichak bays inner bays less often, perhaps because ther from the Beaufort Sea stock or and associated river mouths and trib- the bays are covered in ice and pose a from a group closely related to that utaries during the summer and range risk of entrapment or because few prey stock. Why the group of belugas using more widely in the northeast region are available there. In winter, BB belu- Kotzebue Sound declined after 1983, of Bristol Bay in the winter (Citta et gas are known to spatially overlap with the status of that group of belugas al., 2016, 2017). In spring and summer belugas from the EBS stock but they prior to 1983, and the relationships of (Fig. 4a, b), their distribution is largely have not overlapped in time, although belugas harvested since 1983 to other restricted to Nushagak and Kvichak sample size is small (Fig. 3). Belugas bays (Frost et al., 1985; Lowry et al., 12 in both stocks were tracked in 2013, Gulf (Chukotka) using satellite telemetry. Ma- 2008; Citta et al., 2016; Frost et al. ), rine Mammals of the Holarctic. Abstracts of the where belugas are known to feed on a Fairbanks. Alaska Sea Grant. P.O. Box 755040, conference presentations. Moscow, p. 161–163 201 Elvey Building, Fairbanks, AK 99775-5040. (avail. at http://marmam.ru/upload/conf-docu- 12Frost, K. J., L. F. Lowry, and R. R. Nelson. 13Lowry, L. F., K. J. Frost, and G. A. Seaman. ments/mmc2002_full.pdf). 1984. Belukha whale studies in Bristol Bay, 1988. Investigations of belukha whales in coast- 11Seaman G., E. Barger, and R. Lee. 2015. Alaska. In B. R. Melteff (Editor), Proceed- al waters of western and northern Alaska. Part Buckland Beluga Whale Traditional Knowledge ings of the workshop on biological interactions III. Food habits. U.S. Dep. Commer., Outer Con- Project. Final Rep. Avail. from North Slope Bor- among marine mammals and commercial fisher- tinental Shelf Enviromental Assessment Pro- ough, Dep. Wildl. Manage., Box 69, Barrow, ies in the southeastern Bering Sea, p. 187–200. gram Fin. Rep. 56:359–391 (avail. at https:// AK 99723. Alaska Sea Grant Report 84-1, Univ. Alaska, www.boem.gov/ESPIS/0/80.pdf).

56 Marine Fisheries Review Figure 2.—The summer distribution of known beluga whale stocks in the Bering, Chukchi, and Beaufort seas. Figure modified from Citta et al. (2017). and although one EBS beluga moved tering grounds in the Bering Sea, but kon River water (Fig. 5) where belu- southeastward into the winter range only the EBS stock occupies nearshore gas were most likely feeding on Pacific of BB belugas in January, BB belugas waters in the northeastern Bering Sea salmon, Onchorhynchus spp. Belugas had moved into the inner bay, there- in summer (Fig. 2). are known to occur hundreds of kilo- fore there is no evidence that the two Aerial surveys for belugas in the Yu- meters up the Yukon River on occasion, stocks were in the same place at the kon Delta/Norton Sound region were presumably following salmon. In spring same time (Citta et al., 2017). begun by the ABWC in 1992. Most sur- and fall, belugas are seen along the veys were flown in June when belugas coast at many locations in the Yukon Eastern Bering Sea were concentrated off the mouths of Delta/Norton Sound region (Nelson, Although there were few winter the Yukon River and in southern Nor- 1887; Frost and Lowry, 1990). sightings, Frost and Lowry (1990) re- ton Sound (Lowry et al., 2017a; Lowry SDR’s were attached to two belugas ported belugas in the Norton Sound et al.14). High densities were observed in northern Norton Sound near Nome region in all seasons. ECS and Beau- along the 5 m isobath in silt-laden Yu- in the autumn of 2012 (Citta et al., fort Sea belugas may migrate through 2017). Those whales remained in Nor- the western part of this region in 14Lowry, L. F., D. P. DeMaster, and K. J. Frost. ton Sound in October and early Novem- spring and autumn when moving be- 1999. Alaska Beluga Whale Committee sur- ber, then as sea ice cover advanced they veys of beluga whales in the eastern Bering Sea, tween summering grounds in the 1992–1995. Paper SC/51/SM 34 presented to moved out of the Sound and southward, Chukchi and Beaufort seas and win- the IWC Scientific Committee, May 1999. but remained in the eastern Bering Sea

81(3–4) 57 Figure 3.—Winter ranges (minimum convex polygons of beluga whale satellite tag locations) of beluga stocks that winter in the Bering Sea. Polygons are drawn using January–March locations and years are denoted by the degree of shading. Figure repro- duced from Citta et al. (2017).

(Fig. 3). Both returned to Norton Sound Eastern Chukchi Sea tence hunt at Point Lay and equipped by mid-June 2013. Another beluga was with SDR’s that each provided loca- Studies conducted in the 1970’s and tagged near Nome in November 2016. tion data for 5–522 days (Suydam, early 1980’s reported belugas congre- That animal spent November–Decem- 2009; Hauser et al., 2014). Results gating in nearshore waters and passes ber 2016 and January–April 2017 in showed that after leaving Kasegaluk western Norton Sound and adjacent near Kasegaluk Lagoon typically in Lagoon in July, whales moved into waters of the eastern Bering Sea. In late June (Frost and Lowry, 1990; Sea- 8 the northern Chukchi and Beaufort May–June it moved into Norton Sound man et al. ). Traditional knowledge seas and some went far into the Arc- and to the mouth of the Yukon River confirmed this was a long-established tic Ocean, penetrating heavy ice cov- where it remained through October then summer concentration area (Hunting- er north of lat. 80° N (Suydam et al., moved again to western Norton Sound ton et al., 1999). Other than the an- 2001). Although belugas ranged wide- (ABWC15). nual return to the Kasegaluk Lagoon ly in summer, both adults and sub- area, little was known about the dis- 15Satellite tagging maps 2016-17 (avail. at http:// adults and both sexes were most often www.north-slope.org/departments/wildlife- tribution of the ECS stock until belu- found in water deeper than 200 m, management/co-management-organizations/ gas were tagged with SDR’s. During along and beyond the continental shelf alaska-beluga-whale-committee/abwc-research- projects/satellite-maps-of-tagged-alaskan- 1998–2012, 29 belugas were captured break, including into very deep basin beluga-stocks/satellite-tagging-maps-nov-2016). in conjunction with the annual subsis- waters (Citta et al., 2013). They rarely

58 Marine Fisheries Review Figure 4.—Locations for satellite tagged beluga whales in the Bristol Bay stock for (a) the spring (16 April–22 June), when salmon smolt, Oncorhynchus spp., and rainbow smelt, Osmerus mordax, are migrating; (b) the summer (23 June–1 September), when adult salmon are migrating; (c) the autumn, after the salmon migrations are complete (2 September–14 December); and (d) the winter (15 December–15 April), when sea ice is typically present. Data include those presented in Citta et al. (2016). used shelf waters of the Beaufort Sea into May (Fig. 3). One tag lasted long where belugas have been observed (Suydam, 2009; Clarke and Ferguson, enough to re-enter the Chukchi Sea in during the survey period in late June 2018; Stafford et al., 2018). Hauser et late May and another stopped trans- and early July. Weather permitting, al. (2014) used these data to describe mitting in early May, just south of Ber- two surveys were conducted each beluga distributions and home ranges ing Strait (Citta et al., 2017). day, both covering the entire summer for July through November by which range of this stock; only data from time the whales had moved southward Abundance and Trends surveys with good viewing conditions through the Chukchi Sea to the Bering were considered. Counts on individ- Bristol Bay Strait region (Fig. 6). The six whales ual flights during 1994–2005 ranged whose tags continued to transmit into Aerial strip-transect surveys were from 200–1,067, with annual averages late fall passed through Bering Strait in conducted in Bristol Bay periodical- of 362–623 (Fig. 7). Data from VHF November–December then remained ly during 1993–2005 (Lowry et al., transmitters attached to two BB belu- in the northern Bering Sea, between 2008). Within each survey year, mul- gas were used to estimate an availabil- Bering Strait and St. Lawrence Island, tiple flights covered the entire area ity correction factor of 2.75 (Frost et

81(3–4) 59 Figure 5.—MODIS image of Norton Sound and the Yukon River Delta taken from the Terra satellite on 17 June 2002. Dots are sightings of beluga whales made during aerial surveys 1995–2000. The dotted line indicates the 5 m isobath. The discharge plume of the Yukon River is darker where silt is more dense. al., 1985), which was later revised to that are dark colored and difficult to To further address the issues of 2.62 (Frost and Lowry16). The estimate see during surveys. abundance and correction factors, the of abundance for the BB stock in the The ABWC conducted aerial surveys ABWC and collaborators conducted a most current SAR is 1,926 (Muto et again in 2016 using the same methods genetic mark-recapture study of the BB al., 2018) and was calculated by mul- as the 1993–2005 surveys (Citta et al., stock beginning in 2002. Estimates of tiplying the average of counts from 2019). The average count from eight abundance based upon mark-recapture surveys in 2004 and 2005 (623) by complete surveys of Bristol Bay in methods are not reliant on estimating the revised availability correction fac- 2016 was 660 (coefficient of variation correction factors and provide an inde- tor (2.62) and by a correction for the (CV) = 0.09; see Fig. 7). Using the cor- pendent estimate of abundance. Dur- number of calves (1.18; Brodie, 1971), rections that have been applied in the ing 2002–11, the Alaska Department past yields an estimated abundance of of Fish and Game (ADFG) worked 2,040 (CV = 0.26) for 2016. The un- with Alaska Native beluga hunters and 16Frost, K. J., and L. F. Lowry. 1995. Radio tag certainty in the correction factors has collected skin samples using biopsy based correction factors for use in beluga whale population estimates. Working paper for Alaska, not been estimated; instead we have tips mounted on jab-sticks. Unique Beluga Whale Comm. Sci. Workshop, Anchor- estimated the CV of the abundance es- genotypes were determined by PCR age, AK, 5–7 April 1995, 12 p. Avail. from North Slope Borough, Dep. of Wildlife Man- timate using the standard deviation of amplification of mtDNA and eight mi- age., Box 69, Barrow, AK 99723. the counts divided by the average. crosatellite loci. Using a POPAN Jolly-

60 Marine Fisheries Review Figure 6.—Daily locations and home ranges of eastern Chukchi Sea belugas based on data collected during 1998–2012 from 29 whales equipped with satellite data recorders. Locations were collected during July–November; core and home ranges shown are for July and August, only. Modified from Hauser et al. (2014). Seber model, abundance was estimated is likely that some belugas did not en- over the 12-yr period, 1993–2005 at 1,928 belugas (95% confidence in- ter the sampling area during sampling, (Lowry et al., 2008). The mean and terval (CI) = 1,611–2,337; Citta et al., this estimate of abundance is best con- range of counts made in 2016 is com- 2018). Most belugas were sampled in sidered a minimum population size. parable to those in 2004–2005 (Fig. 7) Kvichak Bay at a time when belugas Results from the genetic mark-recap- suggesting that the population growth are also known to occur in Nushagak ture study are consistent with the es- observed during 1993–2005 had Bay. The pattern of genetic recaptures timate of 2,040 belugas from the 2016 slowed or ceased. and data from belugas with SDR’s in- aerial surveys. dicated that belugas in the two bays A regression analysis of trend Eastern Bering Sea regularly mix, suggesting the estimate showed that the mean count of BB be- To develop a population estimate for of abundance likely applies to all Bris- lugas increased 4.8% per year (95% the EBS beluga stock, for which no tol Bay belugas. However, because it confidence interval (CI) = 2.1–7.5%) directed efforts had ever been done,

81(3–4) 61 River) and the correction factor of 2.0 may be too low to account for the frac- tion of whales submerged in very tur- bid waters (Lowry et al., 2017a). Eastern Chukchi Sea An initial assessment of abundance of the ECS stock was made by using aerial photographs of belugas concentrated at Kasegaluk Lagoon passes to estimate that 2,282 belugas were present on 15 July 1979. The estimate included correction factors for whales outside the concentration area (+10%), whales too deep to be seen on the photographs (+20%), and dark colored yearlings that are difficult to see (+8%) (Seaman et al.8). Subsequent aerial surveys were conducted in the 1980’s and 1990’s. On 8 July 1987, an aerial strip transect sur- Figure 7.—Number of beluga whales observed during aerial surveys in Bristol vey conducted over a large concentra- Bay, 1993–2016. Black dots are the number of belugas counted during replicate tion of belugas near Point Lay counted flights and diamonds are the annual averages. For more information on aerial sur- 723 belugas; using correction factors of vey methods, see Lowry et al. (2008). The fit of linear versus other trends is statis- 2 or 3 to account for animals diving in tically equivocal so we do not present a trend line here. relatively deep water it was estimated that there may have been 1,400–2,100 ABWC conducted aerial line-transect accepted correction factor for availabil- belugas in that group (Frost and Lowry, surveys in the Norton Sound/Yukon ity of 2.0 (Reeves et al., 2011) was ap- 1990). During 1989–91, aerial surveys Delta region during 1993–95 (Low- plied, resulting in an abundance estimate of the concentration areas at Kasegaluk ry et al.14). These initial surveys pro- of 6,994 (95% CI = 3,162–15,472). In Lagoon resulted in single day counts vided distribution information and a June 2017 NMFS conducted an aerial ranging from 7 to 1,200 whales (Frost preliminary abundance estimate that survey of this population following pro- et al., 1993); offshore waters where confirmed that the EBS stock was cedures similar to the 2000 survey (Fig. belugas also occur were not surveyed. likely large (in the thousands) but the 8; Ferguson et al.17). Analysis of the Correcting the 1,200 minimum count adequacy of survey coverage was ques- survey data estimated a surface abun- using VHF tag data from Bristol Bay tionable and confidence intervals of dance of 4,621 belugas (CV=0.12, 95% for the proportion of belugas that were estimates were large. Additional line- CI =3,635–5,873); applying the multi- diving and thus not visible at the sur- transect surveys planned to cover all plier of 2.0 to account for submerged face (2.62; Frost and Lowry16), and for of Norton Sound and the Yukon Delta whales yields an abundance estimate of the proportion of neonates and year- were flown in 1999 and 2000. Density 9,242 belugas (Ferguson et al.17). With lings not seen due to small size and and abundance were estimated from the only two population estimates 17 years dark coloration (1.18; Brodie, 1971) 2000 survey, which had the most com- apart, the current trend in abundance produced a minimum abundance es- plete coverage of the area (Lowry et of the EBS stock is unknown; however, timate of 3,710 belugas for the ECS al., 2017a). In 2000, belugas were sel- the two estimates are not significant- stock. That estimate has been used in dom seen in the northern portion of the ly different, and we conclude that the NOAA’s SAR (Muto et al., 2016) and Sound, thus the study area was restricted population has not declined. These two elsewhere (Laidre et al., 2015). to the central and southern Sound and estimates may be conservative because Surveys conducted during 1996–98 the northern and western Yukon Delta, some belugas may have been outside also found belugas farther offshore and divided into four strata by latitude. the area surveyed (e.g., in the Yukon (Lowry et al.18), so subsequent efforts The density estimated with the model during 2001–03 included more off- that received most Akaike Information 17Ferguson, M., K. Frost, A. Brower, A. Wil- loughby, C. Sims, and R. Suydam. 2018. Esti- Criterion support was 0.121 belugas/ mated abundance and distribution of eastern 18Lowry, L. F., D. P. DeMaster, K. J. Frost, and km2 and the number of belugas at the Bering Sea belugas from aerial surveys in 2017. W. Perryman. 1999. Alaska Beluga Whale Com- 2018 Alaska Mar. Sci. Symp., Jan. 22–26, An- mittee surveys of beluga whales in the east- surface in the study area was estimated chorage, AK (Abstract only: avail. at https:// ern Chukchi Sea, 1996–1998. Rep. Int. Whal. to be 3,497 (CV = 0.37). A generally www.alaskamarinescience.org/past-symposia/). Comm. SC/51/SM 33.

62 Marine Fisheries Review Figure 8.—Transects flown, strata used in the analysis, and beluga sightings made during NMFS beluga surveys in the eastern Bering Sea, June 2017. shore flight lines. While belugas were A different approach was clearly estimated 5,547 (CV = 0.22) surface- occasionally sighted >50 km offshore, needed for estimating abundance of visible belugas. SDR data were used to sightings were infrequent (Lowry and the ECS stock. An analysis of the SDR develop correction factors to account Frost19,20). Locations from whales location data from belugas belonging for animals that were missed because tagged with SDR’s at Kasegaluk La- to the ECS and Beaufort Sea stocks they were outside of the study area and goon showed that many were beyond (Hauser et al., 2014) identified an area those diving too deep to be seen, re- the limits of the area surveyed (Suy- in the Beaufort Sea (long. 140° W sulting in a total abundance estimate dam et al., 2001). Aerial surveys for to 157° W) and a period (19 July–20 of 20,752 (CV = 0.70) (Lowry et al., the ECS stock were suspended by the August) when the two stocks did not 2017b). Additional surveys were con- ABWC after 2003 due to the high cost overlap (Lowry et al., 2017b). In 2012, ducted in 2013–16 and a full analysis relative to the low value of results for an aerial line-transect survey was con- of ECS beluga abundance using all assessing abundance. ducted in that area during that period available ASAMM data is underway. by the Aerial Surveys of Arctic Marine 19Lowry, L., and K. Frost. 2002. Beluga whale Anthropogenic Removals surveys in the Chukchi Sea, July 2002. Alaska Mammals (ASAMM) project (Clarke Beluga Whale Comm., Rep. 02-2. Avail. from et al.21) (Fig. 9). Analysis of those data North Slope Borough, Dep. Wildl. Manage., Subsistence Harvest Box 69, Barrow, AK 99723. 21Clarke, J. T., C. L. Christman, A. A. Brower, 20Lowry, L. F., and K. J. Frost. 2003. Beluga and M. C. Ferguson. 2013. Distribution and The ABWC, through its hunter del- whale surveys in the eastern Chukchi Sea, July relative abundance of marine mammals in the egates and collaborators, primarily the 2003. AK Beluga Whale Comm. Rep. 03-1. northeastern Chukchi and western Beaufort Avail. from North Slope Borough, Dep. Wildl. Seas, 2012. U.S. Bur. Ocean Energy Manage., Bristol Bay Native Association and Manage., Box 69, Barrow, AK 99723. Annu. Rep. OCS-BOEM-2013-00117. the North Slope Borough Department

81(3–4) 63 Figure 9.—Aerial surveys of Arctic marine mammals transect lines and sightings of eastern Chukchi Sea belugas in the Alaska Beaufort Sea during July–August 2012 (Lowry et al., 2017b).

of Wildlife Management, has collect- Table 1.—Alaska communities that reported harvesting belugas from the Bristol Bay, eastern Bering Sea, or east- ed data on Alaska Native subsistence ern Chukchi Sea beluga whale stocks in at least one year during 1987–2016. harvests since 1987. Twelve villages Bristol Bay Eastern Bering Sea Eastern Chukchi Sea harvested belugas in Bristol Bay in Aleknagek Norton Sound Yukon River Point Lay Clark’s Point Elim Alakanuk Wainwright at least one year since 1987 (Table Dillingham Golovin Chevak 1). During 1987–2006, the reported Egegik Koyuk Emmonak Igiugig Nome/Council Hooper Bay number of belugas landed each year Iliamna Saint Michael Kotlik by these villages combined averaged Levelock Shaktoolik Marshall Manokotak Stebbins Mountain Village 17 (95% CI = 14–20, range 6–35; Fig. Naknek Unalakleet Nunam Iqua 10a). During 2007–16, the reported Newhalen White Mountain Pitka’s Point New Stuyahok Pilot Station number of belugas landed each year Togiak Russian Mission Saint Mary’s by these villages combined averaged Scammon Bay

23 (95% CI = 21–25, range 19–28; Fig. 10b). Reporting of belugas struck and lost in the Bristol Bay region is incomplete and total removals could be Twenty-two villages report harvest- The average annual reported harvest somewhat higher (Frost and Suydam, ing belugas from the EBS stock, 9 increased approximately 25% from 22 2010; ABWC ). Although regression from Norton Sound and 13 from the 1987–2006 to 2007–16. Although this lines for both periods show a slight in- Yukon Delta (Table 1). The average increase is statistically significant p( creasing trend, neither is statistically annual reported harvest for 1987–2006 = 0.04), it is mostly due to better data significant p( = 0.64 and 0.61). was 152 belugas (95% CI = 123– being collected from more villages 181, range 31–281; Fig. 11a). During rather than more belugas being har- 22Alaska Beluga Whale Committee (ABWC). 2007–16, the average annual reported vested (ABWC22). When the ABWC Unpubl. data avail. from the North Slope Bor- ough, Dep. Wildl. Manage., Box 69, Barrow, harvest was 191 belugas (95% CI = began meeting in 1988, there were two AK 99723. 171–211, range 126–236; Fig. 11b). delegates representing Norton Sound

64 Marine Fisheries Review Figure 10.—(a) Number and trend of Bristol Bay belugas landed by subsistence hunters in Alaska during 1987–2006, and (b) during 2007–16). For more information on how harvest is documented see Frost and Suydam (2010).

Figure 11.—(a) Number and trend of eastern Bering Sea belugas landed by subsistence hunters in Alaska during 1987–2006, and (b) during 2007–16. For more information on how harvest is documented see Frost and Suydam (2010). and the Yukon Delta. Ten years later vest was 57 belugas (95% CI = 38–76, have monitored the groundfish trawl, there were 10, and currently there are range 14–121, Fig. 12b). The slight longline, and pot fisheries off western 15 communities represented by del- positive trend for 1987–2006 is not Alaska and during 2011–15 only one egates who attend meetings and report statistically significant (p = 0.93). beluga mortality was reported (Muto harvest data for their own and nearby The apparent strong negative trend for et al., 2018). villages. Intermittent struck and lost 2007–16 is not statistically significant During the Bristol Bay sockeye data are available for the EBS stock either (p = 0.15) because of substan- salmon fishery (managed by the State for 17 villages during the last 5 years. tial annual variations in harvest. Both of Alaska) in late June and early July, During those years, the number of be- Point Lay and Wainwright usually con- belugas are observed swimming near lugas reported to be struck and lost av- duct drive hunts, and typically only fishing operations, suggesting they eraged 13% of the landed but this is one or two whales at most are struck could be caught in the salmon set gill- based on incomplete data (ABWC22). and lost during those hunts (ABWC22). net and drift gillnet fisheries that oc- Harvest of belugas from the ECS cur in the inner bays. During May–July stock occurs mainly at the villages Fishery Bycatch 1983, Frost et al.12 conducted beach of Point Lay and Wainwright. The In the United States, commercial surveys in the inner bays from airplanes average annual reported harvest for fisheries operating in federal waters and boats and found 27 dead belugas, 1987–2006 was 48 belugas (95% CI (3–200 nmi. offshore) that may take at least 12 of which were attributed to = 37–59, range 0–86; Fig. 12a). Dur- marine mammals as bycatch are reg- bycatch in nets. The commercial gillnet ing 2007–16, the average annual har- ularly monitored. Fishery observers fisheries have never been monitored for

81(3–4) 65 Figure 12.—(a) Number and trend of eastern Chukchi Sea belugas landed by subsistence hunters in Alaska during 1987–2006, and (b) during 2007–16. For more information on how harvest is documented see Frost and Suydam (2010). bycatch and there are no current data assessment published on the IUCN Red 2008), but that may not be the maxi- on incidental take. There is also a large List in 2017 listed the species as “Least mum rate because subsistence harvest subsistence gillnet fishery for salmon in Concern” (Lowry et al.24). was occurring during that period. The Bristol Bay in which four belugas were Under the 1994 reauthorization of measured value for the BB stock is reported taken during 2013–14 (Muto the MMPA, the PBR for a stock is close to the 4%/yr that is used in the et al., 2018). Three of those takes were defined as the product of the mini- NOAA SAR as the default maximum reported as subsistence harvest as they mum population estimate, one-half the net productivity rate for cetaceans were used for subsistence purposes by maximum theoretical net productiv- (Wade, 1998), and we use the value of Alaska Natives. ity rate, and a recovery factor: PBR = 4.8%/yr in the calculations below. State-managed commercial, person- NMIN × 0.5RMAX × FR (Wade and An- Bristol Bay al use, and subsistence gillnet fisher- gliss, 1997). NMIN is the lower 20th ies for salmon or whitefish, Coregonus percentile of a log-normal distribution Based on 2004–05 average counts spp., occur in nearshore waters in the that represents the minimum number from aerial surveys, Muto et al. (2018) range of the EBS and ECS stocks. Al- of whales after accounting for uncer- estimated the minimum population though these fisheries are a potential tainty in the estimates. FR is equal to size for the BB stock as 1,565 belugas source of bycatch mortality and by- 1.0 when a population is stable or in- using a CV of 0.25. They did not esti- catch is not systematically monitored, creasing and can be adjusted lower for mate PBR because the abundance data it is likely that only a few whales declining trends or high uncertainty. were more than 8 years old. Using the are taken each year (ABWC and Although the system was designed 22 rate of increase of 4.8%/yr (Lowry et NSBDWM ). only to evaluate fishery bycatch, PBR al., 2008) as an estimate of R , we can be compared to all anthropogenic MAX calculated PBR using both the 2016 Stock Status removals as a conservative measure of aerial surveys and the mark-recapture None of the western Alaska beluga the sustainability of those removals. estimate of Citta et al. (2018). For the stocks are designated as “depleted” The only data on maximum net or “strategic” under the U.S. Marine productivity for belugas comes from 2016 aerial surveys, NBEST = 2,040; Mammal Protection Act (MMPA), nor the BB stock where the estimated CV = 0.26; NMIN = 1,645, RMAX = are they listed as “threatened” or “en- rate of increase over the 12-yr period 0.048; FR = 1.0; PBR = 39. For the dangered” under the U.S. Endangered 1992–2005 was 4.8%/yr (Lowry et al., mark-recapture estimate, which cov- Species Act (Muto et al., 2018). In an ers the period 2002–2011, NBEST = Bracho, E. Secchi, E. Slooten, B. D. Smith, J. 1,928; CV = 0.1; NMIN = 1,773, RMAX assessment done in 2008, the Interna- Y. Wang, and K. Zhou. 2012. Delphinapter- tional Union for the Conservation of us leucas. The IUCN Red List of Threatened = 0.048; FR = 1.0; PBR = 43. The cur- Nature listed belugas as a species “Near Species 2012: e.T6335A17690692 (avail. at rent average annual subsistence har- https://doi.org/10.2305/IUCN.UK.2012.RLTS. vest of 23 belugas is approximately Threatened” and also noted that the var- T6335A17690692.en). Downloaded on 03 Feb. ious subpopulations should be assessed 2017. 59% of PBR calculated from the 2016 separately (Jefferson et al.23). A revised 24Lowry, L., R. Reeves, and K. Laidre. 2017. survey data and 53% of PBR as cal- Delphinapterus leucas. The IUCN Red List of culated from the mark-recapture study. Threatened Species 2017: e.T6335A50352346 23Jefferson, T. A., L. Karkzmarski, K. Laid- (doi: https://doi.org/10.2305/IUCN.UK.2017-3. Some bycatch in fisheries is known re, G. O’Corry-Crowe, R. Reeves, L. Rojas- RLTS.T6335A50352346.en). to occur (Muto et al., 2018); howev-

66 Marine Fisheries Review er, bycatch has likely been too small is about 19% of PBR. Although coast- cies (Laidre et al., 2008; Haug et al., for total removals to exceed PBR be- al fisheries are not regularly monitored 2017), but the potential costs or bene- cause this stock has been increasing or for incidental take of belugas, all indi- fits to belugas of such changes are not stable. cations are that such takes are very in- known. Killer whales, Orcinus orca, frequent and therefore anthropogenic prey on belugas (Frost et al., 1992) Eastern Bering Sea removals from the ECS beluga stock and concentrated sea ice may provide In the 2017 SAR, the PBR for the are sustainable. belugas some degree of refuge from EBS stock was considered to be “un- predation. There is good evidence that determined” because the most cur- Threats killer whales are expanding into Arc- rent abundance estimate was more Sea Ice and Climate Warming tic regions where sea ice has been de- than 8 years old (Muto et al., 2018). clining (Higdon and Ferguson, 2009; However with the 2017 abundance es- Because belugas are an ice-associ- Ferguson et al., 2010). Belugas are timate of 9,242 (CV = 0.12) (Ferguson ated species, there is concern about susceptible to entrapment in sea ice et al.17), PBR can be calculated as fol- possible impacts of climate warming when conditions change rapidly and, lows: NBEST = 9,242; CV = 0.12; NMIN and associated loss of sea ice habitat. if they cannot escape, they may die or = 8,357, RMAX = 0.048; FR = 1.0; PBR Laidre et al. (2015) analyzed remote- be preyed upon by polar bears, Ursus = 201. It should be noted that this es- ly sensed sea ice data and found little maritimus, and humans (Lowry et al., timate includes an arbitrary correction change in the duration of the reduced 1987; Heide-Jørgensen et al., 2002, factor for missed animals of 2.0 that ice (summer) period in the Bering Sea 2013; Laidre and Heide-Jørgensen, has no associated CV. The average an- from 1979 to 2013. In contrast, they 2005). nual subsistence removal for the past found that the duration of the reduced There have been three studies that 10 years (191) is below this calculat- ice period increased by 44 days in the specifically address the potential in- ed PBR; if struck and lost is consid- Chukchi Sea and 52 days in the Beau- fluence of changes in ice conditions ered, total annual removals would be fort Sea over the same period. These on western Alaska belugas. O’Corry- 215, or 7% above PBR. However, the data suggest that ECS belugas are Crowe et al. (2016) analyzed long- abundance estimate is thought to be more susceptible to possible impacts term sighting and genetic data on low because the survey did not include of sea ice change, while EBS and BB belugas in the Bering, Chukchi, and all potential beluga habitat (e.g., the belugas may be less at risk. However, Beaufort seas in conjunction with Yukon River itself), dark gray animals we note that ABWC members who multi-decadal patterns of sea ice to (calves) were particularly hard to see live and hunt in these regions report investigate the influence of sea ice on in muddy water coming from the Yu- that Bering Sea ice has formed later, spring migration and summer residen- kon, and the analysis did not account melted earlier, and not been as thick as cy patterns. Although substantial vari- for all aspects of perception bias. Re- in previous decades. They also report ations in sea ice conditions were found gardless of the uncertainty in the esti- that, since 2013, some areas have re- across seasons, years, and sub-regions, mate of abundance and PBR, that the mained ice free through the winter and the pattern of beluga migration and harvest is approximately equal to PBR in other areas there has been extreme- residency was quite consistent. Those is of concern and the ABWC request- ly rapid retreat of ice in the spring results suggest that belugas can ac- ed that NOAA conduct line-transect (ABWC22). commodate some changes to sea ice surveys on a regular basis. Although Belugas do not occur in regions conditions and will return to tradition- coastal fisheries are not regularly mon- without at least seasonal sea ice sug- ally used areas. However, they also itored for incidental take of belugas, gesting a strong, if not obligate, observed anomalous movement pat- all indications are that takes of belu- connection. However, some subpopu- terns that coincided with years with gas from this stock are very infrequent lations spend many months far from anomalously low sea ice coverage, and (Muto et al., 2018). ice while others spend most of their in one case with an increase in killer time in or near ice of concentrations whale sightings and predation on be- Eastern Chukchi Sea up to 90%, indicating substantial flex- lugas, indicating that behavioral shifts In the 2017 SAR (Muto et al., ibility in the species as a whole (Haus- may be driven by changing sea-ice and 2018), data provided in Lowry et al. er et al., 2017). Belugas that occupy associated changes in resource disper- (2017b) were used to estimate PBR ice covered areas may do so for feed- sion and predation risk. Hauser et al. for the ECS stock as follows: NBEST ing on abundant ice-associated spe- (2016) compared the timing of the au- = 20,752; CV = 0.70; NMIN = 12,194, cies, such as arctic cod, Boreogadus tumn migration of ECS and Beaufort RMAX = 0.04; FR = 1.0; PBR = 244. saida (Loseto et al., 2009; Hauser et Sea belugas during the periods 1993– Using RMAX = 0.048 we estimate PBR al., 2015). Changes in the distribution 2002 and 2004–12. They found that, in as 293. The average annual Alaska Na- and characteristics of sea ice will re- the later period, ECS beluga migration tive subsistence harvest from the ECS sult in changes in productivity and in during autumn from the Beaufort and stock for the last 10 years (57 belugas) the types and abundance of prey spe- Chukchi seas was delayed by 2 to > 4

81(3–4) 67 weeks, but that Beaufort Sea belugas stomach contents from harvested belu- salmon and less than 5% of the smolt did not shift migration timing between gas, Quakenbush et al. (2015) found a outmigration. periods. Hauser et al. (2018) applied minimum of 14 species of fish and in- Belugas that summer in the Yukon resource selection models to move- vertebrates from BB belugas, 22 spe- Delta region also feed on Pacific salm- ments of ECS and Beaufort Sea belu- cies from EBS belugas, and 15 species on. This is a large stock of whales that gas during 1990–2014 and found that, from ECS belugas. Belugas clearly may consume a substantial portion of although sea ice has declined, belugas show flexibility and adaptive capacity some Yukon River salmon runs, there- are generally found in the same loca- making it particularly difficult to pre- by potentially impacting catches in tions and speculated that bathymetric dict how they will be affected by cli- commercial and subsistence fisheries features were better predictors of sum- mate change. and the trophic structure of the ecosys- mer habitat use than sea ice concentra- tem (Lowry et al., 2017a). tion. Hauser et al. (2018) also found Fishery Interactions that ECS belugas were making longer, No incidental mortalities or in- Industrial Activities deeper dives in recent years and spec- juries to belugas were reported by An increase in the duration of the ulated that this might be due to chang- fishery observers that monitored the open water season and the decline es in sea ice concentration. groundfish trawl, longline, and pot in multi-year sea ice have generated A long-term study of belugas off fisheries off western Alaska during concern that increases in oil and gas West Greenland found that belugas re- 1990–97 (Muto et al., 2016) and only exploration and development, and sponded to changing sea ice by shifting one was reported during 2011–2015 shipping may have negative conse- their distribution and that abundance (Muto et al., 2018). Other observa- quences for belugas (Reeves et al., increased during a period of generally tions show that belugas have been 2014). Most oil and gas activity within declining ice cover (Heide-Jørgensen caught in commercial and subsistence the range of western Alaska belugas et al., 2010). The authors concluded salmon fisheries that occur along the currently occurs over the continental that “Global warming and sea-ice de- coast, but overall there are no reliable shelf in the Beaufort Sea, although clines may pose less of a problem for data on incidental take. Although be- from 2006 to 2015 there was also con- belugas than to other Arctic marine luga mortalities due to fisheries occur siderable activity in the Chukchi Sea. mammals.” Laidre et al. (2008) also in Bristol Bay, they did not prevent In the Beaufort Sea, the distribution of concluded that, on a range-wide basis, population growth between 1993 and ECS belugas is predominantly limited the beluga would be the Arctic ceta- 2005 (Lowry et al., 2008). We suspect to offshore areas, near the continental cean least sensitive to climate change that unless there is a major change in shelf break and in the Arctic Basin. because of their wide distribution, di- how or where commercial gillnet fish- At present, oil and gas activity in the verse diet, and flexible habits. eries occur, these fisheries will not be Alaska portion of the Beaufort Sea It is possible that climate warm- a threat to the long-term sustainabil- is far inshore of where belugas typi- ing may have effects on belugas be- ity of belugas. Nevertheless, monitor- cally range (Suydam et al.25). In 2016, yond those linked to changes in sea ing levels of bycatch in commercial most of Bristol Bay and the U.S. por- ice. Specific annual summering areas and subsistence gillnet fisheries is tion of the Chukchi Sea were removed likely have particularly suitable envi- warranted. from future leasing by Presidential ronmental conditions such as water In Bristol Bay, belugas feed on order, but that order was rescinded in temperature and substrate. Those areas salmon when they are available. They 2018. Also, there are still active oil may be important for feeding, molt- feed both on smolt migrating out of and gas lease areas in Alaska’s Beau- ing, calving, and avoidance of killer river systems and on adults returning fort Sea and in the Russian portion of whales (Frost and Lowry, 1990; Laidre to the rivers to spawn (Brooks et al.1). the Chukchi Sea, so impacts from oil et al., 2008). Little attention has been Because salmon runs were severely spills and shipping activity are still given to measuring the specific fea- depressed in Bristol Bay in the 1950’s, possible in those areas. tures of these areas or projecting how an effort was made to deter belugas Although shipping is increasing those features may change with cli- from river mouths by playing under- with declining sea ice (Eguíluz et al., mate warming. Warmer water may al- water sounds recorded from killer 2016; Pizzolato et al., 2016), belugas low the expansion of new prey species whales (Fish and Vania, 1971). Effica- are not known to be susceptible to into the belugas’ range or cause tradi- cy of this effort was equivocal, and the ship strikes, even in congested areas tionally used prey to move elsewhere. “beluga spooker” program ended after such as the St. Lawrence River (King- Although some beluga stocks may 1978. In the early 1980’s after salmon focus on certain prey, such as Arctic runs had largely recovered, Frost et 25 12 Suydam, R. S., L. F. Lowry, and K. J. Frost. cod or Pacific salmon, belugas are ca- al. conducted additional studies in 2005. Distribution and movements of beluga pable of consuming a wide variety of Bristol Bay and concluded that beluga whales from the eastern Chukchi Sea stock during summer and early autumn. Final report prey and are best classified as gener- predation was equal to less than 1% of to Coastal Marine Institute, Univ. Alaska, Fair- alist predators. In their examination of the commercial catch of adult sockeye banks, AK, 39 p.

68 Marine Fisheries Review sley, 2002). Furthermore, factors in primary summer range of any beluga threats to persistence of western Alas- addition to sea ice, such as where re- stock, EBS belugas are known to fre- ka beluga stocks, although climate sources are being developed and com- quent the area in winter. The Donlin warming, declines in sea ice, and in- modity pricing, determine shipping Mine has been granted federal permits dustrial activities related to resource trends (Brigham, 2011; Bensassi et al., but is still acquiring state permits. development are of concern and could 2016; Pizzolato et al., 2016). As such, pose challenges in the future. predicting how patterns in shipping Conclusions will change is difficult, as is how belu- The BB beluga stock is relatively Acknowledgments gas will respond to those changes. small (approximately 2,000 animals), The authors acknowledge and thank Impacts to belugas in the far north but its abundance and trend are peri- the Alaska Beluga Whale Commit- from noise associated with shipping, odically monitored and the stock ap- tee and the beluga hunters of western including icebreaking (e.g., Finley et pears to have increased between 1993 Alaska without whom much of the al., 1990), or other industrial activities, and 2005, and may now be stable. The progress that has been made in under- may be more of a concern than ship most conservative estimate of PBR for standing beluga biology and manage- strikes. Studies suggest that belugas this stock (39) is more than the aver- ment concerns would not have been may avoid sources of noise (e.g., Fin- age annual Alaska Native subsistence possible. Most of our studies have ley et al., 1990) or change their behav- harvest over the last decade (23). Al- been funded by the Outer Continen- ior in response to noise, by increasing though there is little information re- tal Shelf Environmental Assessment swim speed, making longer dives, or garding incidental take or struck and Program, the U.S. Minerals Manage- foraging less (e.g., Blane and Jaakson, lost rates, the population has increased ment Service (now the U.S. Bureau 1994; Kendall and Cornick, 2015). in recent decades, suggesting that all of Ocean Energy Management), and However, other studies suggest that sources of mortality have not been sig- NOAA. Other substantial support has belugas may habituate to anthropogen- nificant (Lowry et al., 2008). been provided by the North Slope Bor- ic noise or fishing boats (e.g., Fish and The EBS beluga stock is quite large, ough Department of Wildlife Manage- Vania, 1971). The population-level im- and aggregates off the mouths of the ment, the Alaska Department of Fish pacts of noise and shipping are poor- Yukon River and in Norton Sound ev- and Game, and the Bristol Bay Native ly understood and what these studies, ery June. The most recent abundance Association. We thank our numerous conducted in places such as Cook Inlet estimate of over 9,000 is based on data colleagues and friends, both traditional (Kendall and Cornick, 2015) or the St. collected in 2017 and relies on an ar- scientists and indigenous biologists, Lawrence Estuary (Blane and Jaakson, bitrary correction factor to account for 1994), may mean for belugas in Arctic availability bias. Additional work (e.g., who have collaborated and assisted us shipping lanes is unclear. Dedicated SDR tagging) is needed to develop in our efforts to study and conserve studies are needed to investigate how better correction factors. The average beluga whales. Megan Ferguson pro- belugas will respond to anthropogenic annual reported subsistence harvest vided Figure 8 and the data necessary noise in Arctic shipping lanes. (191) does not exceed PBR calcu- for Figure 5. Donna Hauser and Janet There are currently two proposed lated from this abundance estimate Clarke provided Figures 6 and 9, re- mines in southwestern Alaska that (201) however when struck and lost spectively. Much of the material con- have the potential to affect beluga estimates are included it does. While tained in this paper was prepared as habitat. A large copper, gold, and mo- available scientific data do not allow background for the “Global Review lybdenum mine, known as the Pebble an estimation of population trend, lo- of Monodontids” held 13–16 March Mine, is proposed for the headwaters cal and traditional knowledge indicate 2017 at Hillerød, Denmark, and con- of the Nushagak and Kvichak rivers, that there has not been a noticeable vened by the North Atlantic Marine which flow into bays that are the pri- decrease in abundance or availabil- Mammal Commission. mary summer habitat of the BB beluga ity of EBS belugas in recent years Literature Cited stock. This mine would process ore us- (ABWC22). Adams, M., K. J. Frost, and L. Harwood. 1993. ing a cyanide solution and would pro- The ECS beluga stock is large, es- Alaska and Inuvialuit Beluga Whale Com- duce effluents that would be toxic to timated as approximately 20,000 belu- mittee (AIBWC)—an initiative in “at home fish and other organisms if leaked into gas (Lowry et al., 2017b). The average management”. Arctic 46:134–137. Bensassi, S., J. C. Stroeve, I. Martínez-Zarzoso, the river systems. The Final Environ- annual subsistence harvest (57) is well and A. P. Barrett. 2016. Melting ice, growing mental Impact Statement is due to be below PBR (293). ECS belugas are not trade? Elementa: Science of the Anthropo- released by the Army Corp of Engi- at immediate risk from anthropogenic cene 4:000107 (doi: https://doi.org/10.12952/ journal.elementa.000107). neers in summer 2020. The other no- activities or climate change, however, Blane, J., and R. Jaakson. 1994. The impact of table mine, the Donlin Mine, is in the additional monitoring of population ecotourism boats on the St. Lawrence beluga Kuskokwim River drainage and poses size and trend, subsistence harvest, whales. Environ. Cons. 21:267–269. Brigham, L. 2011. Marine protection in the Arc- similar risks to fisheries. Although and health of belugas is warranted. tic cannot wait. Nature 478:157. (doi: https:// Kuskokwim Bay does not contain the There are currently few identified doi.org/10.1038/478157a).

81(3–4) 69 Brodie, P. F. 1971. A reconsideration of aspects Fish, J. F., and J. S. Vania. 1971. Killer whale, Baffin Island. Polar Biol. 25:331–341 (doi: of growth, reproduction, and behavior of the Orcinus orca, sounds repel white whales, Del- https://doi.org/10.1007/s00300-001-0347-6). white whale with reference to the Cumber- phinapterus leucas. Fish. Bull. 69:531–535. ______, K. Laidre, D. Borchers, T. land Sound, Baffin Island, population. J. Fish. Foote, D. C., and H. A. Williamson. 1966. A Marques, H. Stern, and M. Simon. 2010. Res. Board Can. 28:1,309–1,318. human geographical study. In N. J. Wili- The effect of sea-ice loss on beluga whales Brown Gladden, J. G., M. M. Ferguson, and J. movsky and J. N. Wolfe (Editors), The En- (Delphinapterus leucas) in West Greenland. W. Clayton 1997. Matriarchal genetic popu- vironment of the Cape Thompson region, p. Polar Res. 29:198–208 (doi: https://doi. lation structure of North American beluga 1,041–1,107. U.S. Atomic Energy Comm. org/10.1111/j.1751-8369.2009.00142.x). whales (Delphinapterus Ieucas Cetacea: Oak Ridge, Tenn. ______, R. G. Hansen, K. Westdal, R. R. Monodontidae). Mol. Ecol. 6:1,033–1,046. Frost, K. J., and L. F. Lowry. 1990. Distribution, Reeves, and A. Mosbech. 2013. Narwhals ______, ______, M. K. Friesen, and abundance, and movements of beluga whales, and seismic exploration: Is seismic noise in- J. W. Clayton. 1999. Population structure of Dephinapterus leucas, in coastal waters of creasing the risk of ice entrapments? Biol. North American beluga whales (Delphin- western Alaska. Can. Bull. Fish. Aquatic Sci. Conserv. 158:50–54 (doi: https://doi. apterus leucas) based on nuclear DNA mic- 224:39–57. org/10.1016/j.biocon.2012.08.005). rosatellite variation and contrasted with the ______and R. S. Suydam. 2010. Subsis- Higdon, J. W., and S. H. Ferguson. 2009. Loss of population structure revealed by mitochon- tence harvest of beluga or white whales (Del- Arctic sea ice causing punctuated change in drial DNA variation. Mol. Ecol. 8:347–369. phinapterus leucas) in northern and western sightings of killer whales (Orcinus orca) over Citta, J. J., R. S. Suydam, L. T. Quakenbush, K. Alaska, 1987–2006. J. Cetacean Res. Ma- the past century. Ecol. Appl. 19:1,365–1,375. J. Frost, and G. M. O’Corry-Crowe. 2013. nage. 11(3):293–299. Huntington, H. P., and the communities of Buck- Dive behavior of eastern Chukchi beluga ______, L. F. Lowry, and R. R. Nel- land, Elim, Koyuk, Point Lay, and Shaktoolik. whales (Delphinapterus leucas), 1998–2008. son. 1985. Radiotagging studies of belukha 1999. Traditional knowledge of the ecology Arctic 66(4):389–406. whales (Delphinapterus leucas) in Bristol of beluga whales (Delphinapterus leucas) ______, L. T. Quakenbush, K. J. Frost, L. Bay, Alaska. Mar. Mammal Sci. 1:191–202. in the eastern Chukchi and northern Bering Lowry, R. C. Hobbs and H. Aderman. 2016. ______, R. B. Russell, and L. F. Lowry. Seas, Alaska. Arctic 52:49–61. Movements of beluga whales (Delphinaptrus 1992. Killer whales, Orcinus orca, in the Kendall, L. S., and L. A. Cornick. 2015. Be- leucas) in Bristol Bay, Alaska. Mar. Mam- southeastern Bering Sea: recent sightings and havior and distribution of Cook Inlet beluga mal Sci. 32:1,272–1,298 (doi: https://doi. predation on other marine mammals. Mar. whales, Delphinaterus leucas, before and org/10.1111/mms.12337). Mammal Sci. 8:110–119. during pile driving activity. Mar. Fish. Rev. ______, P. Richard, L. F. Lowry, G. ______, L. F. Lowry, and G. Carroll. 1993. 77(2):106–114 (doi: https://doi.org/10.7755/ O’Corry-Crowe, M. Marcoux, R. Suydam, Beluga whale and spotted seal use of a coast- MFR.77.2.6). L.T. Quakenbush, R. C. Hobbs, D. I. Litovka, al lagoon system in the northeastern Chuk- Kingsley, M. C. S. 2002. Status of the belugas K. J. Frost, and T. Gray. 2017. Satellite telem- chi Sea. Arctic 46(1):8–16 (doi: https://doi. of the St. Lawrence Island estuary, Canada. etry reveals population specific winter rang- org/10.14430/arctic1316). In M. P. Heide-Jørgensen and Ø. Wigg (Edi- es of beluga whales in the Bering Sea. Mar. Haug, T., B. Bogstad, M. Chierici, H. Gjøsæter, tors), Belugas in the North Atlantic and the Mammal Sci. 33(1):236–250. E. H. Hallfredsson, Å. S. Høines, A. H. Hoel, Russian Arctic, p. 239–257. NAMMCO Sci. ______, G. O’Corry Crowe, L. T. Quak- R. B. Ingvaldsen, L. L. Jørgensen, T. Knutsen, Publ. No. 4. enbush, A. L. Bryan, T. Ferrer, R. C. Hobbs, and H. Loeng. 2017. Future harvest of living Laidre, K. L., and M. P. Heide-Jørgensen. 2005. resources in the Arctic Ocean north of the Arctic sea ice trends and narwhal vulner- and M. J. Olsen. 2018. Assessing the abun- Nordic and Barents Seas: a review of possi- ability. Biol. Conserv. 121(4):509–517 (doi: dance of Bristol Bay belugas with genetic bilities and constraints. Fish. Res.188:38–57. https://doi.org/10.1016/j.biocon.2004.06. mark-recapture methods. Mar. Mammal Sci. Hauser, D. D. W., K. L. Laidre, R. S. Suydam, 003). 34:666–686. and P. R. Richard. 2014. Population-specific ______, I. Stirling, L. Lowry, Ø. Wiig, M. ______, K. J. Frost, and L. Quakenbush. home ranges and migration timing of Pacific P. Heide-Jørgensen, and S. Ferguson. 2008. 2019. Aerial surveys of Bristol Bay beluga Arctic beluga whales (Delphinapterus leu- Quantifying the sensitivity of arctic marine whales, Delphinapterus leucas, in 2016. Mar. cas). Polar Biol. 37:1,171–1,183. mammals to climate-induced habitat change. Fish. Rev. 81(3–4):98–104 (doi:https://doi. ______, ______, S. L. Parker-Stetter, J. Ecol. Appl. 18(2):S97–S125 (doi: https://doi. org/10.7755/MFR.81.3-4.5). K. Horne, R. S. Suydam, and P. R. Richard. org/10.1890/06-0546.1). Clarke, J. T., and M. C. Ferguson. 2018. Bow- 2015. Regional diving behavior of Pacific ______, H. Stern, K. M. Kovacs, L. Lowry, head whale and beluga distributions, sighting Arctic beluga whales Delphinapterus leucas S. E. Moore, E. V. Regehr, S. H. Ferguson, Ø. rates, and habitat associations in the western and possible associations with prey. Mar. Wiig, P. Boveng, R. P. Angliss, E. W. Born, Beaufort Sea, summer and fall 2009–2016, Ecol. Prog. Ser. 541:245–264 (doi: https:// D., Litovka, L. Quakenbush, C. Lydersen, D. with a retrospective comparison to 1982– doi.org/10.3354/meps11530). Vongraven, and F. Ugarte. 2015. Arctic ma- 1991. Arctic 71(2):115–138. ______, ______, K. M. Stafford, H. L. rine mammal population status, sea ice habi- Eguíluz, V. M., J. Fernández-Gracia, X. Irigoien, Stern, R. S. Suydam, and P. R. Richard. 2016. tat loss, and conservation recommendations and C. M. Duarte. 2016. A quantitative as- Decadal shifts in autumn migration timing for the 21st century. Conserv. Biol. 29:724– sessment of Arctic shipping in 2010–2014. by Pacific Arctic beluga whales are related 737 (doi: https://doi.org/10.1111/cobi.12474). Nature 6:30682 (doi: https://doi.org/10.1038/ to delayed annual sea ice formation. Global Loseto, L. L., G. A. Stern, T. L. Connelly, D. srep30682). Change Biol. 23:2,206–2,217 (doi: https:// Deibel, B. Gemmill, A. Prokopowcz, L. Forti- Ferguson, S. H., J. W. Higdon, and E. G. Chmel- doi.org/10.1111/gcb.13564). er, and S. H. Ferguson. 2009. Summer diet of nitsky. 2010. The rise of killer whales as a ______, ______, H. L. Stern, S. E. belgua whales inferred by fatty acid analysis major Arctic predator. In S. H. Ferguson, L. Moore, R. S. Suydam, and P. R. Richard. of the eastern Beaufort Sea food web. J. Ex- L. Loseto, and M. L. Mallory (Editors), A 2017. Habitat selection by two beluga whale perimental Mar. Biol. Ecol. 374:12–18 (doi: little less Arctic: top predators in the world’s populations in the Chukchi and Beaufort seas. https://doi.org/10.1016/j.jembe.2009.03.015). largest northern inland sea, Hudson Bay, p. PloS ONE 12(2):p.e0172755 (doi: https://doi. Lowry, L. F., J. J. Burns, and R. R. Nelson. 117–136. Springer, Netherl. org/10.1371/journal.pone.0172755). 1987. Polar bear predation on beluga whales Fernandez-Gimenez, M. E., H. P. Huntington, ______, ______, ______, R. S. in the Bering and Chukchi seas. Can. Field- and K. J. Frost. 2006. Integration or co-op- Suydam, and P. R. Richard. 2018. Indirect ef- Nat. 101:141–146 tation? Traditional knowledge and science in fects of sea ice loss on summer–fall habitat ______, K. J. Frost, A. Zerbini, D. DeMas- the Alaska Beluga Whale Committee. Envi- and behaviour for sympatric populations of ter, and R. R. Reeves. 2008. Trend in aerial ron. Conserv. 33:1–10. an Arctic marine predator. Diversity Distrib. counts of beluga or white whales (Delphin- Finley, K. J., G. W. Miller, R. A. Davis, and C. 24:791–799 (doi: https://doi.org/10.1111/ apterus leucas) in Bristol Bay, Alaska, 1993– R. Greene. 1990. Reactions of belugas, Del- ddi.12722). 2005. J. Cetacean Res. Manage. 10:201–207. phinapterus leucas, and narwhals, Monodon Heide-Jørgensen, M. P., R. Dietz, K. Laidre, and ______, A. Zerbini, K. J. Frost, D. P. De- monoceros, to ice-breaking ships in the Cana- P. Richard. 2002. Autumn movements, home Master, and R. C. Hobbs. 2017a. Develop- dian high Arctic. Can. Bull. Fish. Aquat. Sci. ranges, and winter density of narwhals (Mon- ment of an abundance estimate for the eastern 224:97–117. odon monoceros) tagged in Tremblay Sound, Bering Sea stock of beluga whales (Delphin-

70 Marine Fisheries Review apterus leucas). J. Cetacean Res. Manage. Serv., U.S. Army, Wash., D.C., 337 p. (doi: Reeves, R. R., R. L. Brownell, Jr., V. Burkanov, 16:39–47. https://doi.org/10.5962/bhl.title.7334). M. C. S. Kingsley, L. F. Lowry, and B. Tay- ______, M. C. S. Kingsley, D. D. W. Haus- O’Corry-Crowe, G. M., and L. F. Lowry. 1997. lor. 2011. Sustainability assessment of beluga er, J. Clarke, and R. Suydam. 2017b. Aerial Genetic ecology and management concerns (Delphinapterus leucas) live-capture remov- survey estimates of abundance of the east- of the beluga whale (Delphinapterus leucas, als in the Sakhalin-Amur region, Okhoska ern Chukchi Sea stock of beluga whales Pallas, 1776). In A. E. Dizon, S. J. Chivers, Sea, Russia. Rep. Indep. Rev. Panel. Occa- (Delphinapterus leucas) in 2012. Arctic and W. F. Perrin (Editors), Molecular genetics sional Pap. Spec. Surv. Commiss. 44, IUCN, 70(3):273–286. of marine mammals, p. 249–274. Soc. Mar. Gland, Switzerland, 34 p. Meschersky, I. G., M. V. Kholodova, and E.Yu. Mammal. Spec. Publ. No. 3. ______, P. J. Ewins, S. Agbayani, M. P. Zvychaynaya. 2008. Molecular genetic study ______, R. S. Suydam, A. Rosenberg, Heide-Jørgensen, K. M. Kovacs, C. Ly- of the beluga (Delphinapterus leucas: Ceta- K. J. Frost, and A. E. Dizon. 1997. Phy- dersen, R. Suydam, W. Elliott, G. Polet, Y. cea, Monodontidae) summering in the south- logeography, population structure and van Dijk, and R. Blijleven. 2014. Distribu- ern Sea of Okhotsk as compared to North dispersal patterns of the beluga whale Del- tion of endemic cetaceans in relation to hy- American populations. Russ. J. Genetics phinapterus leucas in the western Ne- drocarbon development and commercial 44(9):1105–1110. arctic revealed by mitochondrial DNA. shipping in a warming Arctic. Mar. Poli- ______, O. V. Shpak, D. I. Litovka, D. Mol. Ecol. 6:955–970 (doi: https://doi. cy 44:375–389 (https://doi.org/10.1016/j. M. Glazov, E. A. Borlsova, and V. V. Rozh- org/10.1046/j.1365-294X.1997.00267.x). marpol.2013.10.005). nov. 2013. A genetic analysis of the beluga ______, A. E. Dizon, R. S. Suydam, and L. Stafford, K. M., M. C. Ferguson, D. D. W. Haus- whale Delphinapterus leucas (Cetacea: Mon- F. Lowry. 2002. Molecular genetic studies of er, S. R. Okkonen, C. L. Berchok, J. J. Citta, odontidae) from summer aggregations in population structure and movement patterns J. T. Clarke, E. C. Garland, J. Jones, and R. S. the Russian Far East. Russian J. Mar. Biol. in a migratory species: the beluga whale, Suydam. 2018. Beluga whales in the western 39(2):125–135 (doi: https://doi.org/10.1134/ Delphinapterus leucas, in the Western Nearc- Beaufort Sea: Current state of knowledge on S1063074013020065). tic. In C. J. Pfeiffer (Editor), Molecular and timing, distribution, habitat use and environ- Muto, M. M., V. T. Helker, R. P. Angliss, B. A. cell biology of marine mammals p. 53–63. mental drivers. Deep Sea Research II: Topical Allen, P. L. Boveng, J. M. Breiwick, M. F. Krieger Publ. Co., Malabar, Fla. Studies in Oceanography 152:182–194 (doi: Cameron, P. J. Clapham, S. P. Dahle, M. E. ______, A. R. Mahoney, R. Suydam, L. https://doi.org/10.1016/j.dsr2.2016.11.017). Dahlheim, B. S. Fadely, M. C. Ferguson, L. W. Fritz, R. C. Hobbs, Y. V. Ivashchenko, Quakenbush, A. Whiting, L. Lowry, and Suydam, R. S. 2009. Age, growth, reproduc- A. S. Kennedy, J. M. London, S. A. Miz- L. Harwood. 2016. Genetic profiling links tion, and movements of beluga whales (Del- roch, R. R. Ream, E. L. Richmond, K. E. changing sea-ice to shifting beluga migra- phinapterus leucas) from the eastern Chukchi W. Shelden, R. G. Towell, P. R. Wade, J. M. tion patterns. Biol. Lett. 12:20160404 (doi: Sea. PhD thesis, Univ. of Wash., Seattle, 152 https://doi.org/10.1098/rsbl.2016.0404). p. Waite, and A. N. Zerbini. 2016. Alaska marine mammal stock assessments, 2015. U.S. ______, R. Suydam, L. Quakenbush, B. ______, L. F. Lowry, K. J. Frost, G. M. Dep. Commer., NOAA Tech. Memo. NMFS- Potgieter, L. Harwood, D. Litovka, T. Fer- O’Corry-Crowe, and D. Pikok, Jr. 2001. Sat- AFSC-323, 300 p. (doi: https://doi.org/10. rer, J. Citta, V. Burkanov, K. Frost, and B. ellite tracking of eastern Chukchi Sea be- 7289/V5/TM-AFSC-323). Mahoney. 2018. Migratory culture, popula- luga whales into the Arctic Ocean. Arctic ______, ______, ______, tion structure and stock identity in North Pa- 54(3):237–243. ______, ______, ______, cific beluga whales (Delphinapterus leucas). Wade, P. R. 1998. Calculating limits to the allow- ______, ______, ______, PloS ONE 13(3):e0194201 (doi: https://doi. able human-caused mortality of cetaceans and ______, ______, ______, org/10.1371/journal.pone.0194201). pinnipeds. Mar. Mammal Sci. 14:1–37 (doi: ______, ______, ______, Pizzolato, L., S. E. L. Howell, J. Dawson, F. https://doi.org/10.1111/j.1748-7692.1998. ______, ______, ______, Laliberte, and L. Copland. 2016. The influ- tb00688.x). ______, ______, ______, ence of declining sea ice on shipping activ- ______and R. Angliss. 1997. Guidelines ______, ______, ______, and ity in the Canadian Arctic. Geophy. Res. for assessing marine mammal stocks: report ______. 2018. Alaska marine mammal Lett. 43:12,146–12,154 (doi: https://doi. of the GAMMS workshop April 3–5, 1996, stock assessments, 2017. U.S. Dep. Commer., org/10.1002/2016GL071489). Seattle, Washington. U.S. Dep. Commer., NOAA Tech. Memo. NMFS-AFSC-378, Quakenbush, L. T., R. S. Suydam, A. L. Bryan, NOAA Tech. Memo. NMFS-OPR-12, 93 p. 382 p. (doi: https://doi.org/10.7289/V5/TM- L. F. Lowry, K. J. Frost, and B. A. Mahoney. Zagoskin, L. A. 1967. Lieutenant Zagoskin’s AFSC-378). 2015. Diet of beluga whales (Delphinapter- travels in Russian America, 1842–1844. In Nelson, E. W. 1887. Report upon natural history us leucas) in Alaska from stomach contents, H. N. Michael (Editor), Anthropology of the collections made in Alaska between the years March–November. Mar. Fish. Rev. 77:70–84 North: Translations from Russian Sources 7, 1887 and 1881. Arctic Ser. Publ. 3, Signal (doi: https://doi.org/10.7755/MFR.77.1.7). Univ. of Toronto Press, Canada, 358 p.

81(3–4) 71