Genetic history and stock identity of beluga whales in Kotzebue Sound

  • Gregory O'Corry-Crowe Harbor Branch Oceanographic Institute, Florida Atlantic University, Fort Pierce, FL, USA
  • Tatiana Ferrer Harbor Branch Oceanographic Institute, Florida Atlantic University, Fort Pierce, FL, USA
  • John J. Citta Alaska Department of Fish and Game, Fairbanks, AK, USA
  • Robert Suydam North Slope Borough Department of Wildlife Management, Utqiaġvik, AK, USA
  • Lori Quakenbush Alaska Department of Fish and Game, Fairbanks, AK, USA
  • John J. Burns Living Resources Inc., Fairbanks, AK, USA
  • Jorge Monroy Harbor Branch Oceanographic Institute, Florida Atlantic University, Fort Pierce, FL, USA
  • Alex Whiting Native Village of Kotzebue, Kotzebue, AK, USA
  • Glenn Seaman Seaman Consulting, Homer, AK, USA
  • Willie Goodwin, Sr. Alaska Beluga Whale Committee, Kotzebue, AK, USA
  • Matthias Meyer Max Planck Institute for Evolutionary Anthropology, Leipzig, Germany
  • Sarah Rodgers Harbor Branch Oceanographic Institute, Florida Atlantic University, Fort Pierce, FL, USA
  • Kathryn J. Frost Alaska Beluga Whale Committee, Kailua-Kona, HI, USA
Keywords: population decline, ancient DNA, Delphinapterus leucas, Indigenous Knowledge, Iñupiat, migratory culture

Abstract

We investigate the recent history and stock identity of beluga whales (Delphinapterus leucas) in Kotzebue Sound in the Chukchi Sea, a region long frequented by large numbers of belugas in summer until their near disappearance in the 1980s. Wide variation in numbers since then suggests a complex recent history that hinders recovery efforts. Analysis of teeth sampled during the historical (pre-decline) era using ancient DNA (aDNA) methods found that the original Kotzebue Sound whales were differentiated for mitochondrial DNA (mtDNA) from other summering concentrations across the Pacific Arctic revealing a demographically distinct subpopulation where long-established migratory culture likely facilitated population divergence. Analysis of microsatellite (nDNA) and mtDNA markers in belugas from the contemporary (post-decline) era revealed that whales from other stocks likely visited Kotzebue Sound, including during two low ice years when relatively large numbers of whales were present. Some mtDNA lineages were found only in Kotzebue Sound, with one recorded in both the historical and contemporary eras. Exclusion tests found a number of whales in Kotzebue Sound during the contemporary era that had nDNA genotypes unlikely to arise in other contemporary stocks in the Pacific Arctic. Our findings indicate that the Kotzebue Sound belugas comprised a unique stock of which a few remnants likely still co-occur with belugas from other larger stocks. We recommend that the US government work through the co-management process to greatly reduce or eliminate the taking of belugas, especially adult females, likely to belong to the Kotzebue Sound stock, until they recover.

Downloads

Download data is not yet available.

References


Avise J.C. 1995. Mitochondrial DNA polymorphism and a connection between genetics and demography of relevance to conservation. Conservation Biology 9, 686-690, doi: 10.1046/j.1523-1739.1995.09030686.x.


Banks M.A. & Eichert W. 2000. WHICHRUN V4.1: a computer program for population assignment of individuals based on multilocus genotype data. Journal of Heredity 91, 88–89, doi: 10.1093/jhered/91.1.87.


Burch E.S. 1998. The Iñupiaq Eskimo nations of northwest Alaska. Fairbanks: University of Alaska Press.


Burns J.J. & Seaman G.A. 1986. Investigations of belukha whales in coastal waters of western and northern Alaska. II: biology and ecology. Final report. Juneau, AK: Outer Continental Shelf Environmental Assessment Program.


Caron L.M.J. & Smith T.G. 1990. Philopatry and site tenacity of belugas, Delphinapterus leucas, hunted by the Inuit at the Nastapoka estuary, eastern Hudson Bay. Canadian Bulletin of Fisheries and Aquatic Sciences 224, 69–79.


Castellote M., Stafford K. & Small R.J. 2017. Acoustic monitoring of cetaceans in Kotzebue Sound: 2014–2017. Final report submitted to the ABWC, Aug 2017. Unpublished report.


Citta J.J., O’Corry-Crowe G., Quakenbush L.T., Bryan A.L., Ferrer T., Olson M.J., Hobbs R.C., & Potgieter B. 2018. Assessing the abundance of Bristol Bay belugas with genetic mark–recapture methods. Marine Mammal Science 34, 666–686, doi: 10.1111/mms.12472.


Citta J.J., Richard P., Lowry L.F., O’Corry-Crowe G., Marcoux M., Suydam R., Quakenbush L.T., Hobbs R.C., Litovka D.I., Frost K.J., Gray T., Orr J., Tinker B., Aderman H. & Druckenmiller M.L. 2016. Satellite telemetry reveals population specific winter ranges of beluga whales in the Bering Sea. Marine Mammal Science 33, 236–250, doi: 10.1111/mms.12357.


COSEWIC (Committee on the Status of Endangered Wildlife in Canada) 2004. COSEWIC assessment and update status report on the beluga whale Delphinapterus leucas in Canada. Ottawa: Committee on the Status of Endangered Wildlife in Canada.


DFO (Fisheries and Oceans Canada) 2018. Harvest advice for eastern and western Hudson Bay beluga (Delphinapterus leucas). DFO Canadian Science Advisory Secretariat Science Advisory Report 2018/008. Ottawa: Fisheries and Oceans Canada.


Excoffier L. & Lischer H. 2015. Arlequin V3.5; an integrated software package for population genetics data analysis. Bern: University of Bern.


Fejes C. 1966. People of the Noatak. New York: Alfred A. Knopf.


Foote A.C. & Cooke D.C. 1960. The Eskimo hunter of Noatak, Alaska. Winter 1960. Summer 1960. Washington, D.C.: US Atomic Energy Commission.


Foote A.C. & Williamson H.A. 1966. A human geographical study. In N.J. Wilimovsky & J.N. Wolfe (eds.): Environment of the Cape Thompson region, Alaska. Pp. 1041–1107. Oak Ridge, TN: US Atomic Energy Commission.


Frost K.J., Gray T., Goodwin W. Sr., Schaeffer R. & Suydam R. 2021. Alaska Beluga Whale Committee—a unique model of co-management. Polar Research 40, article no. 5611, doi: 10.33265/polar.v40.5611.


Frost K.J. & Lowry L.F. 1990. Distribution, abundance, and movements of beluga whales, Delphinapterus leucas, in coastal waters of western Alaska. Canadian Bulletin of Fisheries and Aquatic Sciences 224, 39–57.


Giddings J.L. & Anderson D.A. 1986. Beach ridge archeology of Cape Krusenstern: Eskimo and pre-Eskimo settlements around Kotzebue Sound, Alaska. Vol. 20. Washington, D.C.: National Park Service.


Hammill M.O., Mosnier A. & Bordeleau X. 2021. An update of impacts of harvesting on the abundance of Nunavik beluga. DFO Canadian Science Advisory Secretariat Research Document 2021/003. Ottawa: Fisheries and Oceans Canada.


Hammill M.O., Mosnier A., Gosselin J.-F., Matthews C.J.D., Marcoux M. & Ferguson S.H. 2017. Management approaches, abundance indices and total allowable harvest levels of belugas in Hudson Bay. DFO Canadian Science Advisory Secretariat Research Document 2017/062. Ottawa: Fisheries and Oceans Canada.


Hauser D.D.W., Laidre K.L., Suydam R.S. & Richard P.R. 2014. Population-specific home ranges and migration timing of Pacific Arctic beluga whales (Delphinapterus leucas). Polar Biology 37, 1171–1183, doi: 10.1007/s00300-014-1510-1.


Hobbs R.C. Reeves R.R., Prewitt J.S., Desportes G., Bretonhoneyman K., Christensen T., Citta J.J., Ferguson S.H., Frost K.J., Garde E., Gavrilo M., Ghazal M., Glazov D.M., Gosselin J.-F., Hammill M., Hansen R.G., Harwood L., Heide-Jørgensen M.P., Inglangasuk G., Kovacs K.M., Krasnova V.V., Kuznetsova D.M., Lee D.S., Lesage V., Litovka D.I., Lorenzen E.D., Lowry L.F., Lydersen C., Matthews C.J.D., Meschersky I.G., Mosnier A., O’Corry-Crowe G., Postma L., Quakenbush L.T., Shpak O.V., Skovrind M., Suydam R.S. & Watt C.A. 2019. Global review of the conservation status of monodontid stocks. Marine Fisheries Review 81(3-4), 1–53, doi: 10.7755/MFR.81.3–4.1.


Höss M. & Pääbo S. 1993. DNA extraction from Pleistocene bones by a silica-based purification method. Nucleic Acids Research 21, 3913-3914, doi: 10.1093/nar/21.16.3913.


Huntington H.P. & the communities of Buckland, Koyuk, Shaktoolik and Point Lay 1999. Traditional knowledge of the ecology of beluga whales (Delphinapterus leucas) in the eastern Chukchi and Northern Bering Seas, Alaska. Arctic 52, 49–61, doi: 10.14430/arctic909.


Huntington H.P., DanielsonS.L. , WieseF.K. , BakerM. , BovengP. , CittaJ.J. , De RobertisA. , DicksonD.M.S. , FarleyE. , GeorgeJ.C. , IkenK. , KimmelD.G. , KuletzK. , LaddC. , LevineR. , Quakenbush,L., StabenoP. , StaffordK.M. , StockwellD. & Wilson, C. 2020. Evidence suggests potential transformation of the Pacific Arctic ecosystem is underway. Nature Climate Change 10, 242-248, doi: 10.1038/s41558-020-0695-2.


Ivashin M.V. & Shevlyagin K.V. 1987. The white whale (Delphinapterus leucas Pallas, 1776): entrapment and escape in the ice of Senjavin Strait, U.S.S.R. Reports of the International Whaling Commission 37, 357–359.


Laidre K.L., Stern H., Kovacs K.M., Lowry L., Moore S.E., Regehr E.V., Ferguson S.H., Wiig O., Boveng P., Angliss R.P., Born E.W., Litovka D., Quakenbush L., Lydersen C., Vongraven D. & Ugarte F. 2015. Arctic marine mammal population status, sea ice habitat loss, and conservation recommendations for the 21st century. Conservation Biology 29, 724–737, doi: 10.1111/cobi.12474.


Loseto L.L., Richard P., Stern G.A., Orr J. & Ferguson S.H. 2006. Segregation of Beaufort Sea beluga whales during the open-water season. Canadian Journal of Zoology 84, 1743-1751, doi: 10.1139/Z06-160.


Lowry L.F., Burns J.J. & Nelson R.R. 1987. Polar bear predation on beluga whales in the Bering and Chukchi seas. Canadian Field-Naturalist 101, 141–146.


Lowry L.F., Citta J.J., O’Corry-Crowe G., Quakenbush L.T., Frost K.J., Suydam R. & Hobbs R.C. 2019. Distribution, abundance, harvest, and status of western Alaska beluga whale, Delphinapterus leucas, stocks. Marine Fisheries Review 81, 54−71, doi: 10.7755/MFR.81.3–4.2.


Lucier C.V. & Vanstone J.W. 1995. Traditional beluga drives of the Iñupiat of Kotzebue Sound, Alaska. Chicago: Field Museum of Natural History.


Luque S.P. & Ferguson S.H. 2010. Age structure, growth, mortality, and density of belugas (Delphinapterus leucas) in the Canadian Arctic: responses to environment? Polar Biology 33, 163–178, doi: 10.1007/s00300-009-0694-2.


Meschersky I.G., Shpak O.V., Litovka D.I., Glazov D.M., Borisova E.A. & Rozhnov V.V. 2013. A genetic analysis of the beluga whale Delphinapterus leucas (Cetacea: Monodontidae) from summer aggregations in the Russian Far East. Russian Journal of Marine Biology 39, 125-135, doi: 10.1134/S1063074013020065.


Morin P.A. & McCarthy M. 2007. Highly accurate SNP genotyping from historical and low-quality samples. Molecular Ecology Notes 7, 937-946, doi: 10.1111/j.1471-8286.2007.01804.x.


Morseth C.M. 1997. Twentieth-century changes in beluga whale hunting and butchering by the Kaἠiġmiut of Buckland, Alaska. Arctic 50, 241-255, doi: 10.14430/arctic1106.


Mymrin N.I. & Huntington H.P. 1999. Traditional knowledge of the ecology of beluga whales (Delphinapterus leucas) in the northern Bering Sea, Chukotka, Russia. Arctic 52, 62–70.


NMFS (National Marine Fisheries Service) 2005. Revisions to guidelines for assessing marine mammal stocks. Accessed on the internet at https://www.fisheries.noaa.gov/national/marine-mammal-protection/guidelines-assessing-marine-mammal-stocks#previous-workshop-reports-and-guidelines on 17 September 2021.


O’Corry-Crowe G.M., Dizon A.E., Suydam R.S. & Lowry L.F. 2002. Molecular genetic studies of population structure and movement patterns in a migratory species: the beluga whale (Delphinapterus leucas) in the western Nearctic. In C.J. Pfeiffer (ed.): Molecular and cell biology of marine mammals. Pp. 53-64. Malabar, FL: Krieger Publishing Co.


O’Corry-Crowe G., Lucey W., Archer F.I. & Mahoney B. 2015. The genetic ecology and population origins of the beluga whales of Yakutat Bay. Marine Fisheries Review 71, 47-48, doi: 10.7755/MFR.77.1.5.


O’Corry-Crowe G.M., Lydersen C., Heide-Jørgensen M.P., Hansen L., Mukhametov L.M., Dove O., Kovacs K.M. 2010. Population genetic structure and evolutionary history of North Atlantic beluga whales (Delphinapterus leucas) from west Greenland, Svalbard and the White Sea. Polar Biology 33, 1179-1194, doi: 10.1007/s00300-010-0807-y.


O’Corry-Crowe G., Mahoney A., Suydam R., Quakenbush L., Whiting A., Lowry L. & Harwood L. 2016. Genetic profiling links changing sea ice to shifting beluga whale migration patterns. Biology Letters 12, article no. 20160404, doi: 10.1098/rsbl.2016.0404.


O’Corry-Crowe G., Suydam R., Quakenbush L., Potgieter B., Harwood L., Litovka D., Ferrer T., Citta J., Burkanov V., Frost K. & Mahoney B. 2018. Migratory culture, population structure and stock identity in North Pacific beluga whales (Delphinapterus leucas). PLoS One 13, e0194201, doi: 10.1371/journal.pone.0194201.


O’Corry-Crowe G.M., Suydam R.S., Rosenberg A., Frost K.J. & Dizon A.E. 1997. Phylogeography, population structure and dispersal patterns of the beluga whale Delphinapterus leucas in the western Nearctic revealed by mitochondrial DNA. Molecular Ecology 6, 955-970, doi: 10.1046/j.1365-294X.1997.00267.x.


Paetkau D., Calvert W., Stirling I. & Strobeck C. 1995. Microsatellite analysis of population structure in Canadian polar bears. Molecular Ecology 4, 347–354, doi: 10.1111/j.1365-294X.1995.tb00227.x.


Paetkau D., Slade R., Burden M. & Estoup A. 2004. Direct, real-time estimation of migration rate using assignment methods: a simulation-based exploration of accuracy and power. Molecular Ecology 13, 55–65, doi: 10.1046/j.1365-294X.2004.02008.x.


Pella J. & Masuda M. 2001. Bayesian methods for analysis of stock mixtures from genetic characters. Fisheries Bulletin 99, 151–167.


Piry S., Alapetite A., Cornuet J.-M., Paetkau D., Baudouin L. & Estoup A. 2004. GeneClass2: a software for genetic assignment and first-generation migrant detection. Journal of Heredity 95, 536–539, doi: 10.1093/jhered/esh074.


Pritchard J.K., Stephen M. & Donnelly P. 2000. Inference of population structure using multilocus genotype data. Genetics 155, 945–959.


Richard P.R., Martin A.R. & Orr J.R. 2001. Summer and autumn movements of belugas of the eastern Beaufort Sea stock. Arctic 54, 223–236, doi: 10.14430/arctic783.


Rohland N. & Hofreiter M. 2007. Ancient DNA extraction from bones and teeth. Nature Protocols 2, 1756–1762.


Seaman G.A., Barger E. & Raymond L. Jr. 2015. Buckland Beluga Whale Traditional Ecological Knowledge Project. Final report. Buckland, AK: Buckland Beluga Traditional Ecological Knowledge Project.


Seaman G.A., Frost K.J. & Lowry L.F. 1986. Investigations of belukha whales in coastal waters of western and northern Alaska. I. Distribution, abundance, and movements. Final report. Outer Continental Shelf Environmental Assessment Program. Anchorage: National Oceanic and Atmospheric Administration.


Seaman G.A. & Noatak IRA Council 2018. Noatak Beluga Whale Traditional Knowledge Project. Final report. Noatak, AK: Native Village of Noatak.


Shelden K.E.W. & Wade P.R. (eds.) 2019. Aerial surveys, distribution, abundance, and trend of belugas (Delphinapterus leucas) in Cook Inlet, Alaska, June 2018. AFSC Processed Report 2019-09. Seattle: Alaska Fisheries Science Center, National Marine Fisheries Service National Oceanic and Atmospheric Administration, US Dept. of Commerce.


Stafford K.M. 2019. Increasing detections of killer whales (Orcinus orca) in the Pacific Arctic. Marine Mammal Science 35: 696–706, doi: 10.1111/mms.12551.


van Oosterhout C., Hutchinson W.F., Wills D.P.M. & Shipley P. 2004. MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Molecular Ecology Notes 4, 535-538, doi: 10.1111/j.1471-8286.2004.00684.x.


Wade P.R. 1998. Calculating limits to the allowable human caused mortality of cetaceans and pinnipeds. Marine Mammal Science 14, 1–37, doi: 10.1111/j.1748-7692.1998.tb00688.x.


Wade P.R. & Angliss R. 1997. Guidelines for assessing marine mammal stocks: report of the GAMMS workshop. April 3-5, 1996, Seattle, Washington. NOAA Technical Memorandum NMFS-OPR-12. Silver Spring, MD: National Atmospheric and Oceanic Administration.


Whiting A., Castellote M., Small R.J., Frost K.J. & Suydam R. 2019. Unexpected mid-winter presence of harbor porpoises (Phocoena phocoena) in Kotzebue Sound, Alaska. Marine Mammal Science 36, 354-358, doi: 10.1111/mms.12641.


Willoughby A.L., Ferguson M.C., Stimmelmayr R., Clarke J.T. & Brower A.A. 2020. Bowhead whale (Balaena mysticetus) and killer whale (Orcinus orca) cooccurrence in the U.S. Pacific Arctic, 2009–2018: evidence from bowhead whale carcasses. Polar Biology 43, 1669-1679, doi: 10.1007/s00300-020-02734-y.
Published
2021-11-29
How to Cite
O’Corry-Crowe G., Ferrer T., Citta J. J., Suydam R., Quakenbush L., Burns J. J., Monroy J., Whiting A., Seaman G., Goodwin, Sr. W., Meyer M., Rodgers S., & Frost K. J. (2021). Genetic history and stock identity of beluga whales in Kotzebue Sound. Polar Research, 40(S1). https://doi.org/10.33265/polar.v40.7623

Most read articles by the same author(s)