Abstract
The climate regime in the eastern Bering Sea has recently been dominated by a pattern of multi-year stanzas, in which several successive years of minimal sea-ice formation and warm summer temperatures (e.g., 2002–2005, 2014–2017) alternate with several years of relatively extensive sea-ice formation and cold summer temperatures (e.g., 2006–2013). This emerging climate pattern may be forcing long-term changes in the spatial distributions of the Bering Sea’s marine fauna. The National Marine Fisheries Service’s Alaska Fisheries Science Center recently conducted two bottom trawl surveys covering the entire Bering Sea shelf from the Alaska Peninsula to the Bering Strait. The first, in the summer of 2010, was conducted during a cold year when the majority of the continental shelf was covered by a pool of cold (< 2 °C) water. The second, in the summer of 2017, was during a warmer year with water temperatures above the long-term survey mean. These two surveys recorded significantly different spatial distributions for populations of several commercially important fish species, including walleye pollock (Gadus chalcogrammus), Pacific cod (Gadus macrocephalus), and several flatfish species, as well as jellyfishes. Population shifts included latitudinal displacement as well as variable recruitment success. The large-scale distributional shifts reported here for high-biomass species raise questions about long-term ecosystem impacts, and highlight the need for continued monitoring. They also raise questions about our management strategies for these and other species in Alaska’s large marine ecosystems.











Similar content being viewed by others
Explore related subjects
Discover the latest articles and news from researchers in related subjects, suggested using machine learning.Notes
Reference to trade names does not imply endorsement by the National Marine Fisheries Service, NOAA.
References
Alverson DL, Pereyra WT (1969) Demersal fish explorations in the northeast Pacific Ocean: an evaluation of exploratory fishing methods and analytical approaches to stock size and yield forecasts. J Fish Res B Can 26:1985–2001
Aydin K, Mueter F (2007) The Bering Sea: a dynamic food web perspective. Deep-Sea Res II: Top Stud Oceanogr 54(23–26):2501–2525
Bakkala RG, Wakabayashi K (1985) Result of cooperative U.S. Japan groundfish investigations in the Bering Sea during May–August 1979. Int North Pac Fish Commun Bull 44:252
Bakkala RG, Traynor JJ, Teshima K, Shimada AM, Yamaguchi H (1985) Results of cooperative U.S. Japan groundfish investigations in the eastern Bering Sea during June-November 1982. US Dep Commer, NOAA Tech Memo. NMFS F/NWC-87, p 448. https://www.afsc.noaa.gov/Publications/FNWC-TM/NOAA-TM-FNWC-87.pdf
Bakkala RG, Karp WA, Walters GF, Sasaki T, Wilson MT, Sample TM, Shimada AM,Adams, D, Armistead CE (1992) Distribution, abundance, and biological characteristics of groundfish in the Eastern Bering Sea based on results of U.S. Japan bottom trawl and midwater surveys during June–September 1988. U.S. Dep. Commer., NOAA Tech. Memo. NMFS F/NWC-213, p 362
Brodeur RD, Decker MB, Ciannelli L, Purcell JE, Bond NA, Stabeno PJ, Acuna E, Hunt GL Jr (2008) Rise and fall of jellyfish in the eastern Bering Sea in relation to climate regime shifts. Prog Oceanogr 77:103–111
Cobb JN (1916) Pacific cod fisheries. Appendix IV to the Report of the U.S. Commissioner of Fisheries for 1915
Conner J, Lauth RR (2017) Results of the 2016 eastern Bering Sea continental shelf bottom trawl survey of groundfish and invertebrate resources. US Dep Commer, NOAA Tech Memo NMFS-AFSC-352, p 159
Cooper DW, Nichol DG (2016) Juvenile northern rock sole (Lepidopsetta polyxystra) spatial distribution and abundance patterns in the eastern Bering Sea: spatially dependent production linked to temperature. ICES J Mar Sci 73:1138–1146
Coyle KO, Eisner LB, Mueter FJ, Pinchuk AI, Janout MA, Cieciel KD, Farley EV, Andrews AG (2011) Climate change in the southeastern Bering Sea: impacts on pollock stocks and implications for the Oscillating Control Hypothesis. Fish Oceanogr 20:139–156
Dulvy NK, Rogers SI, Jennings S, Stelzenmüller V, Dye SR, Skjoldal HR (2008) Climate change and deepening of the North Sea fish assemblage: a biotic indicator of warming seas. J App Ecol 45:1029–1039
Fletcher GL, King MJ, Kao MH (1987) Low temperature regulation of antifreeze glycopeptide levels in Atlantic cod (Gadus morhua). Can J Zool 65:227–233
Fossheim M, Primicerio R, Johannesen E, Ingvaldsen RB, Aschan MM, Dolgov AV (2015) Recent warming leads to a rapid borealization of fish communities in the Arctic. Nat Clim Change 5:673–677
Francis CR, Hurst RJ, Renwick JA (2003) Quantifying annual variation in catchability for commercial and research fishing. Fish Bull US 101:293–304
Grebmeier JM, McRoy CP, Feder HM (1988) Pelagic-benthic coupling on the shelf of the northern Bering and Chukchi Seas. I. Food supply source and benthic biomass. Mar Ecol Prog Ser 48:57–67
Grebmeier JM, Overland JE, Moore SE, Farley EV, Carmack EC, Cooper LW, Frey KE, Helle JH, McLaughlin FA, McNutt SL (2006) A major ecosystem shift in the northern Bering Sea. Science 311:1461–1464
Hew CL, Slaughter D, Fletcher GL, Joshi SB (1981) Antifreeze glycoproteins in the plasma of Newfoundland Atlantic cod (Gadus morhua). Can J Zool 59:2186–2192
Highsmith RC, Coyle KO (1992) Productivity of arctic amphipods relative to gray whale energy requirements. Mar Ecol Prog Ser 83:141–150
Hunt GL Jr, Coyle KO, Eisner LB, Farley EV, Heintz RA, Mueter F, Napp JM, Overland JE, Ressler PH, Salo S, Stabeno PJ (2011) Climate impacts on eastern Bering Sea foodwebs: a synthesis of new data and an assessment of the Oscillating Control Hypothesis. ICES J Mar Sci 68:1230–1243
Jay CV, Grebmeier JM, Fischbach AS, McDonald TL, Cooper LW, Hornsby F (2014) Pacific walrus (Odobenus rosmarus divergens) resource selection in the northern Bering Sea. PLoS ONE 9:e93035
Johansen GO, Johannesen E, Michalsen K, Aglen A, Fotland A (2013) Seasonal variation in geographic distribution of North East Arctic (NEA) cod: survey coverage in a warmer Barents Sea. Mar Biol Res 9:908–919
Kotwicki S, Lauth RR (2013) Detecting temporal trends and environmentally-driven changes in the spatial distribution of bottom fishes and crabs on the eastern Bering Sea shelf. Deep-Sea Res II: Top Stud Oceanogr 94:231–243
Kotwicki S, Ono K (in press) The effect of variable sampling efficiency on reliability of the observation error as a measure of uncertainty in abundance indices from scientific surveys. Fish Fish
Kotwicki S, Buckley TW, Honkalehto T, Walters G (2005) Variation in the distribution of walleye pollock (Theragra chalcogramma) with temperature and implications of seasonal migration. Fish Bull US 103:574–587
Lauth RR (2011) Results of the 2010 eastern and northern Bering Sea continental shelf bottom trawl survey of groundfish and invertebrate fauna. US Dep Commer, NOAA Tech Memo NMFS-AFSC-227, p 256. http://www.afsc.noaa.gov/Publications/AFSC-TM/NOAA-TM-AFSC-227.pdf
Lauth RR, Conner JC (in review) Results of the 2017 eastern and northern Bering Sea continental shelf bottom trawl survey of groundfish and invertebrate fauna
Lovvorn JR, Richman SE, Grebmeier JM, Cooper LW (2003) Diet and body condition of spectacled eiders wintering in pack ice of the Bering Sea. Polar Biol 26:259–267
Lowther A, Liddell M (2015) Fisheries of the United States 2014. Current Fishery Statistics No. 2014, National Marine Fisheries Service, Silver Spring, MD, p 135. https://www.st.nmfs.noaa.gov/Assets/commercial/fus/fus14/documents/FUS2014.pdf. Accessed 24 Oct 2017
Mackenzie BR, Schiedek D (2007) Daily ocean monitoring since the 1860s shows record warming of northern European seas. Glob Change Biol 13:1335–1347
Moore SE, Grebmeier JM, Davies JR (2003) Gray whale distribution relative to forage habitat in the northern Bering Sea: current conditions and retrospective summary. Can J Zool 82:734–742
Mueter FJ, Litzow MA (2008) Sea ice retreat alters the biogeography of the Bering Sea continental shelf. Ecol Appl 18:309–320
Napp JM, Baier CT, Brodeur RD, Coyle KO, Shiga N, Mier K (2002) Interannual and decadal variability in zooplankton communities of the southeast Bering Sea shelf. Deep-Sea Res II: Top Stud Oceanogr 49(26):5991–6008
Overland JE, Wang M, Wood KR, Percival DB, Bond NA (2012) Recent Bering Sea warm and cold events in a 95-year context. Deep-Sea Res II 65–70:6–13
Perry AL, Low PJ, Ellis JR, Reynolds JD (2005) Climate change and distribution shifts in marine fishes. Science 308:1912–1915
Purcell JE, Arai MN (2001) Interactions of pelagic cnidarians and ctenophores with fish: a review. Hydrobiologia 451:27–44
R Core Team (2017) R: a language and environment for statistical computing. R Foundation for Statistical Computing Vienna, Austria. http://www.R-project.org/.
Ressler PH, DeRobertis A, Warren JD, Smith JN, Kotwicki S (2012) Developing an acoustic survey of euphausiids to understand trophic interactions in the Bering Sea ecosystem. Deep-Sea Res II 65–70:184–195
Sample TM, Nichol DG (1994) Results of the U.S.-U.S.S.R. cooperative bottom trawl survey of the eastern and northwestern Bering Sea shelf. US Dep Commer, NOAA Tech Memo NMFS-AFSC-34, p 183. http://www.afsc.noaa.gov/Publications/AFSC-TM/NOAA-TM-AFSC-34.pdf
Sample TM, Wolotira RJ Jr (1985) Demersal fish and shellfish resources of Norton Sound and adjacent waters during 1979. US Dep Commer, NOAA Tech Memo NMFS F/NWC-89, p 208. http://www.afsc.noaa.gov/Publications/FNWC-TM/NOAA-TM-FNWC-89.pdf
Smedsrud LH, Esau I, Ingvaldsen RB, Eldevik T, Haugan PM, Li C, Lien VS, Olsen A, Omar AM, Ottera OH, Risebrobakken B, Sando AB, Semenov VA, Sorokina SA (2013) The role of the Barents Sea in the Arctic climate system. Rev Geophys 51:415–449
Spencer P (2008) Density-independent and density-dependent factors affecting temporal changes in spatial distributions of eastern Bering Sea flatfish. Fish Oceanogr 17:396–410
Stabeno PJ, Bond NA, Kachel NB, Salo SA, Schumacher JD (2001) On the temporal variability of the physical environment over the south-eastern Bering Sea. Fish Oceanogr 10:81–98
Stabeno PJ, Duffy-Anderson JT, Eisner L, Farley E, Heintz R, Mordy CW (2017) Return of warm conditions in the southeastern Bering Sea: physics to fluorescence. PLoS ONE 12:e0185464
Stabeno PJ, Farley EV Jr, Kachel NB, Moore S, Mordy CW, Napp JM, Overland JE, Pinchuk AI, Sigler MF (2012a) A comparison of the physics of the northern and southern shelves of the eastern Bering Sea and some implications for the ecosystem. Deep-Sea Res II 65–70:14–30
Stabeno PJ, Kachel NB, Moore SE, Napp JM, Sigler M, Yamaguchi A, Zerbini AN (2012b) Comparison of warm and cold years on the southeastern Bering Sea shelf and some implications for the ecosystem. Deep-Sea Res II 65–70:31–45
Stauffer G (2004) NOAA protocols for groundfish bottom trawl surveys of the nation’s fishery resources. US Dep Commer, NOAA Tech Memo NMFS-F/SPO-65, p 205. https://spo.nmfs.noaa.gov/sites/default/files/tm65.pdf
Stevenson DE, Lauth RR (2012) Latitudinal trends and temporal shifts in the catch composition of bottom trawls conducted on the eastern Bering Sea shelf. Deep-Sea Res II 65–70:251–259
Swartzman G, Stuetzle W, Kulman K, Powojowski M (1994) Relating the distribution of pollock schools in the Bering Sea to environmental factors. ICES J Mar Sci 51:481–492
Thorson JT, Shelton AO, Ward EJ, Skaug HJ (2015) Geostatistical delta-generalized linear mixed models improve precision for estimated abundance indices for West Coast groundfishes. ICES J Mar Sci 72:1297–1310
Van Vorhees D, Lowther A (2010) Fisheries of the United States 2009. Current Fishery Statistics No. 2009, National Marine Fisheries Service, Silver Spring, MD, p 103. https://www.st.nmfs.noaa.gov/st1/fus/fus09/fus_2009.pdf. Accessed 24 Oct 2017
Veniaminov I (1984) Notes on the Islands of the Unalashka District. (trans: Black LT, Geoghegan RH). Elmer E. Rasmuson Library Translation Program, University of Alaska, Fairbanks
Wakabayashi K, Bakkala RG, Alton MS (1985) Methods of the U.S. Japan demersal trawl surveys. In: Bakkala RG, Wakabayashi K (eds) Results of cooperative U.S. Japan groundfish investigations in the Bering Sea during May–August 1979
Walters GE, Wilderbuer TK (2000) Decreasing length at age in a rapidly expanding population of northern rock sole in the eastern Bering Sea and its effect on management advice. J Sea Res 44:17–26
Walters GE, Teshima K, Traynor JJ, Bakkala RG, Sassano JA, Halliday KL, Karp WA, Mito K, Williamson NJ, Smith DM (1988) Distribution, abundance, and biological characteristics of groundfish in the eastern Bering Sea based on results of the U.S. Japan triennial bottom trawl and hydroacoustic surveys during May–September, 1985. US Dep Commer, NOAA Tech Memo NMFS F/NWC-154, p 401
Walsh SJ (1997) Efficiency of bottom sampling trawls in deriving survey abundance indices. Ocean Lit Rev 7:748
Wickham H (2009) Ggplot2: elegant graphics for data analysis. Springer, New York
Wolotira RJ Jr, Sample TM, Morin M Jr (1977) Demersal fish and shellfish resources of Norton Sound, the southeastern Chukchi Sea, and adjacent waters in the baseline year 1976. NWAFC Processed Rep., p. 69. Northwest and Alaska Fish Cent, Natl Mar Fish Serv, NOAA. https://www.afsc.noaa.gov/Publications/ProcRpt/10_1977_FNWAK_Wolotira.pdf
Wyllie-Echeverria T, Wooster WS (1998) Year-to-year variations in Bering Sea ice cover and some consequences for fish distributions. Fish Oceanogr 7:159–170
Zimmermann M, Goddard P, Sample TM (1994) Results of the 1991 U.S.-U.S.S.R. cooperative bottom trawl survey of the eastern and western Bering Sea continental shelf. US Dep Commer, NOAA Tech Memo NMFS-AFSC-41, p 178. http://www.afsc.noaa.gov/Publications/AFSC-TM/NOAA-TM-AFSC-41.pdf
Acknowledgements
We thank the multitude of scientists and vessel crew that participated in the EBS and NBS bottom trawl surveys of 2010 and 2017 on the FV Aldebaran, FV Alaska Knight, and FV Vesteraalen. We also thank S. Kotwicki, D. Nichol, and S. Zador for reviewing earlier drafts of the manuscript. This research was supported in part by the NOAA Fisheries Loss of Sea Ice (LOSI) initiative. We thank the NMFS Office of Science and Technology for their support. The recommendations and general content presented in this paper do not necessarily represent the views or official position of the Department of Commerce, the National Oceanic and Atmospheric Administration, or of the National Marine Fisheries Service.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Human and animal rights
All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.
Rights and permissions
About this article
Cite this article
Stevenson, D.E., Lauth, R.R. Bottom trawl surveys in the northern Bering Sea indicate recent shifts in the distribution of marine species. Polar Biol 42, 407–421 (2019). https://doi.org/10.1007/s00300-018-2431-1
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00300-018-2431-1