Marine Ecology Progress Series
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DOI: https://doi.org/10.3354/meps14850
copiedJuvenile salmon body condition in Southeast Alaska is buffered during marine heatwaves
ABSTRACT:
Pacific salmon (Oncorhynchus spp.) are ecologically, culturally, and commercially valuable throughout the Pacific Rim. Early marine survival of juvenile salmon is crucial for maintaining population abundance and sustainable fisheries. Climate variability, including multiple marine heatwaves, have recently caused ecosystem-wide changes and stressors with reduced return rates for some salmon populations in the Gulf of Alaska. We examined dietary niche breadth and condition metrics in juveniles of 4 salmon species (chum O. keta, coho O. kisutch, pink O. gorbuscha, and sockeye O. nerka), spanning 2010 to 2019, including 2 prominent heatwaves (2015-2016 and 2019). Samples were collected annually in Icy Strait, a major fish migration corridor in the Southeast Alaska archipelago. Analyses included bulk δ15N and δ13C stable isotopes, stomach contents, energy density, and morphometrics to evaluate variability in niche breadth and condition in response to extreme climate events. Interannual variability in stable isotopes was primarily explained by sea surface temperature (SST) anomalies for all species. The inverse relationship between SST and δ13C suggests the potential for increased terrestrial input into the nearshore environment during warmer conditions. We also found weak relationships between interannual variability in stomach contents and SST anomalies for pink salmon and a combination of δ13C, δ15N, SST, and condition for coho. However, fish condition did not show a significant relationship with SST anomalies. We propose that the complex topography and oceanography of northern Southeast Alaska provide marine habitat that temporarily buffers juvenile salmon from declines in body condition during heatwaves prior to migration into the Gulf of Alaska.
KEYWORDS
Supplement 1 (.pdf, 305 kB)
Text S1, Tables S1–S4, Figs. S1 & S2Supplement 2-1 (BiometricsIsotopesED.csv, 43 kB)
Juvenile salmon data used in this study, including length (mm), weight (g), stable isotope ratios of carbon-13 and nitrogen-15 (‰), and energy density by dry weight (kJ g–1)Supplement 2-2 (seakDiets.csv, 15 kB)
Juvenile salmon diet data are identified by prey items and quantified as percent composition by weightSupplement 2-3 (seak-egoaSST.csv, 25 kB)
Seawater temperatures integrated averages down to a depth of 20 m
Adams JN, Brodeur RD, Daly EA, Miller TW (2017) Prey availability and feeding ecology of juvenile Chinook (Oncorhynchus tshawytscha) and coho (O. kisutch) salmon in the northern California Current ecosystem, based on stomach content and stable isotope analyses. Mar Biol 164:98 Crossref
Amaya DJ, Miller AJ, Xie SP, Kosaka Y (2020) Physical drivers of the summer 2019 North Pacific marine heatwave. Nat Commun 11:1903 PubMed Crossref
Anderson M, Gorley R, Clarke K (2008) PERMANOVA+ for Primer: guide to software and statistical methods. Primer-E, Plymouth
Andrews AG, Farley EV, Moss JH, Murphy JM, Husoe EF (2009) Energy density and length of juvenile pink salmon Oncorhynchus gorbuscha in the Eastern Bering Sea from 2004 to 2007: a period of relatively warm and cool sea surface temperatures. Bull North Pac Anadromous Fish Comm 5:183-189
Arimitsu ML, Piatt JF, Hatch S, Suryan RM and others (2021) Heatwave-induced synchrony within forage fish portfolio disrupts energy flow to top pelagic predators. Glob Change Biol 27:1859-1878 PubMed Crossref
Beamish RJ, Mahnken C (2001) A critical size and period hypothesis to explain natural regulation of salmon abundance and the linkage to climate and climate change. Prog Oceanogr 49:423-437 Crossref
Bond NA, Cronin MF, Freeland H, Mantua N (2015) Causes and impacts of the 2014 warm anomaly in the NE Pacific. Geophys Res Lett 42:3414-3420 Crossref
Botsford LW, Lawrence CA (2002) Patterns of co-variability among California Current chinook salmon, coho salmon, Dungeness crab, and physical oceanographic conditions. Prog Oceanogr 53:283-305 Crossref
Cabana G, Rasmussen JB (1996) Comparison of aquatic food chains using nitrogen isotopes. Proc Natl Acad Sci USA 93:10844-10847 PubMed Crossref
Cavole L, Demko A, Diner R, Giddings A and others (2016) Biological impacts of the 2013-2015 warm-water anomaly in the Northeast Pacific: winners, losers, and the future. Oceanography 29:273-285 Crossref
Clarke KR, Ainsworth M (1993) A method of linking multivariate community structure to environmental variables. Mar Ecol Prog Ser 92:205-219 Crossref
Clarke KR, Warwick RM (1998) A taxonomic distinctness index and its statistical properties. J Appl Ecol 35:523-531 Crossref
Clarke KR, Warwick RM (2001) Change in marine communities: an approach to statistical analysis and interpretation, 2nd edn. Primer-E, Plymouth
Cooney RT, Allen JR, Bishop MA, Eslinger DL and others (2001) Ecosystem controls of juvenile pink salmon (Oncorhynchus gorbuscha) and Pacific herring (Clupea pallasi) populations in Prince William Sound, Alaska. Fish Oceanogr 10:1-13 Crossref
Curran JH, Biles FE (2021) Identification of seasonal streamflow regimes and streamflow drivers for daily and peak flows in Alaska. Water Resour Res 57:e2020WR028425
Daly EA, Brodeur RD (2015) Warming ocean conditions relate to increased trophic requirements of threatened and endangered salmon. PLOS ONE 10:e0144066 PubMed Crossref
Daly EA, Brodeur RD, Auth TD (2017) Anomalous ocean conditions in 2015: impacts on spring Chinook salmon and their prey field. Mar Ecol Prog Ser 566:169-182 Crossref
Danielson SL, Hennon TD, Monson DH, Suryan RM and others (2022) Temperature variations in the northern Gulf of Alaska across synoptic to century-long time scales. Deep Sea Res II 203:105155 Crossref
Di Lorenzo E, Mantua N (2016) Multi-year persistence of the 2014/15 North Pacific marine heatwave. Nat Clim Change 6:1042-1047 Crossref
Ebisuzaki W (1997) A method to estimate the statistical significance of a correlation when the data are serially correlated. J Clim 10:2147-2153 Crossref
Farley EV Jr, Trudel M (2009) Growth rate potential of juvenile sockeye salmon in warmer and cooler years on the Eastern Bering Sea shelf. J Mar Biol 2009:640215 Crossref
Farley EV Jr, Murphy JM, Adkison M, Eisner L (2007) Juvenile sockeye salmon distribution, size, condition and diet during years with warm and cool spring sea temperatures along the eastern Bering Sea shelf. J Fish Biol 71:1145-1158 Crossref
Farley EV Jr, Yasumiishi EM, Murphy JM, Strasburger W and others (2024) Critical periods in the marine life history of juvenile western Alaska chum salmon in a changing climate. Mar Ecol Prog Ser 726:149-160 Crossref
Fergusson EA, Watson J, Gray A, Murphy J (2018) Annual survey of juvenile salmon, ecologically-related species, and biophysical factors in the marine waters of southeastern Alaska, May-August 2016. NPAFC Doc 1771. National Oceanic and Atmospheric Administration (NOAA), National Marine Fisheries Service (NMFS), Alaska Fisheries Science Center, Auke Bay Laboratories, Ted Stevens Marine Research Institute, Juneau, AK. repository.library.noaa.gov/view/noaa/18271 Link
Fergusson E, Miller T, McPhee MV, Fugate C, Schultz H (2020) Trophic responses of juvenile Pacific salmon to warm and cool periods within inside marine waters of Southeast Alaska. Prog Oceanogr 186:102378 Crossref
Gladics AJ, Suryan RM, Brodeur RD, Segui LM, Filliger LZ (2014) Constancy and change in marine predator diets across a shift in oceanographic conditions in the Northern California Current. Mar Biol 161:837-851 Crossref
Graham C, Pakhomov EA, Hunt BPV (2021) Meta-analysis of salmon trophic ecology reveals spatial and interspecies dynamics across the North Pacific Ocean. Front Mar Sci 8:618884 Crossref
Gustafson RG, Winans GA (1999) Distribution and population genetic structure of river- and sea-type sockeye salmon in western North America. Ecol Freshw Fish 8:181-193 Crossref
Hagerman G, Vaughn M, Priest J (2021) Annual management report for the 2020 Southeast Alaska/Yakutat salmon troll fisheries. Alaska Department of Fish and Game, Division of Sport Fish and Commercial Fisheries, Juneau, AK
Harley JR, Biles FE, Brooks MK, Fellman J, Hood E, D’Amore DV (2023) Riverine dissolved inorganic carbon export from the southeast Alaskan drainage basin with implications for coastal ocean processes. J Geophys Res Biogeosci 128:e2023JG007609 Crossref
Heinl SC, Jones EL III, Piston AW, Richards PJ and others (2017) Review of salmon escapement goals in Southeast Alaska, 2017. Alaska Department of Fish and Game Division of Sport Fish and Commercial Fisheries, Juneau, AK Link
Hobday AJ, Oliver ECJ, Sen Gupta A, Benthuysen JA and others (2018) Categorizing and naming marine heatwaves. Oceanography 31:162-173 Crossref
Jackson AL, Inger R, Parnell AC, Bearhop S (2011) Comparing isotope niche widths among and within communities: SIBER - Stable Isotope Bayesian Ellipses in R. J Anim Ecol 80:595-602 PubMed Crossref
Keister JE, Herrmann B, Bos J (2022) Zooplankton composition links to climate and salmon survival in a northern temperate fjord. Limnol Oceanogr 67:2389-2404 Crossref
Kiljunen M, Grey J, Sinisalo T, Harrod C, Immonen H, Jones RI (2006) A revised model for lipid-normalizing d13C values from aquatic organisms, with implications for isotope mixing models. J Appl Ecol 43:1213-1222 Crossref
Kohan ML, Mueter FJ, Orsi JA, McPhee MV (2019) Variation in size, condition, and abundance of juvenile chum salmon (Oncorhynchus keta) in relation to marine factors in Southeast Alaska. Deep Sea Res II 165:340-347 Crossref
Lenth R (2024) Emmeans: estimated marginal means, aka least-squares means. R package version 1.10.2. CRAN.R-project.org/package=emmeans Link
Lerner JE, Hunt BPV (2022) Experimental validation confirms a carbon stable isotope lipid normalization procedure for Pacific salmon. Mar Ecol Prog Ser 698:191-197 Crossref
Litzow MA, Hunsicker ME, Bond NA, Burke BJ and others (2020) The changing physical and ecological meanings of North Pacific Ocean climate indices. Proc Natl Acad Sci USA 117:7665-7671 PubMed Crossref
Litzow MA, Malick MJ, Bond NA, Cunningham CJ, Gosselin JL, Ward EJ (2020) Quantifying a novel climate through changes in PDO-climate and PDO-salmon relationships. Geophys Res Lett 47:e2020GL087972 Crossref
Malick MJ, Haldorson LJ, Piccolo JJ, Boldt JL (2011) Growth and survival in relation to body size of juvenile pink salmon in the northern Gulf of Alaska. Mar Coast Fish 3:261-270 Crossref
Malick MJ, Cox SP, Mueter FJ, Peterman RM (2015) Linking phytoplankton phenology to salmon productivity along a north-south gradient in the Northeast Pacific Ocean. Can J Fish Aquat Sci 72:697-708 Crossref
McKinstry CAE, Campbell RW (2018) Seasonal variation of zooplankton abundance and community structure in Prince William Sound, Alaska, 2009-2016. Deep Sea Res II 147:69-78 Crossref
Moron V (2017) WEACLIM. MATLAB Central File Exchange. www.mathworks.com/matlabcentral/fileexchange/10881-weaclim Link
Mueter FJ, Peterman RM, Pyper BJ (2002) Opposite effects of ocean temperature on survival rates of 120 stocks of Pacific salmon (Oncorhynchus spp.) in northern and southern areas. Can J Fish Aquat Sci 59:456-463 Crossref
Murphy JM, Howard KG, Gann JC, Cieciel KC, Templin WD, Guthrie CM III (2017) Juvenile Chinook salmon abundance in the northern Bering Sea: implications for future returns and fisheries in the Yukon River. Deep Sea Res II 135:156-167 Crossref
Murphy JM, Garcia S, Dimond J, Moss J and others (2021) Northern Bering Sea surface trawl and ecosystem survey cruise report, 2019. Tech Memo NMFS-AFSC-423. US Department of Commerce, NOAA, Juneau, AK
Murphy JM, Garcia S, Piston A, Moss JH and others (2022) Coastal surveys in Alaska and their application to salmon run-size and harvest forecasts. North Pac Anadromous Fish Comm Tech Rep 18:140-146
NOAA Fisheries (2022) Fishery disaster determinations. www.fisheries.noaa.gov/national/funding-and-financial-services/fishery-disaster-determinations (accessed 1 November 2023) Link
North Pacific Anadromous Fish Commission (2021) North Pacific salmon catches decline to lowest levels in 4 decades. NPAFC, Vancouver
Orsi JA, Fergusson EA (2016) Annual survey of juvenile salmon, ecologically-related species, and biophysical factors in the marine waters of southeastern Alaska, May-August 2015. NPAFC National Oceanic and Atmospheric Administration (NOAA), National Marine Fisheries Service (NMFS), Alaska Fisheries Science Center, Auke Bay Laboratories, Ted Stevens Marine Research Institute, Juneau, AK. repository.library.noaa.gov/view/noaa/19447 Link
Orsi JA, Fergusson EA (2017) Annual survey of juvenile salmon, ecologically-related species, and biophysical factors in the marine waters of southeastern Alaska, May-August 2015. NPAFC Doc 1739. NPAFC National Oceanic and Atmospheric Administration (NOAA), National Marine Fisheries Service (NMFS), Alaska Fisheries Science Center, Auke Bay Laboratories, Ted Stevens Marine Research Institute, Juneau, AK. www.npafc.org/wp-content/uploads/Public-Documents/2018/1739USA.pdf Link
Peterson WT, Bond N, Robert M (2016) The Blob (part 3): going, going, gone? PICES Press 24:46-48
Post DM, Layman CA, Arrington DA, Takimoto G, Quattrochi J, Montaña CG (2007) Getting to the fat of the matter: models, methods and assumptions for dealing with lipids in stable isotope analyses. Oecologia 152:179-189 PubMed Crossref
R Core Team (2022) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna
Reid R, Oatman M, McCulloch J, Ned M and others (2019) Pacific Salmon Commission Thirty-Fourth Annual Report 2018/2019. Pacific Salmon Commission, Vancouver
Robinson CLK, Bertram DF, Shannon H, von Biela VR, Greentree W, Duguid W, Arimitsu ML (2024) Reduction in overwinter body condition and size of Pacific sand lance has implications for piscivorous predators during marine heatwaves. Mar Ecol Prog Ser 737:89-99 Crossref
Rogers MC, Heintz RA, Vollenweider JJ, Sreenivasan A, Miller KB (2023) Climate change-informed dietary modeling in Pacific cod: experimentally-derived effects of temperature and dietary quality on carbon and nitrogen stable isotope trophic discrimination factors. PLOS ONE 18:e0295564 PubMed Crossref
Ruggerone GT, Irvine JR, Connors B (2021) Did recent marine heatwaves and record high pink salmon abundance lead to a tipping point that caused record declines in North Pacific salmon abundance and harvest in 2020? North Pac Anadromous Fish Comm Tech Rep 17:78-82 Crossref
Sakano H, Fujiwara E, Nohara S, Ueda H (2005) Estimation of nitrogen stable isotope turnover rate of Oncorhynchus nerka. Environ Biol Fishes 72:13-18 Crossref
Schober P, Boer C, Schwarte LA (2018) Correlation coefficients: appropriate use and interpretation. Anesth Analg 126:1763-1768 PubMed Crossref
Sergeant CJ, Bellmore JR, McConnell C, Moore JW (2017) High salmon density and low discharge create periodic hypoxia in coastal rivers. Ecosphere 8:e01846 Crossref
Siddon EC, Heintz RA, Mueter FJ (2013) Conceptual model of energy allocation in walleye pollock (Theragra chalcogramma) from age-0 to age-1 in the southeastern Bering Sea. Deep Sea Res II 94:140-149 Crossref
Stabeno PJ, Bond NA, Hermann AJ, Kachel NB, Mordy CW, Overland JE (2004) Meteorology and oceanography of the Northern Gulf of Alaska. Cont Shelf Res 24:859-897 Crossref
Stabeno PJ, Bond NA, Kachel NB, Ladd C, Mordy CW, Strom SL (2016) Southeast Alaskan shelf from southern tip of Baranof Island to Kayak Island: currents, mixing and chlorophyll-a. Deep Sea Res II 132:6-23 Crossref
Sturdevant MV, Fergusson E, Hillgruber N, Reese C and others (2012) Lack of trophic competition among wild and hatchery juvenile chum salmon during early marine residence in Taku Inlet, Southeast Alaska. Environ Biol Fishes 94:101-116 Crossref
Suryan RM, Arimitsu ML, Coletti HA, Hopcroft RR and others (2021) Ecosystem response persists after a prolonged marine heatwave. Sci Rep 11:6235 PubMed Crossref
Thalmann HL, Daly EA, Brodeur RD (2020) Two anomalously warm years in the Northern California Current: impacts on early marine steelhead diet composition, morphology, and potential survival. Trans Am Fish Soc 149:369-382 Crossref
The Mathworks Inc (2020) MATLAB. www.mathworks.com/help/matlab/
Thynes TS, Bednarski JA, Conrad SK, Dupuis AW and others (2022) Annual management report of the 2021 Southeast Alaska commercial purse seine and drift gillnet fisheries. Fishery Management Report No. 22-25. Alaska Department of Fish Game Division of Sport Fish and Commercial Fisheries, Juneau, AK
Vander Zanden MJ, Rasmussen JB (1999) Primary consumer d13C and d15N and the trophic position of aquatic consumers. Ecology 80:1395-1404 Crossref
von Biela VR, Arimitsu ML, Piatt JF, Heflin B, Schoen SK, Trowbridge JL, Clawson CM (2019) Extreme reduction in nutritional value of a key forage fish during the Pacific marine heatwave of 2014-2016. Mar Ecol Prog Ser 613:171-182 Crossref
von Biela VR, Sergeant CJ, Carey MP, Liller Z and others (2022) Premature mortality observations among Alaska’s Pacific salmon during record heat and drought in 2019. Fisheries 47:157-168 Crossref
Walsh JE, Thoman RL, Bhatt US, Bieniek PA and others (2018) The high latitude marine heat wave of 2016 and its impacts on Alaska. Bull Am Meteorol Soc 99:S39-S43 Crossref
Wechter ME, Beckman BR, Andrews AG III, Beaudreau AH, McPhee MV (2017) Growth and condition of juvenile chum and pink salmon in the northeastern Bering Sea. Deep Sea Res II 135:145-155 Crossref
Weingartner T, Eisner L, Eckert GL, Danielson S (2009) Southeast Alaska: oceanographic habitats and linkages. J Biogeogr 36:387-400 Crossref
Wickham H, Averick M, Bryan J, Chang W and others (2019) Welcome to the Tidyverse. J Open Source Softw 4:1686 Crossref
Willette TM, Cooney RT, Patrick V, Mason DM, Thomas GL, Scheel D (2001) Ecological processes influencing mortality of juvenile pink salmon (Oncorhynchus gorbuscha) in Prince William Sound, Alaska. Fish Oceanogr 10:14-41 Crossref
Mariela Brooks (Corresponding Author)
- Auke Bay Laboratories, Alaska Fisheries Science Center, NOAA NMFS, 17109 Point Lena Loop Rd, Juneau, AK 99801, USA
Emily Fergusson (Co-author)
- Auke Bay Laboratories, Alaska Fisheries Science Center, NOAA NMFS, 17109 Point Lena Loop Rd, Juneau, AK 99801, USA
Matthew Rogers (Co-author)
- Auke Bay Laboratories, Alaska Fisheries Science Center, NOAA NMFS, 17109 Point Lena Loop Rd, Juneau, AK 99801, USA
Wesley Strasburger (Co-author)
- Auke Bay Laboratories, Alaska Fisheries Science Center, NOAA NMFS, 17109 Point Lena Loop Rd, Juneau, AK 99801, USA
Robert Suryan (Co-author)
- Auke Bay Laboratories, Alaska Fisheries Science Center, NOAA NMFS, 17109 Point Lena Loop Rd, Juneau, AK 99801, USA
Handling Editor:
Stephen Wing, Dunedin, New Zealand
Reviewers:
E.A. Daly, L.K. Rasmuson and 1 anonymous referee
Acknowledgements:
We thank NMFS AFSC, Alaska Department of Fish and Game, and the Pacific Salmon Commission Northern Fund. Additional thanks to the survey and vessel crews, laboratory technicians, and Ella Piatt, in particular, for weighing out archived samples for isotope analysis. Thank you to Todd Miller (NOAA-AFSC) for thoughtful discussions throughout this project. The scientific results and conclusions, as well as any views or opinions expressed herein, are those of the authors and do not necessarily reflect those of NOAA or the Department of Commerce. Reference to trade names does not imply endorsement by the Auke Bay Laboratories, National Marine Fisheries Service, NOAA, or the US Department of Commerce.