Climate and ecosystem linkages explain widespread declines in North American Atlantic salmon populations

Global Change Biology

Volumn 19, Issue 10, 2013, Pages 3046-3061

  Mills, Katherine E ^a,b   Pershing, Andrew J ^a,b   Sheehan, Timothy F ^c   Mountain, David ^d  

^a UNIVERSITY OF MAINE   (United States)

^b GULF OF MAINE RESEARCH INSTITUTE   (United States)

^c NORTHEAST FISHERIES SCIENCE CENTER   (United States)

^d UNIVERSITY OF ARIZONA   (United States)

Author keywords

Capelin; Chronological cluster analysis; Climate change; Dynamic factor analysis; Northwest Atlantic; Phytoplankton; Regime shift; Sea surface temperature; Zooplankton

Indexed keywords

ABUNDANCE; CLIMATE CONDITIONS; CLUSTER ANALYSIS; ENVIRONMENTAL FACTOR; MARINE ECOSYSTEM; PHYTOPLANKTON; POPULATION DECLINE; POPULATION DISTRIBUTION; POPULATION SIZE; SALMONID; SEA SURFACE TEMPERATURE; SURVIVORSHIP; TROPHIC LEVEL; ZOOPLANKTON;

NORTH AMERICA;

MALLOTUS (FISH); SALMO SALAR;

ANIMAL; ARTICLE; ATLANTIC OCEAN; ATLANTIC SALMON; CANADA; CAPELIN; CHRONOLOGICAL CLUSTER ANALYSIS; CLIMATE; CLIMATE CHANGE; DYNAMIC FACTOR ANALYSIS; ECOSYSTEM; NORTHWEST ATLANTIC; OSMERIFORMES; PHYTOPLANKTON; POPULATION DENSITY; REGIME SHIFT; SEA SURFACE TEMPERATURE; THEORETICAL MODEL; UNITED STATES; ZOOPLANKTON;

CAPELIN; CHRONOLOGICAL CLUSTER ANALYSIS; CLIMATE CHANGE; DYNAMIC FACTOR ANALYSIS; NORTHWEST ATLANTIC; PHYTOPLANKTON; REGIME SHIFT; SEA SURFACE TEMPERATURE; ZOOPLANKTON;

ANIMALS; ATLANTIC OCEAN; CANADA; CLIMATE; ECOSYSTEM; MODELS, THEORETICAL; OSMERIFORMES; PHYTOPLANKTON; POPULATION DENSITY; SALMO SALAR; UNITED STATES; ZOOPLANKTON;

EID: 84883740093     PISSN: 13541013     EISSN: 13652486     Source Type: Journal    
DOI: 10.1111/gcb.12298     Document Type: Article

References (85)

1. Akenhead SA (1987) Temperature and Salinity Off Newfoundland: Station 27 Annual Cycle and Residuals. Northwest Atlantic Fisheries Organization, NAFO SCR Doc. 87/66, Ser. No. N1355, Dartmouth, Nova Scotia.
2. Beamish RJ, Noakes DJ, McFarlane GA, Klyashtorin L, Ivanov VV, Kurashov V (1999) The regime concept and natural trends in the production of Pacific salmon. Canadian Journal of Fisheries and Aquatic Sciences, 56, 516-526.
3. Beaugrand G, Reid PC (2003) Long-term changes in phytoplankton, zooplankton and salmon linked to climate. Global Change Biology, 9, 801-817.
4. Beaugrand G, Reid PC (2012) Relationships between North Atlantic salmon, plankton, and hydroclimate change in the Northeast Atlantic. ICES Journal of Marine Science, 69, 1549-1562.
5. Behrenfeld MJ, O'Malley RT, Siegel DA et al. (2006) Climate-driven trends in contemporary ocean productivity. Nature, 444, 753-755.
6. Bennett K (1996) Determination of the number of zones in a biostratigraphic sequence. New Phytologist, 132, 155-170.
7. Carscadden JE, Frank KT (2002) Temporal variability in the condition factors of Newfoundland capelin (Mallotus villosus) during the past two decades. ICES Journal of Marine Science, 59, 950-958.
8. Carscadden JE, Frank KT, Leggett WC (2001) Ecosystem changes and the effects on capelin (Mallotus villosus), a major forage species. Canadian Journal of Fisheries and Aquatic Sciences, 58, 73-85.
9. Chaput G, Legault CM, Reddin DG, Caron F, Amiro PG (2005) Provision of catch advice taking account of non-stationarity in productivity of Atlantic salmon (Salmo salar L.) in the Northwest Atlantic. ICES Journal of Marine Science, 62, 131-143.
10. Chaput G, Dempson JB, Caron F, Jones R, Gibson J (2006) A synthesis of life history characteristics and stock grouping of Atlantic salmon (Salmo salar L.) in eastern Canada. DFO Canadian Science Advisory Secretariat Research Document 2006/015.
11. Condron A, DeConto R, Bradley RS, Juanes F (2005) Multidecadal North Atlantic climate variability and its effect on North American salmon abundance. Geophysical Research Letters, 32, L23703, doi:10.1029/2005GL024239.
12. COSEWIC (2010) COSEWIC Assessment and Status Report on the Atlantic salmon Salmo salar
13. Davoren GK, Montevecchi WA (2003) Signals from seabirds indicate changing biology of capelin stocks. Marine Ecology Progress Series, 258, 253-261.
14. Delworth TL, Mann ME (2000) Observed and simulated multidecadal variability in the Northern Hemisphere. Climate Dynamics, 16, 661-676.
15. Department of Fisheries and Oceans Canada (2011) Assessment of capelin in SA 2 + Div. 3KL in 2010. DFO Canadian Science Advisory Secretariat Science Advisory Report, 2010/090.
16. Doney SC, Ruckelshaus MH, Duffy JE et al. (2012) Climate change impacts on marine ecosystems. Annual Review of Marine Science, 4, 11-37.
17. Drinkwater KF, Belgrano A, Borja A et al. (2003) The response of marine ecosystems to climate variability associated with the North Atlantic Oscillation. In: The North Atlantic Oscillation: Climatic Significance and Environmental Impact. (eds Hurrell J, Kushnir Y, Ottersen G, Visbeck M), pp. 211-234. Geophysical Monograph, 134. American Geophysical Union, Washington, D. C.
18. Frank KT, Carscadden JE, Simon JE (1996) Recent excursions of capelin (Mallotus villosus) to the Scotian Shelf and Flemish Cap during anomalous hydrographic conditions. Canadian Journal of Fisheries and Aquatic Sciences, 53, 1473-1486.
19. Frank KT, Petrie B, Choi JS, Leggett WC (2005) Trophic cascades in a formerly cod-dominated ecosystem. Science, 308, 1621-1623.
20. Friedland KD (1998) Ocean climate influences on critical Atlantic salmon (Salmo salar) life history events. Canadian Journal of Fisheries and Aquatic Sciences, 55, 119-130.
21. Friedland KD, Reddin DG, Kocik JF (1993) Marine survival of North American and European Atlantic salmon: effects of growth and environment. ICES Journal of Marine Science, 50, 481-492.
22. Friedland KD, Reddin DG, McMenemy JR, Drinkwater KF (2003) Multidecadal trends in North American Atlantic salmon (Salmo salar) stocks and climate trends relevant to survival. Canadian Journal of Fisheries and Aquatic Sciences, 60, 363-383.
23. Friedland KD, Shank BV, Todd CD, McGinnity P, Nye J (2013) Differential response of continental stock complexes of Atlantic salmon (Salmo salar) to the Atlantic Multidecadal Oscillation. Journal of Marine Systems. Available at: http://dx.doi.org/10.1016/j.jmarsys.2013.03.003 (accessed 3 June 2013).
24. Gauthier-Ouellet M, Dionne M, Caron F, King TL, Bernatchez L (2009) Spatiotemporal dynamics of the Atlantic salmon (Salmo salar) Greenland fishery inferred from mixed-stock analysis. Canadian Journal of Fisheries and Aquatic Sciences, 66, 2040-2051.
25. Gerasimova OV (1994) Peculiarities of spring feeding by capelin (Mallotus villosus) on the Grand Banks in 1987-90. Journal of Northwest Atlantic Fishery Science, 17, 59-67.
26. Gjøsæter H, Dalpadado P, Hassel A (2002) Growth of Barents Sea capelin (Mallotus villosus) in relation to zooplankton abundance. ICES Journal of Marine Science, 59, 959-967.
27. Grimm EC (1987) CONISS: A FORTRAN 77 program for stratigraphically constrained cluster analysis by the method of incremental sum of squares. Computers & Geosciences, 13, 13-35.
28. Hare SR, Mantua NJ, Francis RC (1999) Inverse production regimes: Alaskan and West Coast salmon. Fisheries, 24, 6-14.
29. Hedeholm R, Grønkjær P, Rosing-Asvid A, Rysgaard S (2010) Variation in size and growth of West Greenland capelin (Mallotus villosus) along latitudinal gradients. ICES Journal of Marine Science, 67, 1128-1137.
30. Hilborn R, Quinn TP, Schindler DE, Rogers DE (2003) Biocomplexity and fisheries sustainability. Proceedings of the National Academy of Sciences, 100, 6564-6568.
31. Hoegh-Guldberg O, Bruno JF (2010) The impact of climate change on the world's marine ecosystems. Science, 328, 1523-1528.
32. Holmes E, Ward E, Wills K (2011) MARSS: Multivariate Autoregressive State-Space Modeling. R package version 3.2. http://Cran.r-project.org/package=MARSS (accessed 15 August 2011).
33. Hurrell JW (1995) Decadal trends in the North Atlantic Oscillation: regional temperatures and precipitation. Science, 269, 676-679.
34. Hurrell JW, Kushnir Y, Visbeck M, Ottersen G (2003) An overview of the North Atlantic Oscillation. In: The North Atlantic Oscillation: Climatic Significance and Environmental Impact, (eds Hurrell JW, Kushnir Y, Ottersen G, Visbeck M), pp. 1-35. Geophysical Monograph, 134. American Geophysical Union, Washington, D. C.
35. Hurvich CM, Tsai C-L (1989) Regression and time series model selection in small samples. Biometrika, 76, 297-307.
36. ICES (2007) Report of the Working Group on North Atlantic Salmon (WGNAS), 11-20 April 2007, Copenhagen, Denmark. ICES CM 2007/ACFM:13.
37. ICES (2012) Report of the Working Group on North Atlantic Salmon (WGNAS), 26 March-4 April 2012, Copenhagen, Denmark. ICES CM 2012/ACOM:09, 322 pp.
38. Jacobsen JA, Hansen LP (2000) Feeding habits of Atlantic salmon at different life stages at sea. In: The Ocean Life of Atlantic Salmon: Environmental and Biological Factors Influencing Survival, (ed. Mills D), pp. 170-192. Fishing News Books, Oxford.
39. Jonsson B, Jonsson N (2004) Factors affecting marine production of Atlantic salmon (Salmo salar). Canadian Journal of Fisheries and Aquatic Sciences, 61, 2369-2383.
40. Jossi JW, John AWG, Sameoto D (2003) Continuous plankton recorder sampling off the east coast of North America: history and status. Progress in Oceanography, 58, 313-325.
41. Juggins S (2012) Rioja: Analysis of Quaternary Science Data. Version 0.7-3 CRAN. Available at: http://cran.r-project.org/web/packages/rioja/rioja.pdf (accessed 30 April 2012).
42. Kocik JF, Sheehan TF (2006) Status of fishery resources off the northeastern US: Atlantic salmon (Salmo salar). Available at: http://www.nefsc.noaa.gov/sos/spsyn/af/salmon/ (accessed 10 August 2012).
43. Legendre P, Dallot S, Legendre L (1985) Succession of species within a community: chronological clustering, with applications to marine and freshwater zooplankton. The American Naturalist, 125, 257-288.
44. Lucey SM, Nye JA (2010) Shifting species assemblages in the Northeast US Continental Shelf Large Marine Ecosystem. Marine Ecology Progress Series, 415, 23-33.
45. Mantua NJ, Hare SR, Zhang Y, Wallace JM, Francis RC (1997) A Pacific interdecadal climate oscillation with impacts on salmon production. Bulletin of the American Meteorological Society, 78, 1069-1079.
46. Marshall SM, Orr AP (1955) The Biology of a Marine Copepod: Calanus finmarchicus (Gunnerus). Oliver and Boyd, Edinburgh.
47. Martin JHA, Mitchell KA (1985) Influence of sea temperature upon the numbers of grilse and multi-sea winter Atlantic salmon (Salmo salar) caught in the vicinity of the River Dee (Aberdeenshire). Canadian Journal of Fisheries and Aquatic Sciences, 42, 1513-1521.
48. Meehl GA, Stocker TR, Collins WD et al. (2007) Global climate projections. In: Climate Change 2007: The Physical Science Basis. Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change (eds Solomon S, Qin D, Manning M, Chen Z, Marquis M, Averyt KB, Tignor M, Miller HL), pp. 747-845. Cambridge University Press, New York.
49. MERCINA Working Group (2012) Recent Arctic climate change and its remote forcing of Northwest Atlantic shelf ecosystems. Oceanography, 25, 208-213.
50. Miller AS, Sheehan TF, Renkawitz MD, Meister AL, Miller TJ (2012) Revisiting the marine migration of US Atlantic salmon using historical Carlin tag data. ICES Journal of Marine Science, 69, 1609-1615.
51. Mowbray F (2002) Changes in the vertical distribution of capelin (Mallotus villosus) off Newfoundland. ICES Journal of Marine Science, 59, 942-949.
52. Myers RA, Akenhead SA, Drinkwater K (1990) The influence of Hudson Bay runoff and ice-melt on the salinity of the inner Newfoundland Shelf. Atmosphere-Ocean, 28, 241-256.
53. Nakashima BS (1996) The relationship between oceanographic conditions in the 1990s and changes in spawning behaviour, growth and early life history of capelin (Mallotus villosus). Northwest Atlantic Fisheries Organization Science Council Studies, 24, 55-68.
54. National Center for Atmospheric Research (2012) Climate Data Guide: Hurrell North Atlantic Oscillation (NAO) Index (station-based). Available at: http://climatedataguide.ucar.edu/guidance/hurrell-north-atlantic-oscilla tion-nao-index-station-based (accessed 11 April 2012).
55. National Climatic Data Center (2012) Extended Reconstructed Sea Surface Temperature (ERSST.v3b). Available at: http://www.ncdc.noaa.gov/ersst/ (accessed 30 April 2012).
56. National Oceanic and Atmospheric Administration (2012) Climate Timeseries: AMO (Atlantic Multidecadal Oscillation) Index. Available at: http://www.esrl.noaa.gov/psd/data/timeseries/AMO/index.html (accessed 11 April 2012).
57. Nye JA, Link JS, Hare JA, Overholtz WJ (2009) Changing spatial distribution of fish stocks in relation to climate and population size on the Northeast United States continental shelf. Marine Ecology Progress Series, 393, 111-129.
58. Parrish DL, Behnke RJ, Gephard SR, McCormick SD, Reeves GH (1998) Why aren't there more Atlantic salmon (Salmo salar)? Canadian Journal of Fisheries and Aquatic Sciences, 55, 281-287.
59. Pershing AJ, Greene CH, Jossi JW, O'Brien L, Brodziak JKT, Bailey BA (2005) Interdecadal variability in the Gulf of Maine zooplankton community with potential impacts on fish recruitment. ICES Journal of Marine Science, 62, 1511-1523.
60. Pershing AJ, Head EHJ, Greene CH, Jossi JW (2010) Pattern and scale of variability among Northwest Atlantic Shelf plankton communities. Journal of Plankton Research, 32, 1675-1684.
61. Potter ECE, Crozier WW, Schön P-J et al. (2004) Estimating and forecasting pre-fishery abundance of Atlantic salmon in the Northeast Atlantic for the management of mixed-stock fisheries. ICES Journal of Marine Science, 61, 1359-1369.
62. Pyper BJ, Peterman RM (1998) Comparison of methods to account for autocorrelation in correlation analyses of fish data. Canadian Journal of Fisheries and Aquatic Sciences, 55, 2127-2140.
63. R Development Core Team (2013) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0, URL http://www.R-project.org/. (accessed 3 May 2013)
64. Rago PJ (2001) Index measures and stock assessment in Atlantic salmon. In: Stock, Recruitment and Reference Points: Assessment and Management of Atlantic Salmon, (eds Prévost E, Chaput G), pp. 137-176. INRA Editions, Paris.
65. Rago PJ, Reddin DG, Porter TR, Meerburg DJ, Friedland KD, Potter ECE (1993) A Continental Run Reconstruction Model for the Non-maturing Component of North American Atlantic Salmon: Analysis of Fisheries in Greenland and Newfoundland-Labrador, 1974-1991. ICES CM 1993/M:25. Copenhagen, Denmark.
66. Record, NR, Pershing AJ, Maps F (2013) Emergent copepod communities in an adaptive trait-structured model. Ecological Modeling, 260, 11-24.
67. Reddin DG (1988) Ocean life of Atlantic salmon (Salmo salar L.) in the Northwest Atlantic. In: Atlantic Salmon: Planning for the Future (eds Mills DH, Piggins DJ), pp. 483-511. Proceedings of the third international Atlantic salmon symposium, Biarritz, France. Croom Helm, London.
68. Reddin DG, Friedland KD (1999) A history of identification to continent of origin of Atlantic salmon (Salmo salar L.) at west Greenland, 1969-1997. Fisheries Research, 43, 221-235.
69. Reddin DG, Helbig J, Thomas A, Whitehouse BG, Friedland KD (2000) Survival of Atlantic salmon (Salmo salar L.) related to marine climate. In: The Ocean Life of Atlantic Salmon: Environmental and Biological Factors Influencing Survival (ed. Mills D), pp. 88-91. Fishing News Books, Oxford.
70. Reid PC, Colebrook JM, Matthews JBL, Aiken J (2003) The Continuous Plankton Recorder: concepts and history, from Plankton Indicator to undulating recorders. Progress in Oceanography, 58, 117-173.
71. Reygondeau G, Beaugrand G (2011) Future climate-driven shifts in distribution of Calanus finmarchicus. Global Change Biology, 17, 756-766.
72. Rikardsen AH, Dempson JB (2011) Dietary life support: the food and feeding of Atlantic salmon at sea. In: Atlantic Salmon Ecology (eds Aas O, Einum S, Klemetson A, Skurdal J), pp. 115-143. Blackwell Publishing, Oxford.
73. Rose GA (2005) On distributional responses of North Atlantic fish to climate change. ICES Journal of Marine Science, 62, 1360-1374.
74. Sarmiento JL, Slater R, Barber R et al. (2004) Response of ocean ecosystems to climate warming. Global Biogeochemical Cycles, 18, GB3003. doi:10.1029/2003GB002134
75. Scarnecchia DL (1983) Age at sexual maturity in Icelandic stocks of Atlantic salmon (Salmo salar). Canadian Journal of Fisheries and Aquatic Sciences, 40, 1456-1468.
76. Sheehan TF, Reddin DG, Chaput G, Renkawitz MD (2012) SALSEA North America: a pelagic ecosystem survey targeting Atlantic salmon in the Northeast Atlantic. ICES Journal of Marine Science, 69, 1580-1588.
77. Smith TM, Reynolds RW, Peterson TC, Lawrimore J (2008) Improvements to NOAA's historical merged land-ocean surface temperature analysis (1880-2006). Journal of Climate, 21, 2283-2296.
78. Sutton RT, Hodson DLR (2005) Atlantic Ocean forcing of North American and European summer climate. Science, 309, 115-118.
79. Taboada FG, Anadón R (2012) Patterns of change in sea surface temperature in the North Atlantic during the last three decades: beyond mean trends. Climatic Change, 115, 419-431.
80. Thorstad EB, Whoriskey FG, Rikardsen AH, Aarestrup K (2011) Aquatic nomads: the life and migrations of the Atlantic salmon. In: Atlantic Salmon Ecology (eds Aas Ø, Einum S, Klemetsen A, Skurdal J), pp. 1-32. Wiley-Blackwell, Oxford.
81. Visbeck M, Chassignet EP, Curry RG, Delworth TL, Dickson RR, Krahmann G (2003) The ocean's response to North Atlantic Oscillation variability. In: The North Atlantic Oscillation: Climate Significance and Environmental Impact (eds Hurrell JW, Kushnir Y, Ottersen G, Visbeck M), pp. 113-145. American Geophysical Union, Washington, D. C.
82. Warner AJ, Hays GC (1994) Sampling by the continuous plankton recorder survey. Progress in Oceanography, 34, 237-256.
83. Xue Y, Smith TM, Reynolds RW (2003) Interdecadal changes of 30-yr SST normal during 1871-2000. Journal of Climate, 16, 1601-1612.
84. Zuur AF, Fryer RJ, Jolliffe IT, Dekker R, Beukema JJ (2003) Estimating common trends in multivariate time series using dynamic factor analysis. Environmetrics, 14, 665-685.
85. Zuur AF, Leno EN, Smith GM (2007) Analysing Ecological Data. Springer, New York.