Linking Behavior, Physiology, and Survival of Atlantic Salmon Smolts During Estuary Migration

Marine and Coastal Fisheries

Volumn 7, Issue 1, 2015, Pages 68-86

  Stich, Daniel S ^a   Zydlewski, Gayle B ^a   Kocik, John F ^b   Zydlewski, Joseph D ^a  

^a UNIVERSITY OF MAINE   (United States)

^b NOAA EARTH SYSTEM RESEARCH LABORATORY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

SALMO SALAR;

EID: 84934976006     PISSN: None     EISSN: 19425120     Source Type: Journal    
DOI: 10.1080/19425120.2015.1007185     Document Type: Article

References (88)

1. +-ATPase activity and downstream movement in domesticated and first-generation offspring of wild anadromous Brown Trout (Salmo trutta). Canadian Journal of Fisheries and Aquatic Sciences 57:2086–2095.
2. B.I.Berli, M.J.Gilbert, A.L.Ralph, K.B.Tierney, and P.Burkhardt-Holm. 2014. Acute exposure to a common suspended sediment affects the swimming performance and physiology of juvenile salmonids. Comparative Biochemistry and Physiology Part A Molecular and Integrative Physiology 176:1–10.
3. B.F.Blackwell, and F.Juanes. 1998. Predation on Atlantic Salmon smolts by Striped Bass after dam passage. North American Journal of Fisheries Management 18:936–939.
4. B.F.Blackwell, W.B.Krohn, N.R.Dube, and A.J.Godin. 1997. Spring prey use by double-crested cormorants on the Penobscot River, Maine, USA. Colonial Waterbirds 20:77–86.
5. G.Boeuf, 1993. Salmonid smolting:a pre-adaptation to the oceanic environment. Pages 105–135 in J.C.Renkin and F.B.Jensen, editors. Fish ecophysiology. Chapman and Hall, London.
6. K.P.Burnham, and D.R.Anderson. 2002. Model selection and multimodel inference:a practical information-theoretic approach, 2nd edition. Springer, New York.
7. J.B.Carey, and S.D.McCormick. 1998. Atlantic Salmon smolts are more responsive to an acute handling and confinement stress than parr. Aquaculture 168:237–253.
8. G.Chaput, 2012. Overview of the status of Atlantic Salmon (Salmo salar) in the North Atlantic and trends in marine mortality. ICES (International Council for the Exploration of the Sea) Journal of Marine Science 69:1538–1548.
9. G.Chaput, C.M.Legault, D.G.Reddin, F.Caron, and P.G.Amiro. 2005. Provision of catch advice taking account of non-stationarity in productivity of Atlantic Salmon (Salmo salar L.) in the Northwest Atlantic. ICES (International Counsel for the Exploration of the Sea) Journal of Marine Science 62:131–143.
10. Day, L. R. 2006. Restoring native fisheries to Maine's largest watershed:the Penobscot River restoration project. Journal of Contemporary Water Research and Education 134:29–33.
11. J.B.Dempson, M.J.Robertson, C.J.Pennell, G.Furey, M.Bloom, M.Shears, L.M.N.Ollerhead, K.D.Clark, R.Hinks, and G.J.Robertson. 2011. Residency time, migration route, and survival of Atlantic Salmon Salmo salar smolts in a Canadian fjord. Journal of Fish Biology 78:1976–1992.
12. H.Dingle, and V.A.Drake. 2007. What is migration? BioScience 57:113–121.
13. J.Duston, and R.L.Saunders. 1990. The entrainment role of photoperiod on hypoosmoregulatory and growth-related aspects of smolting in Atlantic Salmon (Salmo salar). Canadian Journal of Zoology 68:707–715.
14. J.J.Faraway, 2005. Extending the linear model with R:generalized linear, mixed effects and nonparametric regression models. Chapman and Hall, London.
15. S.M.Fried, J.D.McCleave, and G.W.LaBar. 1978. Seaward migration of hatchery-reared Atlantic Salmon, Salmo salar, smolts in the Penosbcot estuary, Maine:riverine movements. Journal of the Fisheries Research Board of Canada 35:76–87.
16. Friedland, K. 1998. Ocean climate influences on critical Atlantic Salmon (Salmo salar) life history events. Canadian Journal of Fisheries and Aquatic Science 55(Supplement 1):119–130.
17. K.D.Friedland, D.G.Redding, J.R.McMenemy, and K.F.Drinkwater. 2003. Multidecadal trends in North American Atlantic Salmon (Salmo salar) and climate trends relevant to juvenile survival. Canadian Journal of Fisheries and Aquatic Sciences 60:563–583.
18. K.D.Friedland, B.V.Shank, C.D.Todd, P.McGinninty, and J.A.Nye. 2014. Differential response of continental stock complexes of Atlantic Salmon (Salmo salar) to the Atlantic multidecadal oscillation. Journal of Marine Systems 133:77–87.
19. D.Gorsky, J.Trial, J.Zydlewski, and J.McCleave. 2009. The effects of smolt stocking strategies on migratory path selection of adult Atlantic Salmon in the Penobscot River, Maine. North American Journal of Fisheries Management 29:949–957.
20. S.Gudjonsson, I.R.Jonsson, and T.Antonsson. 2005. Migration of Atlantic Salmon, Salmo salar, smolt through the estuary area of River Ellidaar. Environmental Biology of Fishes 74:291–296.
21. P.A.Haefner, Jr. 1967. Hydrography of the Penobscot River (Maine) estuary. Journal of the Fisheries Research Board of Canada 24:1553–1571.
22. E.A.Halfyard, A.J.F.Gibson, M.J.W.Stokesbury, D.E.Ruzzante, and F.G.Whoriskey. 2013. Correlates of estuarine survival of Atlantic Salmon postsmolts from the southern upland, Nova Scotia, Canada. Canadian Journal of Fisheries and Aquatic Sciences 70:452–460.
23. S.O.Handeland, T.Järvi, A.Fernö, and S.O.Stefansson. 1997. Osmotic stress, antipredator behavior, and mortality of Atlantic Salmon (Salmo salar) smolts. Canadian Journal of Fisheries and Aquatic Sciences 53:2673–2680.
24. J.P.Hawkes, R.Saunders, A.D.Vashon, and M.S.Cooperman. 2013. Assessing efficacy of non-lethal harassment of double-crested cormorants to improve Atlantic Salmon smolt survival. Northeastern Naturalist 20:1–18.
25. S.A.Hayes, and J.F.Kocik. 2014. Comparative estuarine and marine migration ecology of Atlantic Salmon and steelhead:blue highways and open plains. Reviews in Fish Biology and Fisheries 24:757–780.
26. R.D.Hedger, F.Martin, D.Hatin, F.Caron, F.G.Whoriskey, and J.J.Dodson. 2008. Active migration of wild Atlantic Salmon Salmo salar smolt through a coastal embayment. Marine Ecological Press Series 355:235–246.
27. W.S.Hoar, 1988. The physiology of smolting salmonids. Pages 275–343 in W.S.Hoar and D.J.Randall, editors. Fish physiology, volume XIB. Academic Press, New York.
28. C.M.Holbrook, M.T.Kinnison, and J.Zydlewski. 2011. Survival of migrating Atlantic Salmon smolts through the Penobscot River, Maine:a prerestoration assessment. Transactions of the American Fisheries Society 140:1255–1268.
29. N.A.Hvidsten, and R.A.Lund. 1988. Predation on hatchery-reared and wild smolts of Atlantic Salmon, Salmo salar L., in the estuary of River Orkla, Norway. Journal of Fish Biology 33:121–126.
30. E.A.Imhoff, and R.L.Harvey. 1972. Penobscot River study. University of Maine, Environmental Studies Center, Technical Report 1, Orono.
31. Y.Itokazu, R.Käkelä, J.Piironen, X.L.Guan, P.Kiiskinen, and M.Vornanen. 2014. Gill tissue lipids of salmon (Salmosalar L.) presmolts and smolts from anadromous and landlocked populations. Comparative Biochemistry and Physiology Part A Molecular and Integrative Physiology 172:39–45.
32. IUBMB (International Union of Biochemistry and Molecular Biology). 1992. Enzyme nomenclature 1992. Academic Press, San Diego, California.
33. T.Järvi, 1989. Synergistic effect on mortality in Atlantic Salmon, Salmo salar, smolt caused by osmotic stress and presence of predators. Environmental Biology of Fishes 26:149–152.
34. T.Järvi, 1990. Cumulative acute physiological stress in Atlantic Salmon smolts:the effect of osmotic imbalance and the presence of predators. Aquaculture 89:337–350.
35. E.Jokikokko, and S.Mäntyniemi. 2003. The survival of stocked Atlantic Salmon smolts during sea run and the timing of migration in the River Simojoki, northern Finland. Aquaculture 219:431–444.
36. M.L.Keefer, G.A., Taylor, D.F.Garletts, C.K.Helms, G.A.Gauthier, T.M.Pierce, and C.C.Caudill. 2012. Reservoir entrapment and dam passage mortality of juvenile Chinook Salmon in the middle fork Willamette River. Ecology of Freshwater Fish 21:222–234.
37. J.F.Kocik, J.P.Hawkes, T.F.Sheehan, P.A.Music, and K.F.Beland. 2009. Assessing estuarine and coastal migration and survival of wild Atlantic Salmon smolts from the Naraguagus River, Maine using acoustic telemetry. Pages 293–310 in A.Haro, K.L.Smith, R.A.Rulifson, C.M.Moffitt, R.J.Klauda, M.J.Dadswell, R.A.Cunjak, J.E.Cooper, K.L.Beal, and T.S.Avery, editors, Challenges for diadromous fishes in a dynamic global environment. American Fisheries Society, Symposium 69, Bethesda, Maryland.
38. J.L.Laake, 2013. RMark:an R interface for analysis of capture-recapture data with MARK. National Marine Fisheries Service, Alaska Fisheries Science Center Report 2013-01, Seattle.
39. G.L.Lacroix, 2008. Influence of origin on migration and survival of Atlantic Salmon (Salmo salar) in the Bay of Fundy, Canada. Canadian Journal of Fisheries and Aquatic Sciences 65:2063–2079.
40. G.L.Lacroix, 2014. Large pelagic predators could jeopardize the recovery of endangered Atlantic Salmon. Canadian Journal of Fisheries and Aquatic Sciences 71:343–350.
41. G.L.Lacroix, D.Knox, and M.J.W.Stokesbury. 2005. Survival and behaviour of post-smolt Atlantic Salmon in coastal habitat with extreme tides. Journal of Fish Biology 66:485–498.
42. E.A.Marschall, M.E.Mather, D.L.Parrish, G.W.Allison, and J.R.McMenemy. 2011. Migration delays caused by anthropogenic barriers:modeling dams, temperature, and success of migrating salmon smolts. Ecological Applications 21:3014–3031.
43. F.Martin, R.D.Hedger, J.J.Dodson, L.Fernandes, D.Hatin, F.Caron, and F.G.Whoriskey. 2009. Behavioural transition during the estuarine migration of wild Atlantic Salmon (Salmo salar L.) smolt. Ecology of Freshwater Fish 18:406–417.
44. D.Mathur, P.G.Heisey, J.R.Skalski, and D.R.Kenney. 2000. Salmonid smolt survival relative to turbine efficiency and entrainment depth in hydroelectric power generation. Journal of the American Water Resources Association 36:737–747.
45. J.D.McCleave, 1978. Rhythmic aspects of estuarine migration of hatchery-reared Atlantic Salmon (Salmo salar) smolts. Journal of fish Biology 12:559–570.
46. +-ATPase activity. Canadian Journal of Fisheries and Aquatic Sciences 50:656–658.
47. S.D.McCormick, 2013. Smolt physiology and endocrinology. Pages 200–237 in S.D.McCormick, A.P.Farrell, and C.J.Brauner, editors, Euryhaline fishes. Academic Press, Oxford, UK.
48. S.D.McCormick, R.A.Cunjak, B.Dempson, M.F.O'Dea, and J.B.Carey. 1999. Temperature-related loss of smolt characteristics in Atlantic Salmon (Salmo salar) in the wild. Canadian Journal of Fisheries and Aquatic Sciences 56:1649–1658.
49. S.D.McCormick, L.P.Hansen, T.P.Quinn, and R.L.Saunders. 1998. Movement, migration, and smolting of Atlantic Salmon (Salmo salar). Canadian Journal of Fisheries and Aquatic Sciences 55:77–92.
50. S.D.McCormick, D.T.Lerner, M.Y.Monette, K.Nieves-Puigdoller, J.T.Kelly, and B.T.Björnsson. 2009. Taking it with you when you go:how perturbations to the freshwater environment, including temperature, dams, and contaminants, affect marine survival of Salmon. Pages 195–214 in A.Haro, K.L.Smith, R.A.Rulifson, C.M.Moffitt, R.J.Klauda, M.J.Dadswell, R.A.Cunjak, J.E.Cooper, K.L.Beal, and T.S.Avery, editors. Challenges for diadromous fishes in a dynamic global environment. American Fisheries Society, Symposium 69, Bethesda, Maryland.
51. S.D.McCormick, and R.L.Saunders. 1987. Preparatory physiological adaptations for marine life in salmonids:osmoregulation, growth and metabolism. Pages 211–229 in M.J.Dadswell, R.J.Klauda, C.M.Moffitt, and R.L.Saunders, editors. Common strategies in anadromous and catadromous fishes. American Fisheries Society, Symposium 1, Bethesda, Maryland.
52. +-ATPase activity, and ion regulation during parr-smolt transformation of Atlantic Salmon (Salmo salar). Fish Physiology and Biochemistry 6:231–241.
53. S.D.McCormick, J.M.Shrimpton, and J.D.Zydlewski. 1997. Temperature effects on osmoregulatory physiology of anadromous fish. Pages 279–301 in C.M.Wood and D.G.McDonald, editors. Global warming implications for freshwater and marine fish. University Press, Cambridge, UK.
54. A.S.Miller, T.F.Sheehan, M.D.Renkawitz, A.L.Meister, and T.J.Miller. 2012. Revisiting the marine migration of US Atlantic Salmon using historical Carlin tag data. ICES (International Council for Exploration of the Sea) Journal of Marine Science 69:1609–1615.
55. K.E.Mills, A.J.Pershing, T.F.Sheehan, and D.F.Mountain. 2013. Climate and ecosystem linkages explain widespread declines in North American Atlantic Salmon populations. Global Change Biology 19:3046–3061.
56. D.C.Montgomery, E.A.Peck, and G.G.Vining. 2006. Introduction to linear regression analysis, 4th edition. Wiley, Hoboken, New Jersey.
57. A.Moore, E.C.E.Potter, N.J.Milner, and S.Bamber. 1995. The migratory behavior of wild Atlantic Salmon (Salmo salar) smolts in the estuary of the River Conway, North Wales. Canadian Journal of Fisheries and Aquatic Sciences 52:1923–1935.
58. P.A.Music, J.P.Hawkes, and M.S.Cooperman. 2011. Magnitude and causes of smolt mortality in rotary screw traps:an Atlantic Salmon case study. North American Journal of Fisheries Management 30:713–722.
59. J.Otero, J.H.L'Abée-Lund, T.Castro-Santos, K.Leonardsson, G.O.Storvik, B.Jonsson, B.Dempson, I.C.Russell, A.J.Jensen, J.-L.Baglinière, M.Dionne, J.D.Armstrong, A.Romakkaniemi, B.H.Letcher, J.F.Kocik, J.Erkinaro, R.Poole, G.Rogan, H.Lundqvist, J.C.MacLean, E.Jokikokko, J.V.Arnekleiv, R.J.Kennedy, E.Niemelä, P.Caballero, P.A.Music, T.Antonsson, S.Gudjonsson, A.E.Veselov, A.Lamberg, S.Groom, B.H.Taylor, M.Taberner, M.Dillane, F.Arnason, G.Horton, N.A.Hvidsten, I.R.Jonsson, N.Jonsson, S.McKelvey, T.F.Naesje, Ø.Skaala, G.W.Smith, H.Saegrov, N.C.Stenseth, and L.A.Vøllestad. 2014. Basin-scale phenology and effects of climate variability on global timing of initial seaward migration of Atlantic Salmon (Salmo salar). Global Change Biology 20:61–75.
60. D.L.Parrish, R.J.Behnke, S.R.Gephard, S.D.McCormick, and G.H.Reeves. 1998. Why aren't there more Atlantic Salmon (Salmo salar)? Canadian Journal of Fisheries and Aquatic Sciences 55(Supplement 1):281–287.
61. T.P.Poe, H.C.Hansel, S.Vigg, D.E.Palmer, and L.A.Prendergast. 1991. Feeding of predaceous fishes on out-migrating juvenile salmonids in John Day reservoir, Columbia River. Transactions of the American Fisheries Society 120:405–420.
62. C.S.Price, and C.B.Schreck. 2003. Stress and saltwater-entry behavior of juvenile Chinook Salmon (Oncorhynchus tshawytscha):conflicts in physiological motivation. Canadian Journal of Fisheries and Aquatic Sciences 60:910–918.
63. R Development Core Team. 2014. R:a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna.
64. H.A.Schaller, C.E.Petrosky, and E.S.Tinus. 2014. Evaluating river management during seaward migration to recover Columbia River stream-type Chinook Salmon considering variation in marine conditions. Canadian Journal of Fisheries and Aquatic Sciences 71:259–271.
65. H.R.Seiwell, 1932. Some physical characteristics of the water of Penobscot Bay, Maine, especially in relation to the tides and a discussion of the results obtained by duplicate measurements of specific gravity of sea water by the Knudsen and Plummet methods. Internationale Revue der Gesamten Hydrobioligie and Hydrographie 27:315–331.
66. T.F.Sheehan, M.D.Renkawitz, and R.W.Brown. 2011. Surface trawl survey for US origin Atlantic Salmon Salmo salar. Journal of Fish Biology 79:374–398.
67. P.K.Smith, R.I.Krohn, G.T.Hermanson, A.K.Mallia, F.H.Gartner, M.D.Provenzano, E.K.Fujimoto, N.M.Goeke, B.J.Olson, and D.C.Klenk. 1985. Measurements of protein using bicinchoninic acid. Analytical Biochemistry 150:76–85.
68. D.S.Stich, M.M.Bailey, J.D.Zydlewski. 2014. Survival of Atlantic Salmon Salmo salar smolts through a hydropower complex in the lower Penobscot River, Maine USA. Journal of Fish Biology 85:1074–1096.
69. D.J.Stier, and B.Kynard. 1986. Use of radio telemetry to determine the mortality of Atlantic Salmon smolts passed through a 17-MW Kaplan turbine at a low-head hydroelectric dam. Transactions of the American Fisheries Society 115:771–775.
70. +-ATPase activity; is sea entry delayed? Environmental Biology of Fishes 90:317–321.
71. M.A.Svenning, R.Borgstrøm, T.O.Dehli, G.Moen, R.T.Barrett, T.Pedersen, and W.Vader. 2005. The impact of marine fish predation on Atlantic Salmon smolts (Salmo salar) in the Tana estuary, north Norway, in the presence of and alternative prey, Lesser Sandeel (Ammodytes marinus). Fisheries Research 76:466–474.
72. G.E.Sykes, C.J.Johnson, and J.M.Shrimpton. 2009. Temperature and flow effects on migration timing of Chinook Salmon smolts. Transactions of the American Fisheries Society 138:1252–1265.
73. E.B.Thorstad, I.Uglem, B.Finstad, C.M.Chittenden, R.Nilsen, F.Økland, and P.A.Bjørn. 2012a. Stocking location and predation by marine fishes affect survival of hatchery-reared Atlantic Salmon smolts. Fisheries Management and Ecology 19:400–409.
74. E.B.Thorstad, F.Whoriskey, I.Uglem, A.Moore, A.H.Rikardsen, and B.Finstad. 2012b. A critical life stage of the Atlantic Salmon Salmo salar:behaviour and survival during the smolt and initial post-smolt migration. Journal of Fish Biology 81:500–542.
75. C.D.Todd, K.D.Friedland, J.C.MacLean, B.D.Whyte, I.C.Russell, M.E.Lonergan, and M.B.Morrissey. 2012. Phenological and phenotypic changes in Atlantic Salmon populations in response to a changing climate. ICES (International Council for the Exploration of the Sea) Journal of Marine Science 69:1686–1698.
76. USASAC (U.S. Atlantic Salmon Assessment Committee). 2012. Annual report of the U.S. Atlantic Salmon Assessment Committee, report 24. Available:http://www.nefsc.noaa.gov/USASAC/Reports/. (August 2014).
77. USASAC (U.S. Atlantic Salmon Assessment Committee). 2014. Annual report of the U.S. Atlantic Salmon Assessment Committee, report 26. Available:http://www.nefsc.noaa.gov/USASAC/Reports/. (May 2014).
78. L.A.Weitkamp, G.Goulette, J.Hawkes, M.O'Malley, and C.Lipsky. 2014. Juvenile salmon in estuaries:comparisons between North American Atlantic and Pacific salmon populations. Reviews in Fish Biology and Fisheries 24:713–736.
79. K.G.Whalen, D.L.Parrish, and S.D.McCormick. 1999. Migration timing of Atlantic Salmon smolts relative to environmental and physiological factors. Transactions of the American Fisheries Society 128:289–301.
80. G.C.White, and K.P.Burnham. 1999. Program MARK:survival estimation from populations of marked animals. Bird Study 46:120–139.
81. W.S.Zaugg, 1982. Some changes in smoltification and seawater adaptability of salmonids resulting from environmental and other factors. Aquaculture 28:143–151.
82. W.S.Zaugg, and L.R.McLain. 1972. Changes in gill adenosinetriphosphatase activity associated with parr-smolt transformation in steelhead trout, Coho, and spring Chinook salmon. Journal of the Fisheries Research Board of Canada 29:161–171.
83. A.Zuur, E.N.Ieno, N.Walker, A.A.Saveliev, and G.M.Smith. 2009. Mixed effects models and extensions in ecology with R. Springer, New York.
84. G.B.Zydlewski, A.Haro, and S.D.McCormick. 2005. Evidence for cumulative temperature as an initiating and terminating factor in downstream migratory behavior of Atlantic Salmon (Salmo salar) smolts. Canadian Journal of Fisheries and Aquatic Sciences 62:68–78.
85. G.B.Zydlewski, D.S.Stich, and S.D.McCormick. 2014. Photoperiod control of the initiation of downstream migration in Atlantic Salmon smolts. Journal of Fish Biology 85:1074–1096.
86. +-ATPase of Atlantic Salmon smolts in freshwater is not a predictor of long-term growth in seawater. Aquaculture 362–363:121–126.
87. J.Zydlewski, and M.P.Wilkie. 2013. Freshwater to saltwater transitions in migratory fishes. Pages 254–294 in S.D.McCormick, A.P.Farrell, and C.J.Brauner, editors, Euryhaline fishes. Academic Press, Oxford, UK.
88. J.Zydlewski, G.Zydlewski, and G.R.Danner. 2010. Descaling injury impairs the osmoregulatory ability of Atlantic Salmon smolts entering seawater. Transactions of the American Fisheries Society 138:129–136.