Environmental Management

, Volume 56, Issue 3, pp 571–586 | Cite as

A Critical Assessment of the Ecological Assumptions Underpinning Compensatory Mitigation of Salmon-Derived Nutrients

  • Scott F. CollinsEmail author
  • Amy M. Marcarelli
  • Colden V. Baxter
  • Mark S. Wipfli


We critically evaluate some of the key ecological assumptions underpinning the use of nutrient replacement as a means of recovering salmon populations and a range of other organisms thought to be linked to productive salmon runs. These assumptions include: (1) nutrient mitigation mimics the ecological roles of salmon, (2) mitigation is needed to replace salmon-derived nutrients and stimulate primary and invertebrate production in streams, and (3) food resources in rearing habitats limit populations of salmon and resident fishes. First, we call into question assumption one because an array of evidence points to the multi-faceted role played by spawning salmon, including disturbance via redd-building, nutrient recycling by live fish, and consumption by terrestrial consumers. Second, we show that assumption two may require qualification based upon a more complete understanding of nutrient cycling and productivity in streams. Third, we evaluate the empirical evidence supporting food limitation of fish populations and conclude it has been only weakly tested. On the basis of this assessment, we urge caution in the application of nutrient mitigation as a management tool. Although applications of nutrients and other materials intended to mitigate for lost or diminished runs of Pacific salmon may trigger ecological responses within treated ecosystems, contributions of these activities toward actual mitigation may be limited.


Oncorhynchus spp. Pacific salmon Atlantic salmon Stream restoration Nutrient supplementation Primary and secondary productivity 



We thank the many people whose hard work and research influenced the content of this paper. We thank James Bellmore, Phil Roni, Gordon Holtgrieve, and an anonymous reviewer for providing constructive and insightful review of this manuscript. This review was funded by the Bonneville Power Administration (2007-332-00), Idaho Department of Fish and Game, and Idaho Power. The use of trade names or products does not constitute endorsement by the U.S. Government.


  1. Allan JD, Wipfli MS, Caouette JP, Prussian A, Rodgers J (2003) Influence of streamside vegetation on inputs of terrestrial invertebrates to salmonid food webs. Can J Fish Aquat Sci 60:309–320Google Scholar
  2. Allen KR (1951) The Horokiwi stream: a study of a trout population. New Zealand Depart Fish Bull 10:1–238Google Scholar
  3. Ambrose HE, Wilzbach MA, Cummins KW (2004) Periphyton response to increased light and salmon carcass introduction in northern California streams. J N Am Benthol Soc 23:701–712Google Scholar
  4. Bellmore JR, Baxter CV, Ray AM, Denny L, Tardy K, Galloway E (2012) Assessing the potential for salmon recovery via floodplain restoration: a multitrophic level comparison of dredge-mined to reference segments. Environ Manag 49:734–750Google Scholar
  5. Bellmore JR, Baxter CV, Martens K, Connolly PJ (2013) The floodplain food web mosaic: a study of its importance to salmon and steelhead with implications for their recovery. Ecol Appl 23:189–207Google Scholar
  6. Bellmore JR, Fremier AK, Mejia F, Newsom M (2014) The response of stream periphyton to Pacific salmon: using a model to understand the role of environmental context. Freshw Biol 59:1437–1451Google Scholar
  7. Ben-David M, Hanley T, Klein D, Schell D (1997) Seasonal changes in diets of coastal and riverine mink: the role of spawning Pacific salmon. Can J Zool 75:803–811Google Scholar
  8. Bilby RE, Fransen BR, Bisson PA (1996) Incorporation of nitrogen and carbon from spawning coho salmon into the trophic system of small streams: evidence from stable isotopes. Can J Fish Aquat Sci 53:164–173Google Scholar
  9. Bilby RE, Fransen BR, Bisson PA, Walter JK (1998) Response of juvenile coho salmon (Oncorhynchus kisutch) and steelhead (Oncorhynchus mykiss) to the addition of salmon carcasses to two streams in southwestern Washington, USA. Can J Fish Aquat Sci 55:1909–1918Google Scholar
  10. Brock CS, Leavitt PR, Schindler DE, Quay PD (2007) Variable effects of marine-derived nutrients on algal production in salmon nursery lakes of Alaska during the past 300 years. Limnol Oceanogr 52:1588–1598Google Scholar
  11. Budy P, Schaller H (2007) Evaluating tributary restoration potential for Pacific salmon recovery. Ecol Appl 17:1068–1086Google Scholar
  12. Budy P, Thiede GP, Bouwes N, Petrosky C, Schaller H (2002) Evidence linking delayed mortality of Snake River salmon to their earlier hydrosystem experience. N Am J Fish Manage 22:35–51Google Scholar
  13. Chaloner DT, Wipfli MS (2002) Influence of decomposing Pacific salmon carcasses on macroinvertebrate growth and standing stock in southeastern Alaska streams. J N Am Benthol Soc 21:430–442Google Scholar
  14. Chaloner DT, Martin KM, Wipfli MS, Ostrom PH, Lamberti GA (2002) Marine carbon and nitrogen in southeastern Alaska stream food webs: evidence from artificial and natural streams. Can J Fish Aquat Sci 59:1257–1265Google Scholar
  15. Chaloner DT, Lamberti GA, Merritt RW, Mitchell NL, Ostrom PH, Wipfli MS (2004) Variation in responses to spawning Pacific salmon among three south-eastern Alaska streams. Freshw Biol 49:587–599Google Scholar
  16. Chapman DW (1966) Food and space as regulators of salmonid populations in streams. Am Nat 100:345–357Google Scholar
  17. Claeson SM, Li JL, Compton JE, Bisson PA (2006) Response of nutrients, biofilm, and benthic insects to salmon carcass addition. Can J Fish Aquat Sci 63:1230–1241Google Scholar
  18. Collins SF, Baxter CV (2014) Heterogeneity of riparian habitats mediates responses of terrestrial arthropods to a subsidy of Pacific salmon carcasses. Ecosphere 5:art 146Google Scholar
  19. Collins SF, Moerke AH, Chaloner DT, Janetski DJ, Lamberti GA (2011) Response of dissolved nutrients and periphyton to spawning Pacific salmon in three northern Michigan streams. J N Am Benthol Soc 30:831–839Google Scholar
  20. Compton JE, Andersen CP, Phillips DL, Brooks JR, Johnson MG, Church MR, Hogsett ME, Cairns MA, Rygiewicz PT, McComb BC (2006) Ecological and water quality consequences of nutrient addition for salmon restoration in the Pacific northwest. Front Ecol Environ 4:18–26Google Scholar
  21. Cooper DC (1973) Enhancement of net primary productivity by herbivore grazing in aquatic laboratory microcosms. Limnol Oceanogr 18:31–37Google Scholar
  22. Coronado C, Hilborn R (1998) Spatial and temporal factors affecting survival in coho salmon (Oncorhynchus kisutch) in the Pacific Northwest. Can J Fish Aquat Sci 55:2067–2077Google Scholar
  23. Cram JM, Kiffney PM, Klett R, Edmonds RL (2011) Do fall additions of salmon carcasses benefit food webs in experimental streams? Hydrobiologia 675:197–209Google Scholar
  24. Denton KP, Rich HB Jr, Quinn TP (2009) Diet, movement, and growth of Dolly Varden in response to sockeye salmon subsidies. Trans Am Fish Soc 138:1207–1219Google Scholar
  25. Ebel JD, Marcarelli AM, Kohler AE (2014) Biofilm nutrient limitation, metabolism, and standing crop responses to experimental application of salmon carcass analog in Idaho streams. Can J Fish Aquat Sci 71:1796–1804Google Scholar
  26. Finney BP, Gregory-Eaves I, Sweetman J, Douglas MSV, Smol JP (2000) Impacts of climatic change and fishing on Pacific salmon abundance over the past 300 years. Science 290:795–799Google Scholar
  27. Francis TB, Schindler DE, Moore JW (2006) Aquatic insects play a minor role in dispersing salmon-derived nutrients into riparian forests in southwestern Alaska. Can J Fish Aquat Sci 63:2543–2552Google Scholar
  28. Gende SM, Edwards RT, Willson MF, Wipfli MS (2002) Pacific salmon in aquatic and terrestrial ecosystems. Bioscience 52:917–928Google Scholar
  29. Gresh T, Lichatowich J, Schoonmaker P (2000) An estimation of historic and current levels of salmon production in the Northeast Pacific ecosystem: evidence of a nutrient deficit in the freshwater systems of the Pacific Northwest. Fisheries 25:15–21Google Scholar
  30. Groot C, Margolis L, Clark WC (1995) Physiological ecology of Pacific salmon. University of British Columbia Press, VancouverGoogle Scholar
  31. Gross HP, Wurtsbaugh WA, Luecke C (1998) The role of anadromous sockeye salmon in the nutrient loading and productivity of Redfish Lake, Idaho. Trans Am Fish Soc 127:1–18Google Scholar
  32. Guyette MQ, Loftin CS, Zydlewski J (2013) Carcass analog addition enhances juvenile Atlantic salmon (Salmo salar) growth and condition. Can J Fish Aquat Sci 70:860–870Google Scholar
  33. Hankin DG, Healey MC (1986) Dependence of exploitation rates for maximum yield and stock collapse on age and sex structure of chinook salmon (Oncorhynchus tshawytscha) stocks. Can J Fish Aquat Sci 43:1746–1759Google Scholar
  34. Harvey BC, Wilzbach MA (2010) Carcass addition does not enhance juvenile salmonid biomass, growth, or retention in six northwestern California streams. N Am J Fish Manag 30:1445–1451Google Scholar
  35. Helfield JM, Naiman RJ (2001) Effects of salmon-derived nitrogen on riparian forest growth and implications for stream productivity. Ecology 82:2403–2409Google Scholar
  36. Helfield JM, Naiman RJ (2002) Salmon and alder as nitrogen sources to riparian forests in a boreal Alaskan watershed. Oecologia 133:573–582Google Scholar
  37. Hicks BJ, Wipfli MS, Lang DW, Lang ME (2005) Marine-derived nitrogen and carbon in freshwater-riparian food webs of the Copper River Delta, southcentral Alaska. Oecologia 144:558–569Google Scholar
  38. Hilderbrand GV, Farley SD, Schwartz CC, Robbins CT (2004) Importance of salmon to wildlife: implications for integrated management. Ursus 15:1–9Google Scholar
  39. Hilderbrand RH, Watts AC, Randle AM (2005) The myths of restoration ecology. Ecol Soc 10:art 19Google Scholar
  40. Hocking MD, Reimchen TE (2006) Consumption and distribution of salmon (Oncorhynchus spp.) nutrients and energy by terrestrial flies. Can J Fish Aquat Sci 63:2076–2086Google Scholar
  41. Hocking MD, Reynolds JD (2011) Impacts of salmon on riparian plant diversity. Science 331:1609–1612Google Scholar
  42. Holtgrieve GW, Schindler DE (2011) Marine-derived nutrients, bioturbation, and ecosystem metabolism: reconsidering the role of salmon in streams. Ecology 92:373–385Google Scholar
  43. Holtgrieve GW, Schindler DE, Jewett PK (2009) Large predators and biogeochemical hotspots: brown bear (Ursus arctos) predation on salmon alters nitrogen cycling in riparian soils. Ecol Res 24:1125–1135Google Scholar
  44. Hoyle GM, Holderman C, Anders PJ, Shafii B, Ashley KI (2014) Water quality, chlorophyll, and periphyton responses to nutrient addition in the Kootenai River, Idaho. Freshw Sci 33:1024–1029Google Scholar
  45. Huryn AD (1996) An appraisal of the Allen paradox in a New Zealand trout stream. Limnol Oceanogr 41:243–252Google Scholar
  46. Huryn AD, Wallace JB (2000) Life history and production of stream insects. Annu Rev Entomol 45:83–110Google Scholar
  47. Hyatt KD, McQueen DJ, Shortreed KS, Rankin DP (2004) Sockeye salmon (Oncorhynchus nerka) nursery lake fertilization: review and summary of results. Environ Rev 12:133–162Google Scholar
  48. Janetski D, Chaloner D, Tiegs D, Lamberti G (2009) Pacific salmon effects on stream ecosystems: a quantitative synthesis. Oecologia 159:583–595Google Scholar
  49. Johnson JH, Ringler NH (1979) Predation on Pacific salmon eggs by salmonids in a tributary of Lake Ontario. G Great Lakes Res 5:177–181Google Scholar
  50. Johnston NT, Perrin CJ, Slaney PA, Ward BR (1990) Increased juvenile salmonid growth by whole-river fertilization. Can J Fish Aquat Sci 47:862–872Google Scholar
  51. Juday C, Rich WH, Kemmerer G, Mann A (1932) Limnological studies of Karluk Lake, Alaska. Fish Bull 12:407–436Google Scholar
  52. Kiernan JD, Harvey BN, Johnson ML (2010) Direct versus indirect pathways of salmon-derived nutrient incorporation in experimental lotic food webs. Can J Fish Aquat Sci 67:1909–1924Google Scholar
  53. Kiffney PM, Buhle ER, Naman SM, Pess GR, Klett RS (2014) Linking resource availability and habitat structure to stream organisms: an experimental and observational assessment. Ecosphere 5:39. doi: 10.1890/ES13-00269.1 Google Scholar
  54. Kirchhoff MD (2003) Effects of salmon-derived nitrogen on riparian forest growth and implications for stream productivity: comment. Ecology 84:3396–3399Google Scholar
  55. Kohler AE, Taki D (2010) Macroinvertebrate response to salmon carcass analogue treatments: exploring the relative influence of nutrient enrichment, stream foodweb, and environmental variables. J N Am Benthol Soc 29:690–710Google Scholar
  56. Kohler AE, Rugenski A, Taki D (2008) Stream food web response to a salmon carcass analogue addition in two central Idaho, USA streams. Freshw Biol 53:446–460Google Scholar
  57. Kohler AE, Pearsons TN, Zendt JS, Mesa MG, Johnson CL, Connolly PJ (2012) Nutrient enrichment with salmon carcass analogs in the Columbia River basin, USA: a stream food web analysis. Trans Am Fish Soc 141:802–824Google Scholar
  58. Kohler AE, Kusnierz PC, Copeland T, Venditti DA, Denny L, Gable J, Lewis BA, Kinzer R, Barnett B, Wipfli MS (2013) Salmon-mediate nutrient flux in selected streams of the Columbia River basin, USA. Can J Fish Aquat Sci 70:502–512Google Scholar
  59. Kondolf GM, Wolman MG (1993) The sizes of salmonid spawning gravels. Water Resour Res 29:2275–2285Google Scholar
  60. Koshino Y, Kudo H, Kaeriyama M (2013) Stable isotope evidence indicates the incorporation into Japanese catchments of marine-derived nutrients transported by spawning Pacific Salmon. Freshw Biol 58:1864–1877Google Scholar
  61. Koyama A, Kavanagh K, Robinson A (2005) Marine nitrogen in central Idaho riparian forests: evidence from stable isotopes. Can J Fish Aquat Sci 62:518–526Google Scholar
  62. Lamberti GA, Resh VH (1983) Stream periphyton and insect herbivores: an experimental study of grazing by a caddisfly population. Ecology 64:1124–1135Google Scholar
  63. Lang DW, Reeves GH, Hall JD, Wipfli MS (2006) The influence of fall-spawning coho salmon (Oncorhynchus kisutch) on growth and production of juvenile coho salmon rearing in beaver ponds on the Copper River Delta, Alaska. Can J Fish Aquat Sci 63:917–930Google Scholar
  64. Lessard JL, Merritt RW (2006) Influence of marine-derived nutrients from spawning salmon on aquatic insect communities in southeast Alaskan streams. Oikos 113:334–343Google Scholar
  65. Lessard JA, Merritt RW, Berg MB (2009) Investigating the effect of marine-derived nutrients from spawning salmon on macroinvertebrate secondary production in southeast Alaskan streams. J N Am Benthol Soc 28:683–693Google Scholar
  66. Levi PS, Tank JL (2013) Nonnative Pacific salmon alter hot spots of sediment nitrification in Great Lakes tributaries. J Geophys Res 118:436–444Google Scholar
  67. Levi PS, Tank JL, Rüegg J, Janetski DJ, Tiegs SD, Chaloner DT, Lamberti GA (2013a) Whole-stream metabolism responds to spawning Pacific salmon in their native and introduced ranges. Ecosystems 16:1–15Google Scholar
  68. Levi PS, Tank JL, Tiegs SD, Chaloner DT, Lamberti GA (2013b) Biogeochemical transformation of a nutrient subsidy: salmon, streams, and nitrification. Biogeochemistry 113:643–655Google Scholar
  69. Lichatowich JA (1999) Salmon without rivers: a history of the Pacific salmon crisis. Island Press, Washington, DCGoogle Scholar
  70. Lichatowich JA, Williams RN (2009) Failures to incorporate science into fishery management and recovery programs: lessons from the Columbia River. Am Fish Soc Symp 70:1005–1019Google Scholar
  71. Lobón-Cerviá J, Gonzalez G, Budy P (2011) Factors driving spatial and temporal variation in production and production/biomass ratio of stream-resident brown trout (Salmo trutta) in Cantabrian streams. Freshwater Biol 56:2272–2287Google Scholar
  72. Mantua NJ, Hare SR, Zhang Y, Wallace JM, Francis RC (1997) A Pacific interdecadal climate oscillation with impacts on salmon production. Bull Am Meteorol Soc 78:1069–1079Google Scholar
  73. Marcarelli AM, Baker MA, Wurtsbaugh WA (2008) Is in-stream N2 fixation an important N source for benthic communities and stream ecosystems? J N Am Benthol Soc 27:186–211Google Scholar
  74. Marcarelli AM, Baxter CV, Wipfli MS (2014) Nutrient additions to mitigate for loss of Pacific salmon: consequences for stream biofilm and nutrient dynamics. Ecosphere 5:69Google Scholar
  75. Martin AE, Wipfli MS, Spangler RE (2010) Aquatic community responses to salmon carcass analog and wood bundle additions in restored floodplain habitats in an Alaskan stream. Trans Am Fish Soc 139:1828–1845Google Scholar
  76. Mason J (1976) Response of underyearling coho salmon to supplemental feeding in a natural stream. J Wildl Manag 40:775–788Google Scholar
  77. Meehan EP, Seminet-Reneau EE, Quinn TP (2005) Bear predation on Pacific salmon facilitates colonization of carcasses by fly maggots. Am Midl Nat 153:142–151Google Scholar
  78. Minakawa N, Gara RI, Honea JM (2002) Increased individual growth rate and community biomass of stream insects associated with salmon carcasses. J N Am Benthol Soc 21:651–659Google Scholar
  79. Minshall GW, Bahman S, Price WJ, Holderman C, Anders PJ, Lester G, Barrett P (2014) Effects of nutrient replacement on benthic macroinvertebrates in an ultraoligotrophic reach of the Kootenai River, 2003–2010. Freshw Sci 33:1009–1023Google Scholar
  80. Mitchell NL, Lamberti GA (2005) Responses in dissolved nutrients and epilithon abundance to spawning salmon in southeast Alaska streams. Limnol Oceanogr 50:217–227Google Scholar
  81. Montgomery DR (2003) King of fish: the thousand-year run of salmon. Westview Press, Boulder COGoogle Scholar
  82. Moore KD, Moore JW (2013) Ecological restoration and enabling behavior: a new metaphorical lens? Conserv Lett 6:1–5Google Scholar
  83. Moore JW, Schindler DE (2004) Nutrient export from freshwater ecosystems by anadromous sockeye salmon (Oncorhynchus nerka). Can J Fish Aquat Sci 61:1582–1589Google Scholar
  84. Moore JW, Schindler DE (2010) Spawning salmon and the phenology of emergence in stream insects. Proc R Soc B 277:1695–1703Google Scholar
  85. Moore JW, Schindler DE, Carter JL, Fox J, Griffiths J, Holtgrieve GW (2007) Biotic control of stream fluxes: spawning salmon drive nutrient and matter export. Ecology 88:1278–1291Google Scholar
  86. Naiman RJ (2013) Socio-ecological complexity and the restoration of river ecosystems. Inland Waters 3:391–410Google Scholar
  87. Naiman RJ, Alldredge JR, Beauchamp DA, Bisson PA, Congleton J, Henny CJ, Huntly N, Lamberson R, Levings C, Merrill EN (2012) Developing a broader scientific foundation for river restoration: columbia River food webs. Proc Nat Acad Sci 109:21201–21207Google Scholar
  88. National Research Council (US) Committee on Protection, and Management of Pacific Northwest Anadromous Salmonids (1996) Upstream: salmon and society in the Pacific Northwest. National Academies PressGoogle Scholar
  89. Nelson PR, Edmondson WT (1955) Limnological effects of fertilizing Bare Lake, Alaska. Fish Bull Fish Wildlife Serv 56:413–436Google Scholar
  90. O’Keefe TC, Edwards RT (2003) Evidence for hyporheic transfer and removal of marine-derived nutrients in a sockeye stream in southwest Alaska. In: Stockner JG (ed) Nutrients in salmonid ecosystems: sustaining production and biodiversity. American Fisheries Society, Bethesda, pp 99–110Google Scholar
  91. Pearsons TN, Roley DD, Johnson CL (2007) Development of a carcass analog for nutrient restoration in streams. Fisheries 32:114–124Google Scholar
  92. Perrin CJ, Rosenau ML, Stables TB, Ashley KI (2006) Restoration of a montane reservoir fishery via biomanipulation and nutrient addition. N Am J Fish Manag 26:391–407Google Scholar
  93. Peterson DP, Foote CJ (2000) Disturbance of small-stream habitat by spawning sockeye salmon in Alaska. Trans Am Fish Soc 129:924–934Google Scholar
  94. Piccolo JJ, Wipfli MS (2002) Does red alder (Alnus rubra) in upland riparian forests elevate macroinvertebrate and detritus export from headwater streams to downstream habitats in southeastern Alaska? Can J Fish Aquat Sci 59:503–513Google Scholar
  95. Pinay G, O’Keefe TC, Edwards RT, Naiman RJ (2008) Nitrate removal in the hyporheic zone of a salmon river in Alaska. River Res Appl 25:367–375Google Scholar
  96. Poff NL, Huryn AD (1998) Multi-scale determinants of secondary production in Atlantic salmon (Salmo salar) streams. Can J Fish Aquat Sci 55:201–217Google Scholar
  97. Rabeni CF, Sowa SP (1996) Integrating biological realism into habitat restoration and conservation strategies for small streams. Can J Fish Aquat Sci 53:252–259Google Scholar
  98. Race MS, Fonseca MS (1996) Fixing compensatory mitigation: what will it take? Ecol Appl 6:94–101Google Scholar
  99. Rae RM, Frances RP, Hamilton PB, Ashley KI (1997) Effects of fertilization on phytoplankton in Kootenay Lake, British Columbia. Lake Reserv Manag 13:57–66Google Scholar
  100. Raymond HL (1979) Effects of dams and impoundments on migrations of juvenile Chinook salmon and steelhead from the Snake River, 1966 to 1975. Trans Am Fish Soc 108:505–529Google Scholar
  101. Reeves GH, Hall JD, Roelofs TD, Hickman TL, Baker CO (1991) Rehabilitating and modifying stream habitats. In Meehan WR (ed) Influences of forest and rangeland management on salmonid fishes and their habitats. American Fisheries Society, Special Publication 19, Bethesda, Maryland, pp 519–557Google Scholar
  102. Reisinger AJ, Chaloner DT, Rüegg J, Tiegs SD, Lamberti GA (2013) Effects of spawning Pacific salmon on the isotopic composition of biota differ among southeast Alaska streams. Freshw Biol 58:938–950Google Scholar
  103. Rex JF, Petticrew EL (2008) Delivery of marine-derived nutrients to streambeds by Pacific salmon. Nat Geosci 1:840–843Google Scholar
  104. Rinella DJ, Wipfli MS, Stricker CA, Heintz RA, Rinella MJ (2012) Pacific salmon (Oncorhynchus spp.) runs and consumer fitness: growth and energy storage in stream-dwelling salmonids increase with salmon spawner density. Can J Fish Aquat Sci 69:73–84Google Scholar
  105. Rinella DJ, Wipfli MS, Walker CM, Stricker CA, Heintz RA (2013) Seasonal persistence of marine-derived nutrients in south-central Alaskan salmon streams. Ecosphere 4:122Google Scholar
  106. Roni P, Beechie TJ, Bilby RE, Leonetti FE, Pollock MM, Pess GR (2002) A review of stream restoration techniques and a hierarchical strategy for prioritizing restoration in Pacific Northwest watersheds. N Am J Fish Manag 22:1–20Google Scholar
  107. Roni P, Hanson K, Beechie T (2008) Global review of the physical and biological effectiveness of stream habitat rehabilitation techniques. N Am J Fish Manag 28:856–890Google Scholar
  108. Rüegg J, Tiegs SD, Chaloner DT, Levi PS, Tank JL, Lamberti GA (2011) Salmon subsidies alleviate nutrient limitation of benthic biofilms in southeast Alaska streams. Can J Fish Aquat Sci 68:277–287Google Scholar
  109. Rüegg J, Chaloner DT, Levi PS, Tank JL, Tiegs SD, Lamberti GA (2012) Environmental variability and the ecological effects of spawning Pacific salmon on stream biofilm. Freshw Biol 57:129–142Google Scholar
  110. Sanderson BL, Coe HJ, Tran CD, Macneale KH, Harstad DL, Goodwin AB (2009) Nutrient limitation of periphyton in Idaho streams: results from nutrient diffusing substrate experiments. J N Am Benthol Soc 28:832–845Google Scholar
  111. Saunders WC, Fausch KD (2012) Grazing management influences the subsidy of terrestrial prey to trout in central Rocky Mountain streams (USA). Freshw Biol 57:1512–1529Google Scholar
  112. Scheuerell MD, Williams JG (2005) Forecasting climate-induced changes in the survival of Snake River spring/summer Chinook salmon (Oncorhynchus tshawytscha). Fish Oceanogr 14:448–457Google Scholar
  113. Scheuerell MD, Levin PS, Zabel RW, Williams JG, Sanderson BL (2005) A new perspective on the importance of marine-derived nutrients to threatened stocks of Pacific salmon (Oncorhynchus spp.). Can J Fish Aquat Sci 62:961–964Google Scholar
  114. Scheuerell MD, Moore JW, Schindler DE, Harvey CJ (2007) Varying effects of anadromous sockeye salmon on the trophic ecology of two species of resident salmonids in southwest Alaska. Freshw Biol 52:1944–1956Google Scholar
  115. Schindler DE, Scheuerell MD, Moore JW, Gende SM, Francis TB, Palen WJ (2003) Pacific salmon and the ecology of coastal ecosystems. Front Ecol Environ 1:31–37Google Scholar
  116. Schindler DE, Leavitt PR, Brock CS, Johnson SP, Quay PD (2005) Marine-derived nutrients, commercial fisheries, and production of salmon and lake algae in Alaska. Ecology 86:3225–3231Google Scholar
  117. Schuldt JA, Hershey AE (1995) Effects of salmon carcass decomposition on Lake Superior tributary streams. J N Am Benthol Soc 14:259–268Google Scholar
  118. Shaff CD, Compton JE (2009) Differential incorporation of natural spawners vs. artificially planted salmon carcasses in a stream food web: evidence from δ15 N of juvenile coho salmon. Fisheries 34:62–72Google Scholar
  119. Slaney PA, Ward BR, Wightman JC (2003) Experimental nutrient addition to the Keogh River and application to the Salmon River in Coastal British Columbia. In: Stockner JG (ed) Nutrients in salmonid ecosystems: sustaining production and biodiversity. American Fisheries Society, Bethesda, pp 111–126Google Scholar
  120. Slavik K, Peterson B, Deegan L, Bowden W, Hershey A, Hobbie J (2004) Long-term responses of the Kuparuk River ecosystem to phosphorus fertilization. Ecology 85:939–954Google Scholar
  121. Stockner JG (2003) Nutrients in salmonid ecosystems: sustaining production and biodiversity. American Fisheries Society Symposium 34, Bethesda, MarylandGoogle Scholar
  122. Tiegs SD, Campbell EY, Levi PS, Rüegg J, Benbow ME, Chaloner DT, Merritt RW, Tank JL, Lamberti GA (2009) Separating physical disturbance and nutrient enrichment caused by Pacific salmon in stream ecosystems. Freshw Biol 54:1864–1875Google Scholar
  123. Tiegs SD, Levi PS, Rüegg J, Chaloner DT, Tank JL, Lamberti GA (2011) Ecological effects of live salmon exceed those of carcasses during an annual spawning migration. Ecosystems 14:598–614Google Scholar
  124. Uchiyama TU, Finney BP, Adkison MD (2008) Effects of marine-derived nutrients on population dynamics of sockeye salmon (Oncorhynchus nerka). Can J Fish Aquat Sci 65:1635–1648Google Scholar
  125. Verspoor J, Braun D, Reynolds J (2010) Quantitative links between Pacific salmon and stream periphyton. Ecosystems 13:1020–1034Google Scholar
  126. Verspoor JJ, Braun DC, Stubbs MM, Reynolds JD (2011) Persistent ecological effects of a salmon-derived nutrient pulse on stream invertebrate communities. Ecosphere 2:art18Google Scholar
  127. Walters CJ, Holling CS (1990) Large-scale management experiments and learning by doing. Ecology 71:2060–2068Google Scholar
  128. Waples RS (1999) Dispelling some myths about hatcheries. Fisheries 24:12–21Google Scholar
  129. Ward DL, Boyce RR, Young FR, Olney FE (1997) A review and assessment of transportation studies for juvenile Chinook salmon in the Snake River. N Am J Fish Manag 17:652–662Google Scholar
  130. Ward BR, Slaney PA, McCubbing DJF (2007) Watershed restoration to reconcile fisheries and habitat impacts at the Keogh River in coastal British Columbia. In: Nielsen J, Dodson JJ, Friedland K, Hamon TR, Musick J, Verspoor E (eds) Reconciling fisheries with conservation: proceedings of the fourth world fisheries congress. American Fisheries Society, Bethesda, pp 587–601Google Scholar
  131. Waters T (1988) Fish production-benthos production relationships in trout streams. Pol Arch Hydrobiol 35:545–561Google Scholar
  132. Williams J (2008) Mitigating the effects of high-head dams on the Columbia River, USA: experience from the trenches. Hydrobiologia 609:241–251Google Scholar
  133. Wilson GA, Ashley KI, Land RW, Slaney PA (2003) Experimental enrichment of two oligotrophic rivers in south coastal British Columbia. In: Stockner JG (ed) Nutrients in salmonid ecosystems: sustaining production and biodiversity. American Fisheries Society, Bethesda, pp 149–162Google Scholar
  134. Wilzbach MA, Harvey BC, White JL, Nakamoto RJ (2005) Effects of riparian canopy opening and salmon carcass addition on the abundance and growth of resident salmonids. Can J Fish Aquat Sci 62:58–67Google Scholar
  135. Wipfli MS (1997) Terrestrial invertebrates as salmonid prey and nitrogen sources in streams: contrasting old-growth and young-growth riparian forests in southeastern Alaska, U.S.A. Can J Fish Aquat Sci 54:1259–1269Google Scholar
  136. Wipfli MS, Baxter CV (2010) Linking ecosystems, food webs, and fish production: subsidies in salmonid watersheds. Fisheries 35:373–387Google Scholar
  137. Wipfli MS, Gregovich DP (2002) Export of invertebrates and detritus from fishless headwater streams in southeastern Alaska: implications for downstream salmonid production. Freshw Biol 47:957–969Google Scholar
  138. Wipfli MS, Hudson J, Caouette J (1998) Influence of salmon carcasses on stream productivity: response of biofilm and benthic macroinvertebrates in southeastern Alaska, USA. Can J Fish Aquat Sci 55:1503–1511Google Scholar
  139. Wipfli MS, Hudson JP, Chaloner DT, Caouette JP (1999) Influence of salmon spawner densities on stream productivity in southeast Alaska. Can J Fish Aquat Sci 56:1600–1611Google Scholar
  140. Wipfli MS, Hudson JP, Caouette JP, Chaloner DT (2003) Marine subsidies in freshwater ecosystems: salmon carcasses increase the growth rates of stream-resident salmonids. Trans Am Fish Soc 132:371–381Google Scholar
  141. Wipfli MS, Hudson JP, Caouette JP (2004) Restoring productivity of salmon-based food webs: contrasting effects of salmon carcass and salmon carcass analog additions on stream-resident salmonids. Trans Am Fish Soc 133:1440–1454Google Scholar
  142. Wipfli MS, Hudson JP, Caouette JP, Mitchell NL, Lessard JL, Heintz RA, Chaloner DT (2010) Salmon carcasses increase stream productivity more than inorganic fertilizer pellets: a test on multiple trophic levels in streamside experimental channels. Trans Am Fish Soc 139:824–839Google Scholar

Copyright information

© Springer Science+Business Media New York 2015

Authors and Affiliations

  • Scott F. Collins
    • 1
    • 4
    Email author
  • Amy M. Marcarelli
    • 2
  • Colden V. Baxter
    • 1
  • Mark S. Wipfli
    • 3
  1. 1.Stream Ecology Center, Department of Biological SciencesIdaho State UniversityPocatelloUSA
  2. 2.Department of Biological SciencesMichigan Technological UniversityHoughtonUSA
  3. 3.U.S. Geological Survey, Alaska Cooperative Fish and Wildlife Research Unit, Institute of Arctic BiologyUniversity of Alaska FairbanksFairbanksUSA
  4. 4.Illinois Natural History SurveyKaskaskia Biological StationSullivanUSA

Personalised recommendations