Salmon carcasses increase stream productivity more than inorganic fertilizer pellets: A test on multiple trophic levels in streamside experimental channels

Transactions of the American Fisheries Society

Volumn 139, Issue 3, 2010, Pages 824-839

  Wipfli, Mark S ^a   Hudson, John P ^b,f   Caouette, John P ^c   Mitchell, Nicole L ^d   Lessard, Joanna L ^e   Heintz, Ron A ^b   Chaloner, Dominic T ^d  

^a UNIVERSITY OF ALASKA FAIRBANKS   (United States)

^b NATIONAL MARINE FISHERIES SERVICE   (United States)

^c THE NATURE CONSERVANCY   (United States)

^d UNIVERSITY OF NOTRE DAME   (United States)

^e MICHIGAN STATE UNIVERSITY   (United States)

^f U S FISH AND WILDLIFE SERVICE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMMONIUM; BIOCHEMICAL COMPOSITION; BIOFILM; BODY CONDITION; CHLOROPHYLL; COASTAL ZONE; CONCENTRATION (COMPOSITION); DRY MATTER; EXPERIMENTAL STUDY; FERTILIZER APPLICATION; FISHERY PRODUCTION; FOOD WEB; GROWTH RATE; HABITAT RESTORATION; JUVENILE; MESOCOSM; NITROGEN; NUTRIENT CYCLING; PHOSPHORUS; PHYSIOLOGICAL RESPONSE; POPULATION DECLINE; POPULATION DENSITY; SALMONID; SOLUBILIZATION; SPAWNING; STREAM; TROPHIC LEVEL;

NORTH AMERICA;

INVERTEBRATA; ONCORHYNCHUS KISUTCH;

EID: 79955126778     PISSN: 00028487     EISSN: 15488659     Source Type: Journal    
DOI: 10.1577/T09-114.1     Document Type: Article

References (77)

1. Adams, S. M. 1998. Ecological role of lipids in the health and success of fish populations. Pages 132-160 in M. T. Arts and B. C. Wainman, editors. Lipids in freshwater ecosystems. Springer-Verlag, New York.
2. Ambrose, H. E., M. A. Wilzbach, and K. W. Cummins. 2004. Periphyton response to increased light and salmon carcass introduction in northern California streams. Journal of the North American Benthological Society 23:701-712.
3. APHA (American Public Health Association), American Water Works Association, Water Environment Federation. 1992. Standard methods for the examination of water and wastewater, 18th edition. American Public Health Association, Washington, D.C.
4. APHA (American Public Health Association), American Water Works Association, Water Environment Federation. 1999. Standard methods for the examination of water and wastewater, 20th edition. APHA Publications, Washington, D.C.
5. Ashley, K. I., and P. A. Slaney. 1997. Accelerating recovery of stream, river and pond productivity by low-level nutrient enrichment. Pages 13-24 in P. A. Slaney and D. Zaldokas, editors. Fish habitat rehabilitation procedures. British Columbia Ministry of Environment, Lands and Parks and Ministry of Forests, Watershed Restoration Technical Circular 9, Vancouver.
6. Bagenal, T. B., and F. W. Tesch. 1978. Age and growth. Pages 101-136 in T. B. Bagenal, editor. Methods for assessment of fish production in fresh waters, 3rd edition. Blackwell Scientific Publications, Oxford.
7. Bilby, R. E., and P. A. Bisson. 1992. Allochthonous versus autochthonous organic matter contributions to the trophic support of fish populations in clear-cut and old-growth forested streams. Canadian Journal of Fisheries and Aquatic Sciences 49:540-551.
8. Bilby, R. E., B. R. Fransen, and P. A. Bisson. 1996. Incorporation of nitrogen and carbon from spawning coho salmon into the trophic system of small streams: evidence from stable isotopes. Canadian Journal of Fisheries and Aquatic Sciences 53:164-173.
9. Bilby, R. E., B. R. Fransen, P. A. Bisson, and J. K. Walter. 1998. Response of juvenile coho salmon (Oncorhynchus kisutch) and steelhead (Oncorhynchus mykiss) to the addition of salmon carcasses to two streams in southwestern Washington, U.S.A. Canadian Journal of Fisheries and Aquatic Sciences 55:1909-1918.
10. Bilby, R. E., B. R. Fransen, J. K. Walter, C. J. Cederholm, and W. J. Scarlett. 2001. Preliminary evaluation of the use of nitrogen stable isotope ratios to establish escapement levels for Pacific salmon. Fisheries 26(1):6-14.
11. Bisson, P. A., and R. E. Bilby. 1998. Organic matter and trophic dynamics. Pages 373-398 in R. J. Naiman and R. E. Bilby, editors. River ecology and management. Springer-Verlag, New York.
12. Borchardt, M. A. 1996. Nutrients. Pages 183-227 in R. J. Stevenson, M. L. Bothwell, and R. L. Lowe, editors. Algal ecology. Academic Press, San Diego, California.
13. Bothwell, M. L. 1989. Phosphorus-limited growth dynamics of lotic periphytic diatom communities: areal biomass and cellular growth rate responses. Canadian Journal of Fisheries and Aquatic Sciences 46:1293-1301.
14. Cederholm, C. J., D. B. Houston, D. L. Cole, and W. J. Scarlett. 1989. Fate of coho salmon (Oncorhynchus kisutch) carcasses in spawning streams. Canadian Journal of Fisheries and Aquatic Sciences 46:1347-1355.
15. Cederholm, C. J., M. D. Kunze, T. Murota, and A. Sibatani. 1999. Pacific salmon carcasses: essential contribution of nutrients and energy for aquatic and terrestrial ecosystems. Fisheries 24(10):6-15.
16. Chaloner, D. T., K. M. Martin, M. S. Wipfli, P. H. Ostrom, and G. A. Lamberti. 2002a. Marine carbon and nitrogen in southeastern Alaska stream food webs: evidence from artificial and natural streams. Canadian Journal of Fisheries and Aquatic Sciences 59:1257-1265.
17. Chaloner, D. T., and M. S. Wipfli. 2002. Influence of decomposing Pacific salmon carcasses on macroinvertebrate growth and standing stock in southeastern Alaska streams. Journal of the North American Benthological Society 21:430-442.
18. Chaloner, D. T., M. S. Wipfli, and J. P. Caouette. 2002b. Mass loss and macroinvertebrate colonization of Pacific salmon carcasses in southeastern Alaska streams. Freshwater Biology 47:263-273.
19. Cummins, K. W., M. A. Wilzbach, D. M. Gates, J. B. Perry, and W. B. Taliaferro. 1989. Shredders and riparian vegetation: leaf litter that falls into streams influences communities of stream invertebrates. BioScience 39:24-30.
20. Elser, J. J., and J. Urabe. 1999. The stoichiometry of consumer-driven nutrient cycling: theory, observations, and consequences. Ecology 80:735-751.
21. Gende, S. M., R. T. Edwards, M. F. Willson, and M. S. Wipfli. 2002. Pacific salmon in aquatic and terrestrial ecosystems. BioScience 52:917-928.
22. Gende, S. M., T. P. Quinn, M. F. Willson, R. Heintz, and T. M. Scott. 2004. Magnitude and fate of salmon-derived nutrients and energy in a coastal stream ecosystem. Journal of Freshwater Ecology 19(1):149-160.
23. Giannico, G. R., and S. G. Hinch. 2007. Juvenile coho salmon (Oncorhynchus kisutch) responses to salmon carcasses and in-stream wood manipulations during winter and spring. Canadian Journal of Fisheries and Aquatic Sciences 64:324-335.
24. Gresh, T., J. Lichatowich, and P. Schoonmaker. 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(1):15-21.
25. Grimm, N. B., and S. G. Fisher. 1986. Nitrogen limitation in a Sonoran Desert stream. Journal of the North American Benthological Society 5:2-15.
26. Groot, C., and L. Margolis. 1991. Pacific salmon life histories. University of British Columbia Press, Vancouver.
27. Heintz, R. A., B. D. Nelson, J. Hudson, M. Larsen, L. Holland, and M. Wipfli. 2004. Marine subsidies in freshwater: effects of salmon carcasses on lipid class and fatty acid composition of juvenile coho salmon. Transactions of the American Fisheries Society 133:559-567.
28. Heintz, R. A., M. S. Wipfli, and J. P. Hudson. 2010. Identification of marine-derived lipids in juvenile coho salmon and aquatic insects through fatty acid analysis. Transactions of the American Fisheries Society 139:840-854.
29. Hicks, B. J., M. S. Wipfli, D. W. Lang, and M. E. Lang. 2005. Marine-derived nitrogen and carbon in freshwater- riparian food webs of the Copper River Delta, southcentral Alaska. Oecologia 144:558-569.
30. Holmes, R. M., A. Aminot, R. Kerouel, B. A. Hooker, and B. J. Peterson. 1999. A simple and precise method for measuring ammonium in marine and freshwater ecosystems. Canadian Journal of Fisheries and Aquatic Sciences 56:1801-1808.
31. Johnston, N. T., J. S. Macdonald, K. J. Hall, and P. J. Tschaplinski. 1997. A preliminary study of the role of sockeye salmon (Oncorhynchus nerka) carcasses as carbon and nitrogen sources for benthic insects and fishes in the "early Stuart" stock spawning streams, 1050 km from the ocean. Fish Project Report RD55, British Colombia Ministry of Environment, Lands and Parks, Victoria, British Colombia, Canada.
32. Johnston, N. T., E. A. MacIsaac, P. J. Tschaplinski, and K. J. Hall. 2004. Effects of the abundance of spawning sockeye salmon (Oncorhynchus nerka) on nutrients and algal biomass in forested streams. Canadian Journal of Fisheries and Aquatic Sciences 61:384-403.
33. Johnston, N. T., C. J. Perrin, P. A. Slaney, and B. R. Ward. 1990. Increased juvenile salmonid growth by whole-river fertilization. Canadian Journal of Fisheries and Aquatic Sciences 47:862-872.
34. Kamphake, L. J., S. A. Hannah, and J. M. Cohen. 1967. Automated analysis for nitrate by hydrazine reduction. Water Research 1:205-216.
35. Kline, T. C., J. J. Goering, O. A. Mathisen, P. H. Poe, and P. L. Parker. 1990. Recycling of elements transported upstream by runs of Pacific salmon I: d15N and d13C evidence in Sashin Creek, southeastern Alaska. Canadian Journal of Fisheries and Aquatic Sciences 47:136-144.
36. Kline, T. C., J. J. Goering, and R. J. Piorkowski. 1997. The effect of salmon carcasses on Alaskan freshwaters. Pages 179-204 in A. M. Milner and M. W. Oswood, editors. Freshwaters of Alaska: ecological syntheses. Springer-Verlag, New York.
37. Kohler, A. E., A. Rugenski, and D. Taki. 2008. Stream food web response to a salmon carcass analogue addition in two central Idaho, U.S.A., streams. Freshwater Biology 53:446-460.
38. Lessard, J. L., and R. W. Merritt. 2006. Influence of marinederived nutrients from spawning salmon on aquatic insect communities in southeast Alaskan streams. Oikos 113:334-343.
39. Lessard, J. L., R. W. Merritt, and M. B. Berg. 2009. Investigating the effect of marine-derived nutrients from spawning salmon on macroinvertebrate secondary production in southeast Alaskan streams. Journal of the North American Benthological Society 28:683-693.
40. Levy, S. 1997. Pacific salmon bring it all back home. BioScience 47:657-660.
41. Lohman, K., and J. C. Priscu. 1992. Physiological indicators of nutrient deficiency in Cladophora (Chlorophyta) in the Clark Fork of the Columbia River, Montana. Journal of Phycology 28:443-448.
42. Mason, J. C. 1976. Response of underyearling coho salmon to supplemental feeding in a natural stream. Journal of Wildlife Management 40:775-788.
43. Meyer, J. L. 1997. Stream health: incorporating the human dimension to advance stream ecology. Journal of the North American Benthological Society 16:439-447.
44. Meyer, J. L., and J. B. Wallace. 2001. Lost linkages and lotic ecology: rediscovering small streams. Pages 295-317 in M. C. Press, N. J. Huntly, and S. Levin, editors. Ecology: achievement and challenge. Blackwell Scientific Publications, Oxford, UK.
45. Minakawa, N., and R. I. Gara. 1999. Ecological effects of a chum salmon (Oncorhynchus keta) spawning run in a small stream of the Pacific Northwest. Journal of Freshwater Ecology 14:327-335.
46. Mitchell, N. L., and G. A. Lamberti. 2005. Responses in dissolved nutrients and epilithon abundance to spawning salmon in southeast Alaska streams. Limnology and Oceanography 50:217-227.
47. Montgomery, D. C. 1991. Design and analysis of experiments, 3rd edition. Wiley, New York.
48. Mundie, J. H., S. M. McKinnell, and R. E. Traber. 1983. Responses of stream zoobenthos to enrichment of gravel substrates with cereal grain. Canadian Journal of Fisheries and Aquatic Sciences 40:1702-1712.
49. Mundie, J. H., K. S. Simpson, and C. J. Perrin. 1991. Responses of stream periphyton and benthic insects to increases in dissolved inorganic phosphorus in a mesocosm. Canadian Journal of Fisheries and Aquatic Sciences 48:2061-2072.
50. Murphy, M. L. 1998. Primary production. Pages 144-168 in R. J. Naiman and R. E. Bilby, editors. River ecology and management. Springer-Verlag, New York.
51. Naiman, R. J., R. E. Bilby, D. E. Schindler, and J. M. Helfield. 2002. Pacific salmon, nutrients, and the dynamics of freshwater ecosystems. Ecosystems 5:399-417.
52. Olsen, Y. 1998. Lipids and essential fatty acids in aquatic food webs: what can freshwater ecologists learn from mariculture? Pages 161-202 in M. T. Arts and B. C. Wainman, editors. Lipids in freshwater ecosystems. Springer-Verlag, New York.
53. Pearsons, T. N., D. D. Roley, and C. L. Johnson. 2007. Development of a carcass analogue for nutrient restoration in streams. Fisheries 32:114-124.
54. Perrin, C. J., M. L. Bothwell, and P. A. Slaney. 1987. Experimental enrichment of a coastal stream in British Columbia: effects of organic and inorganic additions on autotrophic periphyton production. Canadian Journal of Fisheries and Aquatic Sciences 44:1247-1256.
55. Perrin, C. J., and J. S. Richardson. 1997. N and P limitation of benthos abundance in the Nechako River, British Columbia. Canadian Journal of Fisheries and Aquatic Sciences 54:2574-2583.
56. Peterson, B. J., L. Deegan, J. Helfrich, J. E. Hobbie, M. Hullar, B. Mollar, T. E. Ford, A. E. Hershey, A. Hiltner, G. Kipphut, M. A. Lock, D. M. Fiebig, V. McKinley, M. C. Miller, J. R. Vestal, R. Ventullo, and G. Volk. 1993. Biological responses of a tundra river to fertilization. Ecology 74:653-672.
57. Sanderson, B. L., H. J. Coe, C. D. Tran, K. H. Macneale, D. L. Harstad, and A. B. Goodwin. 2009. Nutrient limitation of periphyton in Idaho streams: results from nutrient diffusing substrate experiments. Journal of the North American Benthological Society 28:832-845.
58. SAS Institute. 1989. SAS/STAT user's guide, version 6, edition 4, volume 2. SAS Institute, Cary, North Carolina.
59. Scheuerell, M. D., J. W. Moore, D. E. Schindler, and C. J. Harvey. 2007. Varying effects of anadromous salmon on the trophic ecology of two species of resident stream fishes in southwest Alaska. Freshwater Biology 52:1944-1956.
60. Shapiro, S., and M. Wilk. 1965. An analysis of variance test for normality. Biometrika 52:591-9.
61. Snedecor, G., W. Cochran, and D. Cox. 1989. Statistical methods, 8th edition. Iowa State University Press, Ames.
62. Sokal, R., and J. Rohlf. 1995. Biometry, 3rd edition. Freeman, New York.
63. Steinman, A. D., G. A. Lamberti, and P. R. Leavitt. 2006. Biomass and pigments of benthic algae. Pages 357-380 in F. R. Hauer and G. A. Lamberti, editors. Methods in stream ecology, 2nd edition. Elsevier, Amsterdam, The Netherlands.
64. Stevenson, R. J., M. L. Bothwell, and R. L. Lowe, editors. 1996. Alga ecology: freshwater benthic ecosystems. Academic Press, New York.
65. Stockner, J. G., and K. R. S. Shortreed. 1978. Enhancement of autotrophic production by nutrient addition in a coastal rainforest stream on Vancouver Island. Journal of the Fisheries Research Board of Canada 35:28-34.
66. Stockner, J. G. 2003. Nutrients in salmonid ecosystems: sustaining production and biodiversity. American Fisheries Society, Symposium 34, Bethesda, Maryland.
67. Suberkropp, K. F. 1998. Microorganisms and organic matter decomposition. Pages 120-143 in R. J. Naiman and R. E. Bilby, editors. River ecology and management. Springer-Verlag, New York.
68. Vannote, R. L., G. W. Minshall, K. W. Cummins, J. R. Sedell, and C. E. Cushing. 1980. The river continuum concept. Canadian Journal of Fisheries and Aquatic Sciences 37:130-137.
69. Wallace, J. B., S. L. Eggert, J. L. Meyer, and J. R. Webster. 1997. Multiple trophic levels of a forest stream linked to terrestrial litter inputs. Science 277:102-104.
70. Wallace, J. B., S. L. Eggert, J. L. Meyer, and J. R. Webster. 1999. Effects of resource limitation on a detrital-based ecosystem. Ecological Monographs 69:409-442.
71. Willson, M. F., S. M. Gende, and B. Marston. 1998. Fishes and the forest: expanding perspectives on fish-wildlife interactions. BioScience 48:455-462.
72. Wilzbach, M. A., B. C. Harvey, J. L. White, and R. J. Nakamoto. 2005. Effects of riparian canopy opening and salmon carcass addition on the abundance and growth of resident salmonids. Canadian Journal of Fisheries and Aquatic Sciences 62:58-67.
73. Wipfli, M. S. 1997. Terrestrial invertebrates as salmonid prey and nitrogen sources in streams: contrasting old-growth and young-growth riparian forests in southeastern Alaska, USA. Canadian Journal of Fisheries and Aquatic Sciences 54:1259-1269.
74. Wipfli, M. S., J. P. Hudson, and J. P. Caouette. 1998. Influence of salmon carcasses on stream productivity: response of biofilm and benthic macroinvertebrates in southeastern Alaska, USA. Canadian Journal of Fisheries and Aquatic Sciences 55:1503-1511.
75. Wipfli, M. S., J. P. Hudson, and J. P. Caouette. 2004. Restoring productivity of salmon-based food webs: contrasting effects of salmon carcass and salmon carcass analog additions on stream-resident salmonids. Transactions of the American Fisheries Society 133:1440-1454.
76. Wipfli, M. S., J. P. Hudson, J. P. Caouette, and D. T. Chaloner. 2003. Marine subsidies in freshwater ecosystems: salmon carcasses increase the growth rates of stream-resident salmonids. Transactions of the American Fisheries Society 132:371-381.
77. Wipfli, M. S., J. P. Hudson, D. T. Chaloner, and J. P. Caouette. 1999. Influence of salmon spawner densities on stream productivity in southeast Alaska. Canadian Journal of Fisheries and Aquatic Sciences 56:1600-1611.