Abstract
Migratory animals often transfer nutrients between ecosystems, enhancing productivity in the subsidized system. Most research on nutrient subsidies by migratory fishes has focused on Pacific salmon, whose semelparous life history is unusual among migratory fishes. To test whether iteroparous species can provide ecologically important nutrient inputs to stream ecosystems, we experimentally blocked the migration of suckers (Catostomidae) midway up an oligotrophic tributary of Lake Michigan. Comparing reaches upstream of the barrier to downstream reaches containing thousands of breeding fish, we found that suckers elevated phosphorus and nitrogen concentrations three- to five-fold. Algal accrual was doubled and caddisflies grew 12% larger in subsidized reaches relative to reference reaches. An enclosure experiment demonstrated that caddisflies with access to a fish carcass rapidly became enriched in 15N and 13C, and experimental carcass additions were rapidly colonized by high densities of caddisflies. However, under natural conditions below the experimental barrier, caddisflies became enriched in 15N but not 13C, indicating that fish-derived nutrients entered the stream food web primarily through indirect pathways rather than direct consumption of carcasses or gametes. At pupation, an average of 18% of caddisfly tissue N below the barrier was sucker-derived. In comparison to our focal stream, a reference stream with few suckers showed no seasonal or longitudinal patterns in nutrients and stable isotopes. These results demonstrate that iteroparous fish migrations can spur productivity via nutrient subsidies, despite low mortality rates. Thus, concerns about negative ecosystem-level consequences of blocking migrations of semelparous fishes are also applicable to iteroparous species when migrations are large.
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Baxter CV, Fausch KD, Saunders WC. 2005. Tangled webs: reciprocal flows of invertebrate prey link streams and riparian zones. Freshw Biol 50:201–20.
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 53:164–173.
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 55:1909–18.
Browder RG, Garman GC. 1994. Increased ammonium concentrations in a tidal freshwater stream during residence of migratory Clupeid fishes. Trans Am Fish Soc 123:993–6.
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 21:430–42.
Christie KS, Reimchen TE. 2008. Presence of salmon increases passerine density on Pacific Northwest streams. Auk 125:51–9.
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 63:1230–41.
Durbin AG, Nixon SW, Oviatt CA. 1979. Effects of the spawning migration of the alewife, Alosa pseudoharengus, on freshwater ecosystems. Ecology 60:8–17.
Epanchin PN, Knapp RA, Lawler SP. 2010. Nonnative trout impact an alpine-nesting bird by altering aquatic-insect subsidies. Ecology 91:2406–15.
Finlay JC, Power M, Cabana G. 1999. Effects of water velocity on algal carbon isotope ratios: implications for river food web studies. Limnol Oceanogr 44:1198–203.
Flecker AS, McIntyre PB, Moore J, Anderson J, Taylor B, Hall RJ. 2010. Migratory fishes as material and process subsidies in riverine ecosystems. In: Gido KB, Jackson D, Eds. Community ecology of stream fishes: concepts, approaches, and techniques. Bethesda, MD: American Fisheries Society, Symposium 73. p. 559–592.
France R. 1996. Ontogenetic shift in crayfish delta C-13 as a measure of land-water ecotonal coupling. Oecologia 107:239–42.
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 63:2543–52.
Freeman MC, Pringle CM, Greathouse EA, Freeman NJ. 2003. Ecosystem-level consequences of migratory faunal depletion caused by dams. Trans Am Fish Soc 35:255–66.
Fry B. 2006. Stable isotope ecology. Berlin: Springer.
Han HJ, Allan JD, Scavia D. 2009. Influence of climate and human activities on the relationship between watershed nitrogen input and river export. Environ Sci Technol 43:1916–22.
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 144:558–69.
Hilderbrand GV, Hanley T, Robbins C, Schwartz C. 1999. Role of brown bears (Ursus arctos) in the flow of marine nitrogen into a terrestrial ecosystem. Oecologia 121:546–50.
Holtgrieve GW, Schindler DE. 2011. Marine-derived nutrients, bioturbation, and ecosystem metabolism: reconsidering the role of salmon in streams. Ecology 92:373–85.
Holtgrieve GW, Schindler DE, Gowell CP, Ruff CP, Lisi PJ. 2010. Stream geomorphology regulates the effects on periphyton of ecosystem engineering and nutrient enrichment by Pacific salmon. Freshw Biol 55:2598–611.
Honek A. 1993. Intraspecific variation in body size and fecundity in insects: a general relationship. Oikos 66:483–92.
Janetski DJ, Chaloner DT, Tiegs SD, Lamberti GA. 2009. Pacific salmon effects on stream ecosystems: a quantitative synthesis. Oecologia 159:583–95.
Jannot JE. 2009. Life history plasticity and fitness in a caddisfly in response to proximate cues of pond-drying. Oecologia 161:267–77.
Januchowski-Hartley SR, McIntyre PB, Diebel M, Doran PJ, Infante DM, Joseph C, Allan JD. 2013. Restoring aquatic ecosystem connectivity requires expanding inventories of both dams and road crossings. Front Ecol Environ 11:211–17.
Johansson A, Nilsson A. 1992. Dytiscus latissimus and D. circumcinctus larvae as predators on three case-making caddis larvae. Hydobiologia 248:201–13.
Juday C, Rich WH, Kemmerer GI, Mann A. 1932. Limnological studies of Karluk Lake, Alaska, 1926–1930. Bull US Bur Fish 47:407–36.
Klingler GL, Adams JV, Heinrich JW. 2003. Passage of four teleost species prior to sea lamprey (Petromyzon marinus) migration in eight tributaries of Lake Superior, 1954 to 1979. J Great Lakes Res 29:403–9.
Levi PS, Tank JL, Ruegg J, Janetski DJ, Tiegs SD, Chaloner DT, Lamberti GA. 2013. Whole-stream metabolism responds to spawning Pacific salmon in their native and introduced ranges. Ecosystems 16:269–83.
Liermann CR, Nilsson C, Robertson J, Ng RY. 2012. Implications of dam obstruction for global freshwater fish diversity. Bioscience 62:539–48.
Marczak LB, Thompson RM, Richardson JS. 2007. Meta-analysis: trophic level, habitat, and productivity shape the food web effects of resource subsidies. Ecology 88:140–8.
McIntyre PB, Flecker AS. 2010. Ecological stoichiometry as an integrative framework in stream fish ecology. In: Gido KB, Jackson D, Eds. Community ecology of stream fishes: concepts, approaches, and techniques. Bethesda, MD: American Fisheries Society, Symposium 73. p. 539–558.
McCutchan JH Jr, Lewis WM Jr, Kendall C, McGrath CC. 2003. Variation in trophic shift for stable isotope ratios of carbon, nitrogen, and sulfur. Oikos 102:378–90.
Merritt RW, Cummins KW, Berg MB, Eds. 2008. Introduction to the aquatic insects of North America. 4th edn. Dubuque, IA: Kendall Hunt.
Moore JW, Schindler DE. 2008. Biotic disturbance and benthic community dynamics in salmon-bearing streams. J Anim Ecol 77:275–84.
Moore JW, Schindler DE, Ruff CP. 2008. Habitat saturation drives thresholds in stream subsidies. Ecology 89:306–12.
Moore JW, Schindler DE, Scheuerell MD. 2004. Disturbance of freshwater habitats by anadromous salmon in Alaska. Oecologia 139:298–308.
Naiman RJ, Bilby RE, Schindler DE, Helfield JM. 2002. Pacific salmon, nutrients, and the dynamics of freshwater and riparian ecosystems. Ecosystems 5:399–417.
Nakano S, Murakami M. 2001. Reciprocal subsidies: dynamic interdependence between terrestrial and aquatic food webs. Proc Nat Acad Sci USA 98:166–70.
Page LM, Johnston C. 1990. Spawning in the creek chubsucker, Erimyzon oblongus, with a review of spawning behavior in suckers. Environ Biol Fish 27:265–72.
Petersson E. 1989. Swarming activity patterns and seasonal decline in adult size in some caddisflies (Trichoptera, Leptoceridae). Aquat Insects 11:17–28.
Phillips DL, Gregg JW. 2001. Uncertainty in source partitioning using stable isotopes. Oecologia 127:171–9.
Polis GA, Power ME, Huxel GRE. 2004. Food webs at the landscape level. Chicago: University of Chicago Press.
Post DM. 2002. Using stable isotopes to estimate trophic position: models, methods, and assumptions. Ecology 83:703–718.
Pracheil BM, McIntyre PB, Lyons JD. 2013. Enhancing conservation of large-river biodiversity by accounting for tributaries. Front Ecol Environ 11:124–8.
R Development Core Team. 2010. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org.
Reichert WL, Greene CM, Bilby RE. 2008. Seasonal variations in stable isotope ratios of juvenile coho salmon (Oncorhynchus kisutch) from western Washington rivers. Can J Fish Aquat Sci 65:681–90.
Robertson DM. 1997. Regionalized loads of sediment and phosphorus to Lakes Michigan and Superior: high flow and long-term average. J Great Lakes Res 23:416–39.
Rowe L, Ludwig D. 1991. Size and timing of metamorphosis in complex life-cycles: time constraints and variation. Ecology 72:413–27.
Ruegg J, Chaloner DT, Levi PS, Tank JL, Tiegs SD, Lamberti GA. 2012. Environmental variability and the ecological effects of spawning Pacific salmon on stream biofilms. Freshw Biol 57:129–42.
Schuldt JA, Hershey AE. 1995. Effect of salmon carcass decomposition on Lake Superior tributary streams. J N Am Benthol Soc 14:259–68.
Stanley EH, Doyle MW. 2003. Trading off: the ecological effects of dam removal. Front Ecol Environ 1:15–22.
Svensson BW. 1975. Morphometric variation of adult Potamophylax cingulatus (Trichoptera) reflecting environmental heterogeneity in a South Swedish stream. Oikos 26:365–77.
Taylor BW, Keep CF, Hall RO, Koch B, Tronstad L, Flecker AS, Ulseth A. 2007. Improving the fluorometric ammonium method: matrix effects, background fluorescence, and standard additions. J N Am Benthol Soc 26:167–77.
Tiegs SD, Levi P, Ruegg J, Tank J, Lamberti G. 2011. Ecological effects of live salmon exceed those of carcasses during an annual spawning migration. Ecosystems 14:598–614.
Verspoor JJ, Braun DC, Reynolds JD. 2010. Quantitative links between Pacific salmon and stream periphyton. Ecosystems 13:1020–34.
Walters AW, Barnes RT, Post DM. 2009. Anadromous alewives (Alosa pseudoharengus) contribute marine-derived nutrients to coastal stream food webs. Can J Fish Aquat Sci 66:439–48.
Walton BD. 1980. The reproductive biology, early life history, and growth of white suckers, Catostomus commersonii, and longnose suckers, C. catostomus, in the Willow Creek-Chain Lakes system, Alberta. University of Alberta.
West DC, Walters AW, Gephard S, Post DM. 2010. Nutrient loading by anadromous alewife (Alosa pseudoharengus): contemporary patterns and predictions for restoration efforts. Can J Fish Aquat Sci 67:1211–20.
Woodland RJ, Magnan P, Glemet H, Rodriguez MA, Cabana G. 2012. Variability and directionality of temporal changes in delta C-13 and delta N-15 of aquatic invertebrate primary consumers. Oecologia 169:199–209.
Ziv G, Baran E, Nam S, Rodriguez-Iturbe I, Levin SA. 2012. Trading-off fish biodiversity, food security, and hydropower in the Mekong Basin. Proc Nat Acad Sci USA 109:5609–14.
Acknowledgments
We thank P. Doran, T. Zorn, M. Hermann, D. Kramer, and J. LeMoine for logistical assistance, A. Nilsson for sharing data, and especially Phylis and Leo Hazen for site access. J. Fenner, A. Layman, J. Olsen, and R. Papke helped in the field. Funding was provided by Rackham Graduate School and a Doris Duke Conservation Fellowship (ESC), Smith Fellowship program (PBM), and University of Michigan School of Natural Resources and Environment (JDA).
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ESC conceived of and designed the study, performed the research, analyzed the data, and wrote the paper. JDA conceived of and designed the study and provided editorial suggestions. PBM conceived of and designed the study, performed research, and provided editorial suggestions.
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Childress, E.S., Allan, J.D. & McIntyre, P.B. Nutrient Subsidies from Iteroparous Fish Migrations Can Enhance Stream Productivity. Ecosystems 17, 522–534 (2014). https://doi.org/10.1007/s10021-013-9739-z
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DOI: https://doi.org/10.1007/s10021-013-9739-z