Skip to main content
Log in

Large predators and biogeochemical hotspots: brown bear (Ursus arctos) predation on salmon alters nitrogen cycling in riparian soils

  • Original Article
  • Published:
Ecological Research

Abstract

Two important themes in ecology include the understanding of how interactions among species control ecosystem processes, and how habitats can be connected through transfers of nutrients and energy by mobile organisms. An impressive example of both is the large influx of nutrients and organic matter that anadromous salmon supply to inland aquatic and terrestrial ecosystems and the role of predation by brown bears (Ursus arctos) in transferring these marine-derived nutrients (MDN) from freshwater to riparian habitats. In spite of the recognition that salmon-bear interactions likely play an important role in controlling the flux of MDN from aquatic to riparian habitats, few studies have linked bear predation on salmon to processes such as nitrogen (N) or carbon (C) cycling. We combine landscape-level survey data and a replicated bear-exclosure experiment to test how bear foraging on salmon affects nitrous oxide (N2O) flux, carbon dioxide (CO2) flux, and nutrient concentrations of riparian soils. Our results show that bears feeding on salmon increased soil ammonium (NH4 +) concentrations three-fold and N2O flux by 32-fold. Soil CO2 flux, nitrate (NO3 ), and N transformation differences were negligible in areas where bears fed on salmon. Reference areas without concentrated bear activity showed no detectable change in soil N cycling after the arrival of salmon to streams. Exclosure experiments showed that bear effects on soil nutrient cycles were transient, and soil N processing returned to background conditions within 1 year after bears were removed from the system. These results suggest that recipient ecosystems do not show uniform responses to MDN inputs and highlight the importance of large mobile consumers in generating landscape heterogeneity in nutrient cycles.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Allison SD, Czimczik CI, Treseder KK (2008) Microbial activity and soil respiration under nitrogen addition in Alaskan boreal forest. Glob Change Biol 14:1156–1168. doi:10.1111/j.1365-2486.2008.01549.x

    Article  Google Scholar 

  • Ben-David M, Bowyer RT, Duffy LK, Roby DD, Schell DM (1998) Social behavior and ecosystem processes: river otter latrines and nutrient dynamics of terrestrial vegetation. Ecology 79:2567–2571

    Google Scholar 

  • Bilby RE, Beach EW, Fransen BR, Walter JK, Bisson PA (2003) Transfer of nutrients from spawning salmon to riparian vegetation in western Washington. Trans Am Fish Soc 132:733–745. doi:10.1577/T02-089

    Article  Google Scholar 

  • Bol R, Petersen SO, Christofides C, Dittert K, Hansens MN (2004) Short-term N2O, CO2, NH3 fluxes, and N/C transfers in a Danish grass-clover pasture after simulated urine deposition in autumn. J Soil Sci Plant Nut 167:568–576. doi:10.1002/jpln.200321334

    Article  CAS  Google Scholar 

  • Chapin FS, Matson PA, Mooney HA (2002) Principles of terrestrial ecosystem ecology. Springer, Berlin Heidelberg New York

    Google Scholar 

  • Daily GC (ed) (1997) Nature’s services: societal dependence on natural ecosystems. Island Press, Washington, DC

  • Davidson EA, Keller M, Erickson HE, Verchot LV, Veldkamp E (2000) Testing a conceptual model of soil emissions of nitrous and nitric oxides. Bioscience 50:667–680. doi:10.1641/0006-3568(2000)050[0667:TACMOS]2.0.CO;2

    Article  Google Scholar 

  • Drake DC, Smith JV, Naiman RJ (2005) Salmon decay and nutrient contributions to riparian forest soils. Northwest Sci 79:61–71

    CAS  Google Scholar 

  • Drake DC, Naiman RJ, Bechtold JS (2006) Fate of nitrogen in riparian forest soils and trees: an N-15 tracer study simulating salmon decay. Ecology 87:1256–1266. doi:10.1890/0012-9658(2006)87[1256:FONIRF]2.0.CO;2

    Article  PubMed  Google Scholar 

  • Eichner MJ (1990) Nitrous oxide emissions from fertilized soils: summary of available data. J Environ Qual 19:272–280

    Article  Google Scholar 

  • Erickson H, Keller M, Davidson EA (2001) Nitrogen oxide fluxes and nitrogen cycling during postagricultural succession and forest fertilization in the humid tropics. Ecosystems (NY, Print) 4:67–84. doi:10.1007/s100210000060

    Article  CAS  Google Scholar 

  • Feeley KJ, Terborgh JW (2005) The effects of herbivore density on soil nutrients and tree growth in tropical forest fragments. Ecology 86:116–124. doi:10.1890/03-0657

    Article  Google Scholar 

  • Fellman JB, Hood E, Edwards RT, D’Amore DV (2008) Return of salmon-derived nutrients from the riparian zone to the stream during a storm in southeastern Alaska. Ecosystems (NY, Print) 11:537–544. doi:10.1007/s10021-008-9139-y

    Article  CAS  Google Scholar 

  • 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 63:2543–2552. doi:10.1139/F06-144

    Article  Google Scholar 

  • Gende SM, Edwards RT, Willson MF, Wipfli MS (2002) Pacific salmon in aquatic and terrestrial ecosystems. Bioscience 52:917–928. doi:10.1641/0006-3568(2002)052[0917:PSIAAT]2.0.CO;2

    Article  Google Scholar 

  • Gende SM, Quinn TP, Willson MF, Heintz R, Scott TM (2004) Magnitude and fate of salmon-derived nutrients and energy in a coastal stream ecosystem. J Freshw Ecol 19:149–160

    CAS  Google Scholar 

  • Gende SM, Miller AE, Hood E (2007) The effects of salmon carcasses on soil nitrogen pools in a riparian forest of southeastern Alaska. Can J For Res 37:1194–1202. doi:10.1139/X06-318

    Article  CAS  Google Scholar 

  • Giblin AE, Nadelhoffer KJ, Shaver GR, Laundre JA, McKerrow AJ (1991) Biogeochemical diversity along a riverside toposequence in arctic Alaska. Ecol Monogr 61:415–435. doi:10.2307/2937049

    Article  Google Scholar 

  • 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 25:15–21. doi:10.1577/1548-8446(2000)025<0015:AEOHAC>2.0.CO;2

    Article  Google Scholar 

  • Hart SC, Stark JM, Davidson EA, Firestone MK (1994) Nitrogen mineralization, immobilization, and nitrification. In: Weaver RW, Angle S, Bottomley P, Bezdicek D, Smith S, Tabatabai A, Wollum A (eds) Methods of soil analysis, Part 2. Microbiological and biochemical properties. Soil Science Society of America, Madison, WI, pp 985–1018

    Google Scholar 

  • Hedin LO, von Fischer JC, Ostrom NE, Kennedy BP, Brown MG, Robertson GP (1998) Thermodynamic constraints on nitrogen transformations and other biogeochemical processes at soil-stream interfaces. Ecology 79:684–703

    Google Scholar 

  • Helfield JM, Naiman RJ (2001) Effects of salmon-derived nitrogen on riparian forest growth and implications for stream productivity. Ecology 82:2403–2409

    Google Scholar 

  • Helfield JM, Naiman RJ (2006) Keystone interactions: salmon and bear in riparian forests of Alaska. Ecosystems (NY, Print) 9:167–180. doi:10.1007/s10021-004-0063-5

    Article  Google Scholar 

  • Hilderbrand GV, Hanley TA, Robbins CT, Schwartz CC (1999) Role of brown bears (Ursus arctos) in the flow of marine nitrogen into a terrestrial ecosystem. Oecologia 121:546–550. doi:10.1007/s004420050961

    Article  Google Scholar 

  • Hocking MD, Reimchen TE (2006) Consumption and distribution of salmon (Oncorhynchus spp.) nutrients and energy by terrestrial flies. Can J Fish Aquat Sci 63:2076–2086. doi:10.1139/F06-110

    Article  Google Scholar 

  • Hogberg P (1997) Tansley review No 95-N-15 natural abundance in soil-plant systems. New Phytol 137:179–203. doi:10.1046/j.1469-8137.1997.00808.x

    Article  Google Scholar 

  • Keller M, Reiners WA (1994) Soil atmosphere exchange of nitrous-oxide, nitric-oxide, and methane under secondary succession of pasture to forest in the Atlantic lowlands of Costa-Rica. Glob Biogeochem Cycles 8:399–409. doi:10.1029/94GB01660

    Article  CAS  Google Scholar 

  • Matson PA, Vitousek PM, Livingston GP, Swanberg NA (1990) Sources of variation in nitrous-oxide flux from Amazonian ecosystems. J Geophys Res Atmos 95:16789–16798

    Article  CAS  Google Scholar 

  • McClain ME, Boyer EW, Dent CL, Gergel SE, Grimm NB, Groffman PM, Hart SC, Harvey JW, Johnston CA, Mayorga E, McDowell WH, Pinay G (2003) Biogeochemical hot spots and hot moments at the interface of terrestrial and aquatic ecosystems. Ecosystems (NY, Print) 6:301–312. doi:10.1007/s10021-003-0161-9

    Article  CAS  Google Scholar 

  • McNaughton SJ, Ruess RW, Seagle SW (1988) Large mammals and process dynamics in African ecosystems. Bioscience 38:794–800. doi:10.2307/1310789

    Article  Google Scholar 

  • Meehan EP, Seminet-Reneau EE, Quinn TP (2005) Bear predation on Pacific salmon facilitates colonization of carcasses by fly maggots. Am Midl Nat 153:142–151. doi:10.1674/0003-0031(2005)153[0142:BPOPSF]2.0.CO;2

    Article  Google Scholar 

  • Merz JE, Moyle PB (2006) Salmon, wildlife, and wine: marine-derived nutrients in human-dominated ecosystems of central California. Ecol Appl 16:999–1009. doi:10.1890/1051-0761(2006)016[0999:SWAWMN]2.0.CO;2

    Article  PubMed  Google Scholar 

  • Moore JW, Schindler DE (2004) Nutrient export from freshwater ecosystems by anadromous sockeye salmon (Oncorhynchus nerka). Can J Fish Aquat Sci 61:1582–1589. doi:10.1139/f04-103

    Article  Google Scholar 

  • 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 88:1278–1291. doi:10.1890/06-0782

    Article  PubMed  Google Scholar 

  • Morris AEL, Stark JM, Gilbert BK (2005) Evaluation of isotopic fractionation error on calculations of marine-derived nitrogen in terrestrial ecosystems. Can J For Res Rev Can Rech For 35:1604–1616. doi:10.1139/x05-094

    Article  CAS  Google Scholar 

  • Naiman RJ, Bilby RE, Schindler DE, Helfield JM (2002) Pacific salmon, nutrients, and the dynamics of freshwater and riparian ecosystems. Ecosystems (NY, Print) 5:399–417. doi:10.1007/s10021-001-0083-3

    Article  Google Scholar 

  • O’Keefe T, Edwards R (2002) Evidence for hyporheic transfer and removal of marine-derived nutrients in a sockeye stream in southwest Alaska. Am Fish Soc Symp 33:99–107

    Google Scholar 

  • Pastor J, Dewey B, Naiman RJ, McInnes PF, Cohen Y (1993) Moose browsing and soil fertility in the boreal forests of Isle-Royale National Park. Ecology 74:467–480. doi:10.2307/1939308

    Article  Google Scholar 

  • Polis GA, Anderson WB, Holt RD (1997) Toward an integration of landscape and food web ecology: the dynamics of spatially subsidized food webs. Annu Rev Ecol Syst 28:289–316. doi:10.1146/annurev.ecolsys.28.1.289

    Article  Google Scholar 

  • Schindler DE, Scheuerell MD, Moore JW, Gende SM, Francis TB, Palen WJ (2003) Pacific salmon and the ecology of coastal ecosystems. Front Ecol Environ 1:31–37

    Article  Google Scholar 

  • 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 86:3225–3231. doi:10.1890/04-1730

    Article  Google Scholar 

  • Shadish WR, Haddock CK (1994) Combining estimates of effect size. In: Cooper H, Hedges LV (eds) The handbook of research synthesis. Russell Sage Foundation, New York, pp 261–298

    Google Scholar 

  • Stehfest E, Bouwman L (2006) N2O and NO emission from agricultural fields and soils under natural vegetation: Summarizing available measurement data and modeling of global annual emissions. Nutr Cycl Agroecosyst 74:207–228. doi:10.1007/s10705-006-9000-7

    Article  CAS  Google Scholar 

  • Tardiff SE, Stanford JA (1998) Grizzly bear digging: effects on subalpine meadow plants in relation to mineral nitrogen availability. Ecology 79:2219–2228

    Google Scholar 

  • Winder M, Schindler DE, Moore JW, Johnson SP, Palen WJ (2005) Do bears facilitate transfer of salmon resources to aquatic macroinvertebrates? Can J Fish Aquat Sci 62:2285–2293. doi:10.1139/f05-136

    Article  Google Scholar 

Download references

Acknowledgments

We thank P. Matson, J. Richey, and C. Boatright for providing substantial logistical assistance. M. Baker, T. Francis, S. Johnson, J. Moore, W. Palen, L. Rogers, and M. Winder helped with field collections. S. Alin, M. Baker, T. Francis and two anonymous reviewers provided helpful comments. This is a contribution of the University of Washington Alaska Salmon Program. The Gordon and Betty Moore Foundation, Alaska salmon processors, and National Science Foundation (Biological Oceanography, Biocomplexity) provided financial support. G. Holtgrieve was generously supported by the ARCS foundation and U.S. Environmental Protection Agency’s Science to Achieve Results (STAR) program.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Gordon W. Holtgrieve.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 56 kb)

About this article

Cite this article

Holtgrieve, G.W., Schindler, D.E. & Jewett, P.K. Large predators and biogeochemical hotspots: brown bear (Ursus arctos) predation on salmon alters nitrogen cycling in riparian soils. Ecol Res 24, 1125–1135 (2009). https://doi.org/10.1007/s11284-009-0591-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11284-009-0591-8

Keywords

Navigation