Skip to main content
Log in

Reverberating effects of resource exchanges in stream–riparian food webs

  • Community ecology – original research
  • Published:
Oecologia Aims and scope Submit manuscript

Abstract

Fluxes of materials or organisms across ecological boundaries, often termed “resource subsidies,” directly affect recipient food webs. Few studies have addressed how such direct responses in one ecosystem may, in turn, influence the fluxes of materials or organisms to other habitats or the potential for feedback relationships to occur among ecosystems. As part of a large-scale, multi-year experiment, we evaluated the hypothesis that the input of a marine-derived subsidy results in a complex array of resource exchanges (i.e., inputs, outputs, feedbacks) between stream and riparian ecosystems as responses disperse across ecological boundaries. Moreover, we evaluated how the physical properties of resource subsidies mediated complex responses by contrasting carcasses with a pelletized salmon treatment. We found that salmon carcasses altered stream–riparian food webs by directly subsidizing multiple aquatic and terrestrial organisms (e.g., benthic insect larvae, fishes, and terrestrial flies). Such responses further influenced food webs along indirect pathways, some of which spanned land and water (e.g., subsidized fishes reduced aquatic insect emergence, with consequences for spiders and bats). Subsidy-mediated feedbacks manifested when carcasses were removed to riparian habitats where they were colonized by carrion flies, some of which fell into the stream and acted as another prey subsidy for fishes. As the effects of salmon subsidies propagated through the stream–riparian food web, the sign of consumer responses was not always positive and appeared to be determined by the outcome of trophic interactions, such that localized trophic interactions within one ecosystem mediated the export of organisms to others.

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.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Allen DC, Wesner JS (2016) Synthesis: comparing effects of resource and consumer fluxes into recipient food webs using meta-analysis. Ecology 97:594–604

    PubMed  Google Scholar 

  • Bartels P, Cucherousset J, Steger K, Eklöv P, Tranvik LJ, Hillebrand H (2012) Reciprocal subsidies between freshwater and terrestrial ecosystems structure consumer resource dynamics. Ecology 93:1173–1182

    PubMed  Google Scholar 

  • Barton PS, Cunningham SA, Lindenmayer DB, Manning AD (2013) The role of carrion in maintaining biodiversity and ecological processes in terrestrial ecosystems. Oecologia 171:761–772

    PubMed  Google Scholar 

  • Baxter CV, Fausch KD, Murakami M, Chapman PL (2004) Fish invasion restructures stream and forest food webs by interrupting reciprocal prey subsidies. Ecology 85:2656–2663

    Google Scholar 

  • Baxter CV, Fausch KD, Saunders WC (2005) Tangled webs: reciprocal flows of invertebrate prey link streams and riparian zones. Freshw Biol 50:201–220

    Google Scholar 

  • Benke AC, Wallace JB (1980) Trophic basis of production among net-spinning caddisflies in a southern Appalachian stream. Ecology 61:108–118

    Google Scholar 

  • Benke AC, Huryn AD, Smock LA, Wallace JB (1999) Length-mass relationships for freshwater macroinvertebrates in North America with particular reference to the southeastern United States. J N Am Benthol Soc 18:308–343

    Google Scholar 

  • Cole JJ, Carpenter SR, Pace ML, Van de Bogert MC, Kitchell JL, Hodgson JR (2006) Differential support of lake food webs by three types of terrestrial organic carbon. Ecol Lett 9:558–568

    PubMed  Google Scholar 

  • Collins SF, Baxter CV (2014) Heterogeneity of riparian habitats mediates responses of terrestrial arthropods to a subsidy of Pacific salmon carcasses. Ecosphere 5:Art146

    Google Scholar 

  • Collins SF, Wahl DH (2017) Invasive planktivores as mediators of organic matter exchanges within and across ecosystems. Oecologia 184:521–530

    PubMed  Google Scholar 

  • 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 30:831–839

    Google Scholar 

  • Collins SF, Marcarelli AM, Baxter CV, Wipfli MS (2015) A critical assessment of the ecological assumptions underpinning compensatory mitigation of salmon-derived nutrients. Environ Manag 56:571–586

    Google Scholar 

  • Collins SF, Baxter CV, Marcarelli AM, Wipfli MS (2016) Effects of experimentally added salmon subsidies on resident fishes via direct and indirect pathways. Ecosphere 7(3):e01248

    Google Scholar 

  • Cummins KW (1974) Structure and function of stream ecosystems. Bioscience 24:631–641

    Google Scholar 

  • Elliott J (1976) Body composition of brown trout (Salmo trutta L.) in relation to temperature and ration size. J Anim Ecol 45:273–289

    Google Scholar 

  • Fisher SG, Likens GE (1972) Stream ecosystem: organic energy budget. Bioscience 22:33–35

    Google Scholar 

  • Gende SM, Edwards RT, Willson MF, Wipfli MS (2002) Pacific salmon in aquatic and terrestrial ecosystems. Bioscience 52:917–928

    Google Scholar 

  • Gounand I, Harvey E, Little CJ, Altermatt F (2018) Meta-ecosystems 2.0: rooting the theory into the field. Trends Ecol Evol 33:36–46

    PubMed  Google Scholar 

  • Henschel JR, Mahsberg D, Stumpf H (2001) Allochthonous aquatic insects increase predation and decrease herbivory in river shore food webs. Oikos 93:429–438

    Google Scholar 

  • Hoekman D, Dreyer J, Jackson RD, Townsend PA, Gratton C (2011) Lake to land subsidies: experimental addition of aquatic insects increases terrestrial arthropod densities. Ecology 92:2063–2072

    PubMed  Google Scholar 

  • Holt RD (1977) Predation, apparent competition, and the structure of prey communities. Theor Popul Biol 12:197–229

    CAS  PubMed  Google Scholar 

  • Holt RD (2002) Food webs in space: on the interplay of dynamic instability and spatial processes. Ecol Res 17:261–273

    Google Scholar 

  • Holt RD (2004) Implications of system openness for local community structure and ecosystem function. In: Polis GA, Power ME, Huxel GR (eds) Food webs at the landscape level. University of Chicago Press, Chicago, pp 96–114

    Google Scholar 

  • Hynes HBN (1975) The stream and its valley. Verh Internat Verein Theor Angew Limnol 19:1–15

    Google Scholar 

  • Idaho Department of Fish and Game (IDFG) (1985) Idaho anadromous fisheries management plan 1985–1990. Boise, Idaho, USA

  • Iwata T (2007) Linking stream habitats and spider distribution: spatial variations in trophic transfer across a forest–stream boundary. Ecol Res 22:619–628

    Google Scholar 

  • Janetski DJ, Chaloner DT, Tiegs SD, Lamberti GA (2009) Pacific salmon effects on stream ecosystems: a quantitative synthesis. Oecologia 159:583–595

    PubMed  Google Scholar 

  • Knight TM, McCoy MW, Chase JM, McCoy KA, Holt RD (2005) Trophic cascades across ecosystems. Nature 437:880–883

    CAS  PubMed  Google Scholar 

  • Kraus JM, Vonesh JR (2012) Fluxes of terrestrial and aquatic carbon by emergent mosquitoes: a test of controls and implications for cross-ecosystem linkages. Oecologia 170:1111–1122

    PubMed  Google Scholar 

  • Leibold MA, Holyoak M, Mouquet N, Amarasekare P, Chase JM, Hoopes HR, Shurin JB, Law R, Tilman D, Loreau M, Gonzalez A (2004) The metacommunity concept: a framework for multi-scale community ecology. Ecol Lett 7:601–613

    Google Scholar 

  • Loreau M, Mouquet N, Holt RD (2003) Meta-ecosystems: a theoretical framework for a spatial ecosystem ecology. Ecol Lett 6:673–679

    Google Scholar 

  • Marcarelli AM, Baxter CV, Mineau MM, Hall RO Jr (2011) Quantity and quality: unifying food web and ecosystem perspectives on the role of resource subsidies in freshwaters. Ecology 92:1215–1225

    PubMed  Google Scholar 

  • 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(6):1–22

    Google Scholar 

  • Marczak LB, Thompson RM, Richardson JS (2007) Meta-analysis: trophic level, habitat, and productivity shape the food web effects of resource subsidies. Ecology 88:140–148

    PubMed  Google Scholar 

  • McCann K, Hastings A, Huxel GR (1998) Weak trophic interactions and the balance of nature. Nature 395:794–798

    CAS  Google Scholar 

  • Meadows DH (2008) Thinking in systems: a primer. Chelsea Green Publishing, White River Junction

    Google Scholar 

  • Murakami M, Nakano S (2002) Indirect effect of aquatic insect emergence on a terrestrial insect population through by bird predation. Ecol Lett 5:333–337

    Google Scholar 

  • Nakano S, Miyasaka H, Kuhara N (1999) Terrestrial–aquatic linkages: riparian arthropod inputs alter trophic cascades in a stream food web. Ecology 80:2435–2441

    Google Scholar 

  • Newsome TM, Dellinger JA, Pavey CR, Ripple WJ, Shores CR, Wirsing AJ, Dickman CR (2015) The ecological effects of providing resource subsidies to predators. Glob Ecol Biogeogr 24:1–11

    Google Scholar 

  • Northwest Power and Conservation Council (NWPCC) (2004) Boise, Payette, and Weiser River subbasin plans. NWPCC, Portland

    Google Scholar 

  • Ober HK, Hayes JP (2008) Influence of vegetation on bat use of riparian areas at multiple spatial scales. J Wildl Manag 72:396–404

    Google Scholar 

  • Odum HT (1983) Systems ecology: an introduction. Wiley, New York

    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. Ann Rev Ecol Evol Syst 28:289–316

    Google Scholar 

  • Quinn TP, Carlson SM, Gende SM, Rich HB Jr (2009) Transportation of Pacific salmon carcasses from streams to riparian forests by bears. Can J Zool 87:195–203

    Google Scholar 

  • Richardson JS, Zhang Y, Marczak LB (2010) Resource subsidies across the land–freshwater interface and responses in recipient communities. River Res Appl 26:55–66

    Google Scholar 

  • Rooney N, McCann KS, Moore JC (2008) A landscape theory for food web architecture. Ecol Lett 11:867–881

    PubMed  Google Scholar 

  • Sabo J, Power M (2002) River–watershed exchange: effects of riverine subsidies on riparian lizards and their terrestrial prey. Ecology 83:1860–1869

    Google Scholar 

  • Sabo JL, Bastow JL, Power ME (2002) Length–mass relationships for adult aquatic and terrestrial invertebrates in a California watershed. J N Am Benthol Soc 21:336–343

    Google Scholar 

  • Scharnweber K, Vanni MJ, Hilt S, Syväranta J, Mehner T (2014) Boomerang ecosystem fluxes: organic carbon inputs from land to lakes are returned to terrestrial food webs via aquatic insects. Oikos 123:1439–1448

    CAS  Google Scholar 

  • 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 52:1944–1956

    CAS  Google Scholar 

  • Schindler DE, Smits AP (2017) Subsidies of aquatic resources in terrestrial ecosystems. Ecosystems 20:78–93

    Google Scholar 

  • Schnitzler HU, Moss CF, Denzinger A (2003) From spatial orientation to food acquisition in echolocating bats. Trends Ecol Evol 18:386–394

    Google Scholar 

  • Spiller DA, Piovia-Scott J, Wright AN, Yang LH, Takimoto G, Schoener TW, Iwata T (2010) Marine subsidies have multiple effects on coastal food webs. Ecology 91:1424–1434

    PubMed  Google Scholar 

  • Takimoto G, Iwata T, Murakami M (2009) Timescale hierarchy determines the indirect effects of fluctuating subsidy inputs on in situ resources. Am Nat 173:200–211

    PubMed  Google Scholar 

  • 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 54:1864–1875

    CAS  Google Scholar 

  • Turner MG, Gardner RH, O’Neill RV (2001) Landscape ecology in theory and practice: patterns and processes. Springer, New York

    Google Scholar 

  • Ubick D, Dupérré N (2005) Spiders of North America: an identification manual. American Arachnological Society, Keene

    Google Scholar 

  • Wallace JB, Eggert SL, Meyer JL, Webster JR (1997) Multiple trophic levels of a forest stream linked to terrestrial litter inputs. Science 277:102–104

    CAS  Google Scholar 

  • Warren CE, Davis GE (1967) Laboratory studies on the feeding, bioenergetics and growth of fish. Special Report 230, Pacific Cooperative Water Pollution and Fisheries Research Laboratories, Oregon State University, Corvallis, Oregon

  • Wesner JS (2016) Contrasting effects of fish predation on benthic versus emerging prey: a meta-analysis. Oecologia 180:1205–1211

    PubMed  Google Scholar 

  • Williams DD, Ambrose LG, Browning LN (1995) Trophic dynamics of two sympatric species of riparian spider (Araneae: Tetragnathidae). Can J Zool 73:1545–1553

    Google Scholar 

Download references

Acknowledgements

This project was funded and supported by Bonneville Power Administration (2007-332-00), Idaho Power, and the Idaho Department of Fish and Game. CVB and AMM were partially supported by the National Science FoundationEPSCoR in Idaho (EPS-08-14387) and NSF-DEB-1754224 to CVB. Any use of trade, firm, or product names is for descriptive purposes only and does not imply endorsement by the U.S. Government. The authors have no conflicts of interest to declare.

Author information

Authors and Affiliations

Authors

Contributions

MSW, GS, CVB, AMM, LF planned and designed the experiment. SFC, AMM, and CVB collected stream food web and spider data. SF and LF collected bat data, and SFC analyzed the data. SFC wrote the first draft of the manuscript, and all authors contributed to revisions.

Corresponding author

Correspondence to Scott F. Collins.

Ethics declarations

Ethical approval

All applicable institutional and/or national guidelines for the care and use of animals were followed.

Additional information

Communicated by Robert O. Hall.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Collins, S.F., Baxter, C.V., Marcarelli, A.M. et al. Reverberating effects of resource exchanges in stream–riparian food webs. Oecologia 192, 179–189 (2020). https://doi.org/10.1007/s00442-019-04574-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00442-019-04574-y

Keywords

Navigation