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.
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
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
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
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
Baxter CV, Fausch KD, Saunders WC (2005) Tangled webs: reciprocal flows of invertebrate prey link streams and riparian zones. Freshw Biol 50:201–220
Benke AC, Wallace JB (1980) Trophic basis of production among net-spinning caddisflies in a southern Appalachian stream. Ecology 61:108–118
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
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
Collins SF, Baxter CV (2014) Heterogeneity of riparian habitats mediates responses of terrestrial arthropods to a subsidy of Pacific salmon carcasses. Ecosphere 5:Art146
Collins SF, Wahl DH (2017) Invasive planktivores as mediators of organic matter exchanges within and across ecosystems. Oecologia 184:521–530
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
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
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
Cummins KW (1974) Structure and function of stream ecosystems. Bioscience 24:631–641
Elliott J (1976) Body composition of brown trout (Salmo trutta L.) in relation to temperature and ration size. J Anim Ecol 45:273–289
Fisher SG, Likens GE (1972) Stream ecosystem: organic energy budget. Bioscience 22:33–35
Gende SM, Edwards RT, Willson MF, Wipfli MS (2002) Pacific salmon in aquatic and terrestrial ecosystems. Bioscience 52:917–928
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
Henschel JR, Mahsberg D, Stumpf H (2001) Allochthonous aquatic insects increase predation and decrease herbivory in river shore food webs. Oikos 93:429–438
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
Holt RD (1977) Predation, apparent competition, and the structure of prey communities. Theor Popul Biol 12:197–229
Holt RD (2002) Food webs in space: on the interplay of dynamic instability and spatial processes. Ecol Res 17:261–273
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
Hynes HBN (1975) The stream and its valley. Verh Internat Verein Theor Angew Limnol 19:1–15
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
Janetski DJ, Chaloner DT, Tiegs SD, Lamberti GA (2009) Pacific salmon effects on stream ecosystems: a quantitative synthesis. Oecologia 159:583–595
Knight TM, McCoy MW, Chase JM, McCoy KA, Holt RD (2005) Trophic cascades across ecosystems. Nature 437:880–883
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
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
Loreau M, Mouquet N, Holt RD (2003) Meta-ecosystems: a theoretical framework for a spatial ecosystem ecology. Ecol Lett 6:673–679
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
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
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
McCann K, Hastings A, Huxel GR (1998) Weak trophic interactions and the balance of nature. Nature 395:794–798
Meadows DH (2008) Thinking in systems: a primer. Chelsea Green Publishing, White River Junction
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
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
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
Northwest Power and Conservation Council (NWPCC) (2004) Boise, Payette, and Weiser River subbasin plans. NWPCC, Portland
Ober HK, Hayes JP (2008) Influence of vegetation on bat use of riparian areas at multiple spatial scales. J Wildl Manag 72:396–404
Odum HT (1983) Systems ecology: an introduction. Wiley, New York
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
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
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
Rooney N, McCann KS, Moore JC (2008) A landscape theory for food web architecture. Ecol Lett 11:867–881
Sabo J, Power M (2002) River–watershed exchange: effects of riverine subsidies on riparian lizards and their terrestrial prey. Ecology 83:1860–1869
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
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
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
Schindler DE, Smits AP (2017) Subsidies of aquatic resources in terrestrial ecosystems. Ecosystems 20:78–93
Schnitzler HU, Moss CF, Denzinger A (2003) From spatial orientation to food acquisition in echolocating bats. Trends Ecol Evol 18:386–394
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
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
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
Turner MG, Gardner RH, O’Neill RV (2001) Landscape ecology in theory and practice: patterns and processes. Springer, New York
Ubick D, Dupérré N (2005) Spiders of North America: an identification manual. American Arachnological Society, Keene
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
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
Williams DD, Ambrose LG, Browning LN (1995) Trophic dynamics of two sympatric species of riparian spider (Araneae: Tetragnathidae). Can J Zool 73:1545–1553
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 Foundation–EPSCoR 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
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
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
About this article
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
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00442-019-04574-y