, Volume 20, Issue 1, pp 78–93 | Cite as

Subsidies of Aquatic Resources in Terrestrial Ecosystems

  • Daniel E. SchindlerEmail author
  • Adrianne P. Smits
20th Anniversary Paper


Floods, spatially complex water flows, and organism movements all generate important fluxes of aquatic-derived materials into terrestrial habitats, counteracting the gravity-driven downhill transport of matter from terrestrial-to-aquatic ecosystems. The magnitude of these aquatic subsidies is often smaller than terrestrial subsidies to aquatic ecosystems but higher in nutritional quality, energy density, and nutrient concentration. The lateral extent of biological aquatic subsidies is typically small, extending only a few meters into riparian habitat; however, terrestrial consumers often aggregate on shorelines to capitalize on these high-quality resources. Although the ecological effects of aquatic subsidies remain partially understood, it is clear that ongoing human modification to aquatic ecosystems, riparian habitats and river floodplains affect the magnitude, quality, and spatial and temporal patterning of aquatic subsidies in terrestrial landscapes. These changes will alter the character of aquatic–terrestrial coupling and have consequences for terrestrial organisms that rely on these high-quality and temporally dependable resource subsidies. Homogenization of landscapes and flow regimes, eutrophication, exotic species, and contaminants all represent threats to the vital flows of aquatic-derived resources into terrestrial ecosystems. Research emphasizing that landscapes are integrated terrestrial–aquatic systems, characterized by both biological and hydrological flows among habitats, is needed for understanding the consequences of aquatic subsidies and managing ecological risks of ongoing human development.


heterogeneity complexity habitat coupling global change homogenization food webs 



We wish to acknowledge the National Science Foundation, the Western Alaska Landscape Conservation Cooperative, and the Harriet Bullitt Chair in Conservation for support. APS was supported by an NSF GRFP fellowship.


  1. Aalto R, Maurice-Bourgoin L, Dunne T, Montgomery DR, Nittrouer CA, Guyot JL. 2003. Episodic sediment accumulation on Amazonian flood plains influenced by El Nino/Southern Oscillation. Nature 425:493–7.CrossRefPubMedGoogle Scholar
  2. Armstrong JB, Schindler DE. 2013. Going with the flow: spatial distributions of juvenile coho salmon track an annually shifting mosaic of water temperature. Ecosystems 16:1429–41.CrossRefGoogle Scholar
  3. Armstrong JB, Takimoto GT, Schindler DE, Hayes MM, Kaufman MJ. 2016. Resource waves: phenological diversity enhances foraging opportunities for mobile consumers. Ecology 97:1099–112.CrossRefPubMedGoogle Scholar
  4. Bartels P, Cucherousset J, Steger K, Eklov P, Tranvik LJ, Hillebrand H. 2012. Reciprocal subsidies between freshwater and terrestrial ecosystems structure consumer resource dynamics. Ecology 93:1173–82.CrossRefPubMedGoogle Scholar
  5. Bartrons M, Gratton C, Spiesman BJ, Jake AM, Vander Zanden MJ. 2015. Taking the trophic bypass: aquatic–terrestrial linkage reduces methylmercury in a terrestrial food web. Ecol Appl 25:151–9.CrossRefPubMedGoogle Scholar
  6. Bartrons M, Papeş M, Diebel MW, Gratton C, Vander Zanden MJ. 2013. Regional-level inputs of emergent aquatic insects from water to land. Ecosystems 16:1353–63.CrossRefGoogle Scholar
  7. Bastow JL, Sabo JL, Finlay JC, Power ME. 2002. A basal aquatic–terrestrial trophic link in rivers: algal subsidies via shore-dwelling grasshoppers. Oecologia 131:261–8.CrossRefGoogle Scholar
  8. Baxter CV, Fausch KD, Murakami M, Chapman PL. 2004. Nonnative stream fish invasion restructures stream and forest food webs by interrupting reciprocal prey subsidies. Ecology 85:2656–63.CrossRefGoogle Scholar
  9. Baxter CV, Fausch KD, Saunders WC. 2005. Tangled webs: reciprocal flows of invertebrate prey link streams and riparian zones. Freshw Biol 50:201–20.CrossRefGoogle Scholar
  10. Bayley PB. 1995. Understanding large river-floodplain ecosystems. BioScience 45:153–8.CrossRefGoogle Scholar
  11. Beechie TJ, Pollock MM, Baker S. 2008. Channel incision, evolution and potential recovery in the Walla Walla and Tucannon River basins, northwestern USA. Earth Surf Process Landf 33:784–800.CrossRefGoogle Scholar
  12. Beechie TJ, Sear DA, Olden JD, Pess GR, Buffington JM, Moir H, Roni P, Pollock MM. 2010. Process-based principles for restoring river ecosystems. BioScience 60:209–22.CrossRefGoogle Scholar
  13. Bunn SE, Balcombe SR, Davies PM, Fellows CS, McKenzie-Smith FJ. 2006. Aquatic productivity and food webs of desert river ecosystems. In: Kingsford RT, Ed. Ecology of Desert Rivers. Cambridge: Cambridge University Press. p 76–99.Google Scholar
  14. Carpenter SR, Caraco NF, Correll DL, Howarth RW, Sharpley AN, Smith VH. 1998. Nonpoint pollution of surface waters with phosphorus and nitrogen. Ecol Appl 8:559–68.CrossRefGoogle Scholar
  15. Christensen JR, MacDuffee M, MacDonald RW, Whiticar M, Ross PS. 2005. Persistent organic pollutants in British Columbia grizzly bears: consequences of divergent diets. Environ Sci Technol 39:6952–60.CrossRefPubMedGoogle Scholar
  16. Cristol DA, Brasso RL, Condon AM, Fovargue RE, Friedman SL, Hallinger KK, Monroe AP, White AE. 2008. The movement of aquatic mercury through terrestrial food webs. Science 320:335.CrossRefPubMedGoogle Scholar
  17. Darimont CT, Bryan HM, Carlson SM, Hocking MD, MacDuffee M, Paquet PC, Price MHH, Reimchen TE, Reynolds JD, Wilmers CC. 2010. Salmon for terrestrial protected areas. Conserv Lett 3:379–89.CrossRefGoogle Scholar
  18. Davis JM, Rosemond AD, Small GE. 2011. Increasing donor ecosystem productivity decreases terrestrial consumer reliance on a stream resource subsidy. Oecologia 167:821–34.CrossRefPubMedGoogle Scholar
  19. Dorfman EJ, Kingsford RT. 2001. Scale-dependent patterns of abundance and habitat use by cormorants in Australia and the importance of nomadism. J Arid Environ 49:677–94.CrossRefGoogle Scholar
  20. Downs SG, MacLeod CL, Lester JN. 1998. Mercury in precipitation and its relation to bioaccumulation in fish: a literature review. Water Air Soil Pollut 108:149–87.CrossRefGoogle Scholar
  21. Dreyer J, Townsend PA, Hook JC, Hoekman D, Vander Zanden MJ, Gratton C. 2015. Quantifying aquatic insect deposition from lake to land. Ecology 96:499–509.CrossRefPubMedGoogle Scholar
  22. Epanchin PN, Knapp RA, Lawler SP. 2010. Nonnative trout impact an alpine-nesting bird by altering aquatic-insect subsidies. Ecology 91:2406–15.CrossRefPubMedGoogle Scholar
  23. Finlay JC, Vredenburg VT. 2007. Introduced trout sever trophic connections in watersheds: consequences for a declining amphibians. Ecology 88:2187–98.CrossRefPubMedGoogle Scholar
  24. Francis TB, Schindler DE, Fox JM, Seminet-Reneau E. 2007. Effects of urbanization on the dynamics of organic sediments in temperate lakes. Ecosystems 10:1057–68.CrossRefGoogle Scholar
  25. 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.CrossRefGoogle Scholar
  26. Gende SM, Edwards RT, Willson MF, Wipfli MS. 2002. Pacific salmon in aquatic and terrestrial ecosystems. BioScience 52:917–28.CrossRefGoogle Scholar
  27. Gladyshev MI, Arts MT, Sushchik NI. 2009. Preliminary estimates of the export of omega-3 highly unsaturated fatty acids (EPA+ DHA) from aquatic to terrestrial ecosystems. In: Arts MT, Brett MT, Kainz M, Eds. Lipids in aquatic ecosystems. NewYork: Springer. p 179–210.CrossRefGoogle Scholar
  28. Gratton C, Vander Zanden MJ. 2009. Flux of aquatic insect productivity to land: comparison of lentic and lotic ecosystems. Ecology 90:2689–99.CrossRefPubMedGoogle Scholar
  29. Gurnell AM, Bertoldi W, Tockner K, Wharton G, Zolezzi G. 2016. How large is a river? Conceptualizing river landscape signatures and envelopes in four dimensions. WIREs Water 3:313–25.CrossRefGoogle Scholar
  30. Hagen EM, Sabo JL. 2014. Temporal variability in insectivorous bat activity along two desert streams with contrasting patterns of prey availability. J Arid Environ 102:104–12.CrossRefGoogle Scholar
  31. Heffernan JB, Soranno PA, Angilletta MJ, Buckley LB, Gruner DS, Keitt TH, Kellner JR, Kominosky JS, Rocha AV, Xiao J et al. 2014. Macrosystems ecology: understanding ecological patterns and processes at continental scales. Front Ecol Environ 12:5–14.CrossRefGoogle Scholar
  32. Helfield JM, Naiman RJ. 2001. Effects of salmon-derived nitrogen on riparian forest growth and implications for stream productivity. Ecology 82:2403–9.CrossRefGoogle Scholar
  33. Helfield JM, Naiman RJ. 2006. Keystone interactions: salmon and bear in riparian forests of Alaska. Ecosystems 9:167–80.CrossRefGoogle Scholar
  34. Hocking MD, Reimchen TE. 2006. Consumption and distribution of salmon (Oncorhynchus spp.) nutrients and energy by terrestrial flies. Can J Fish Aquat Sci 63:2076–86.CrossRefGoogle Scholar
  35. Hocking MD, Reynolds JD. 2011. Impacts of salmon on riparian plant diversity. Science 331:1609–12.CrossRefPubMedGoogle Scholar
  36. Holtgrieve GW, Schindler DE, Jewett PK. 2009. Large predators and biogeochemical hotspots: brown bear (Ursus arctos) predation on salmon alters nitrogen cycling in riparian soils. Ecol Res 24:1125–35.CrossRefGoogle Scholar
  37. Jacobson PJ, Jacobson KM, Angermeier PL, Cherry DS. 2000. Hydrologic influences on soil properties along ephemeral rivers in the Namib Desert. J Arid Environ 45:21–34.CrossRefGoogle Scholar
  38. Johnson SP, Schindler DE. 2009. Trophic ecology of Pacific salmon (Oncorhynchus spp.) in the ocean: a synthesis of stable isotope research. Ecol Res 24:855–63.CrossRefGoogle Scholar
  39. Junk WJ, Bayley PB, Sparks RE. 1989. The flood pulse concept in river-floodplain systems. In: Dodge DP, Ed. Proceedings of the International Large River Symposium. Canadian Special Publication of Fisheries and Aquatic Sciences 106.Google Scholar
  40. Kraus JM, Schmidt TS, Walters DM, Wanty RB, Zuellig RE, Wolf RE. 2014. Cross-ecosystem impacts of stream pollution reduce resource and contaminant flux to riparian food webs. Ecol Appl 24:235–43.CrossRefPubMedGoogle Scholar
  41. Larsen S, Muehlbauer JD, Marti E. 2016. Resource subsidies between stream and terrestrial ecosystems under global change. Global Change Biol 22:2489–504.CrossRefGoogle Scholar
  42. Lau DCP, Leung KMY, Dudgeon D. 2008. Experimental dietary manipulations for determining the relative importance of allochthonous and autochthonous food resources in tropical streams. Freshw Biol 53:139–47.Google Scholar
  43. Likens GE. 1992. The ecosystem approach: its use and abuse. Oldendorf/Luhe, Germany: Ecology Institute.Google Scholar
  44. Lisi PJ, Schindler DE. 2011. Spatial variation in timing of marine subsidies influences riparian phenology through a plant-pollinator mutualism. Ecosphere 2:1–15. doi: 10.1890/ES11-00173.1.CrossRefGoogle Scholar
  45. Lisi PJ, Schindler DE, Bentley KT, Pess GR. 2013. Association between geomorphic attributes of watersheds, water temperature, and salmon spawn timing in Alaskan streams. Geomorphology 185:78–86.CrossRefGoogle Scholar
  46. Lisi PJ, Schindler DE, Cline TJ, Scheuerell MD, Walsh PB. 2015. Watershed geomorphology and snowmelt control stream thermal sensitivity to air temperature. Geophys Res Lett 42:3380–8.CrossRefGoogle Scholar
  47. Luck M, Maumenee N, Whited D, Lucotch J, Chilcote S, Lorang M, Goodman D, McDonald K, Kimball J, Stanford J. 2010. Remote sensing analysis of physical complexity of North Pacific Rim rivers to assist wild salmon conservation. Earth Surf Process Landf 35:1330–43.CrossRefGoogle Scholar
  48. Lim SY, Hoshiba J, Moriguchi T, Salem N Jr. 2005. N-3 fatty acid deficiency induced by a modified artificial rearing method leads to poorer performance in spatial learning tasks. Pediat Res 58:741–8.CrossRefPubMedGoogle Scholar
  49. Lindeman RL. 1942. The trophic-dynamic aspect of ecology. Ecology 23:399–418.CrossRefGoogle Scholar
  50. Lytle DA, Poff NL. 2004. Adaptation to natural flow regimes. Trends Ecol Evol 19:94–100.CrossRefPubMedGoogle Scholar
  51. Marcarelli AM, Baxter CV, Mineau MM, Hall RO. 2011. Quantity and quality: unifying food web and ecosystem perspectives on the role of resource subsidies in freshwaters. Ecology 92:1215–25.CrossRefPubMedGoogle Scholar
  52. Matthews KR, Knapp RA, Pope KL. 2002. Garter snake distributions in high-elevation aquatic ecosystems: is there a link with declining amphibian populations and nonnative trout introductions? J Herpetol 36:16–22.CrossRefGoogle Scholar
  53. Moore JW, Schindler DE. 2010. Spawning salmon and the phenology of emergence in stream insects. Proc R Soc B 277:1695–703.CrossRefPubMedPubMedCentralGoogle Scholar
  54. Morris MR, Stanford JA. 2011. Floodplain succession and soil nitrogen accumulation on a salmon river in southwestern Kamchatka. Ecol Monogr 81:43–61.CrossRefGoogle Scholar
  55. Muehlbauer JD, Collins SF, Doyle MW, Tockner K. 2014. How wide is a stream? Spatial extent of the potential “stream signature” in terrestrial food webs using meta-analysis. Ecology 95:44–55.CrossRefPubMedGoogle Scholar
  56. Nakano S, Murakami M. 2001. Reciprocal subsidies: Dynamic interdependence between terrestrial and aquatic food webs. Proc Natl Acad Sci USA 98:166–70.CrossRefPubMedPubMedCentralGoogle Scholar
  57. Naiman RJ, Bilby RE, Schindler DE, Helfield JM. 2002. Pacific salmon, nutrients, and the dynamics of freshwater and riparian ecosystems. Ecosystems 5:399–417.CrossRefGoogle Scholar
  58. Noe GB, Hupp CR. 2005. Carbon, nitrogen, and phosphorus accumulation in floodplains of Atlantic Coastal Plain rivers, USA. Ecol Appl 15:1178–90.CrossRefGoogle Scholar
  59. Pace ML, Cole JJ, Carpenter SR, Kitchell JF, Holdgson JR, Van de Bogert MC, Bade DL, Kritzberg ES, Bastviken D. 2004. Whole-lake carbon-13 additions reveal terrestrial support of aquatic food webs. Nature 427:240–3.CrossRefPubMedGoogle Scholar
  60. Palmer MA, Bernhardt ES, Allan JD, Lake PS, Alexander G, Brooks S, Carr J, Clayton S, Dahm CN, Follstad Shah J, Galat DL, Loss SG, Goodwin P, Hart DD, Hassett B, Jenkinson R, Kondolf GM, Lave R, Meyer JL, O’Donnell TK, Pagano L, Sudduth E. 2005. Standards for ecologically successful river restoration. J Appl Ecol 42:208–17.CrossRefGoogle Scholar
  61. Paetzold A, Schubert CJ, Tockner K. 2005. Aquatic terrestrial linkages along a braided-river: riparian arthropods feeding on aquatic insects. Ecosystems 8:748–59.CrossRefGoogle Scholar
  62. Pawlosky RJ, Denkins Y, Ward G, Salem N Jr. 1997. Retinal and brain accretion of long-chain polyunsaturated fatty acids in developing felines: the effects of corn oil-based maternal diets. Am J Clin Nutri 65:465–72.Google Scholar
  63. Peipoch M, Brauns M, Hauer FR, Weitere M, Valett HM. 2015. Ecological simplification: human influences on riverscape complexity. BioScience 65:1057–65.CrossRefGoogle Scholar
  64. Pinay G, Black VJ, Planty-Tabacchi AM, Gumiero B, Décamps H. 2000. Geomorphic control of denitrification in large river floodplain soils. Biogeochemistry 50:163–82.CrossRefGoogle Scholar
  65. Pinay G, Clément JC, Naiman RJ. 2002. Basic principles and ecological consequences of changing water regimes on nitrogen cycling in fluvial systems. Environ Manag 30:481–91.CrossRefGoogle Scholar
  66. Pinay G, O’Keefe TC, Edwards RT, Naiman RJ. 2009. Nitrate removal in the hyporheic zone of a salmon river in Alaska. River Res Appl 25:367–75.CrossRefGoogle Scholar
  67. Poff NL, Allan JD, Bain MB, Karr JR, Prestegaard KL, Richter BD, Sparks RE, Stromberg JC. 1997. The natural flow regime. BioScience 47:769–84.CrossRefGoogle Scholar
  68. 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 Syst 28:289–316.CrossRefGoogle Scholar
  69. Polis GA, Power M, Huxel GR, Eds. 2004. Food webs at the landscape level. Chicago: University of Chicago Press.Google Scholar
  70. Power ME, Rainey WE. 2000. Food webs and resource sheds: Towards spatially delimiting trophic interactions. In: Hutchings MJ, John EA, Stewart AJA, Eds. Ecological consequences of habitat heterogeneity. Oxford: Blackwell Scientific. p 291–314.Google Scholar
  71. Power ME, Rainey WE, Parker , Sabo JL, Smyth A, Smyth A, Khandwala S, Finlay JC, McNeely FC, Marsee K, Anderson C. 2004. River-to-watershed subsidies in an old-growth conifer forest. In: Polis GA, Power ME, Huxel GR, Eds. Food webs at the landscape scale. Chicago: University of Chicago Press. p 217–40.Google Scholar
  72. Reimchen TE. 2000. Some ecological and evolutionary aspects of bear-salmon interactions in coastal British Columbia. Can J Zool 78:448–57.CrossRefGoogle Scholar
  73. 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.CrossRefGoogle Scholar
  74. Roshier DA, Robertson AI, Kingsford RT. 2002. Responses of waterbirds to flooding in an arid region of Australia and implications for conservation. Biol Conserv 106:399–411.CrossRefGoogle Scholar
  75. Schindler DE, Scheuerell MD, Moore JW, Gende SM, Francis TB, Palen WJ. 2003. Pacific salmon and the ecology of coastal ecosystems. Front Ecol Environ 1:31–7.CrossRefGoogle Scholar
  76. Schindler DE, Armstrong JB, Bentley KT, Jankowski K, Lisi PJ, Payne LX. 2013. Riding the crimson tide: mobile consumers track phenological variation in spawning of an anadromous fish. Biol Lett 9:20130048.CrossRefPubMedPubMedCentralGoogle Scholar
  77. Schulz R, Bundschuh M, Gergs R, Brühl CA, Diehl D, Entling MH, Fahse L, Frör O, Jungkunst HF, Lorke A, Schäfer RB, Schaumann GE, Schwenk K. 2015. Review on environmental alterations propagating from aquatic to terrestrial ecosystems. Sci Tot Environ 15:246–61.CrossRefGoogle Scholar
  78. Shurin JB, Gruner DS, Hillebrand H. 2006. All wet or dried up? Real differences between aquatic and terrestrial food webs. Proc R Soc B 273:1–9.CrossRefPubMedGoogle Scholar
  79. Spink A, Sparks RE, Van Oorchot M, Verhoeven JTA. 1998. Nutrient dynamics of large river floodplains. Regul Rivers 14:203–16.CrossRefGoogle Scholar
  80. Stanford JA, Ward JV. 1993. An ecosystem perspective of alluvial rivers: connectivity and the hyporheic corridor. J N Am Benthol Soc 12:48–60.CrossRefGoogle Scholar
  81. St. Louis VL, Barlow JC. 1993. The reproductive success of tree swallows nesting near experimentally acidified lakes in northwest Ontario. Can J Zool 71:1090–7.CrossRefGoogle Scholar
  82. Torres-Ruiz M, Wehr JD, Perrone AA. 2007. Trophic relations in a stream food web: importance of fatty acids for macroinvertebrate consumers. J N Am Benthol Soc 26:509–22.CrossRefGoogle Scholar
  83. Valett HM, Baker MA, Morrice JA, Crawford CS, Molles MC, Dahm CN, Moyer DL, Thibault JR, Ellis LM. 2005. Biogeochemical and metabolic responses to the flood pulse in a semiarid floodplain. Ecology 86:220–34.CrossRefGoogle Scholar
  84. Walters DM, Fritz KM, Otter RR. 2008. The dark side of subsidies: adult stream insects export organic contaminants to riparian predators. Ecol Appl 18:1835–41.CrossRefPubMedGoogle Scholar
  85. Willson MF, Gende SM, Bisson PA. 2004. Anadromous fishes as ecological links between ocean fresh water, and land. In: Polis GA, Power M, Huxel GR, Eds. Food webs at the landscape scale. Chicago: University of Chicago Press. p 284–300.Google Scholar
  86. Zarfl C, Lumsdon AE, Berlekamp J, Tydecks L, Tockner K. 2015. A global boom in hydropower dam construction. Aquat Sci 77:161–70.CrossRefGoogle Scholar
  87. Zarnetske JP, Haggerty R, Wondzell SM, Baker MA. 2011. Labile dissolved organic carbon supply limits hyporheic denitrification. J Geophys Res Biogeosci 116:G01025. doi: 10.1029/2010JG001356.Google Scholar

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© Springer Science+Business Media New York 2016

Authors and Affiliations

  1. 1.School of Aquatic and Fishery SciencesUniversity of WashingtonSeattleUSA

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