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Terrestrial subsidies to lake food webs: an experimental approach

  • Ecosystem ecology - Original Paper
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Abstract

Cross-ecosystem movements of material and energy are ubiquitous. Aquatic ecosystems typically receive material that also includes organic matter from the surrounding catchment. Terrestrial-derived (allochthonous) organic matter can enter aquatic ecosystems in dissolved or particulate form. Several studies have highlighted the importance of dissolved organic carbon to aquatic consumers, but less is known about allochthonous particulate organic carbon (POC). Similarly, most studies showing the effects of allochthonous organic carbon (OC) on aquatic consumers have investigated pelagic habitats; the effects of allochthonous OC on benthic communities are less well studied. Allochthonous inputs might further decrease primary production through light reduction, thereby potentially affecting autotrophic resource availability to consumers. Here, an enclosure experiment was carried out to test the importance of POC input and light availability on the resource use in a benthic food web of a clear-water lake. Corn starch (a C4 plant) was used as a POC source due to its insoluble nature and its distinct carbon stable isotope value (δ13C). The starch carbon was closely dispersed over the bottom of the enclosures to study the fate of a POC source exclusively available to sediment biota. The addition of starch carbon resulted in a clear shift in the isotopic signature of surface-dwelling herbivorous and predatory invertebrates. Although the starch carbon was added solely to the sediment surface, the carbon originating from the starch reached zooplankton. We suggest that allochthonous POC can subsidize benthic food webs directly and can be further transferred to pelagic systems, thereby highlighting the importance of benthic pathways for pelagic habitats.

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References

  • Ask J, Karlsson J, Persson L, Ask P, Bystrom P, Jansson M (2009a) Terrestrial organic matter and light penetration: effects on bacterial and primary production in lakes. Limnol Oceanogr 54:2034–2040

    Article  Google Scholar 

  • Ask J, Karlsson J, Persson L, Ask P, Bystrom P, Jansson M (2009b) Whole-lake estimates of carbon flux through algae and bacteria in benthic and pelagic habitats of clear-water lakes. Ecology 90:1923–1932

    Article  PubMed  Google Scholar 

  • Baumgärtner D, Rothhaupt KO (2003) Predictive length-dry mass regressions for freshwater invertebrates in a pre-alpine lake littoral. Int Rev Hydrobiol 88:453–463

    Article  Google Scholar 

  • Blomqvist P, Jansson M, Drakare S, Bergstrom AK, Brydsten L (2001) Effects of additions of DOC on pelagic biota in a clearwater system: results from a whole lake experiment in northern Sweden. Microb Ecol 42:383–394

    Article  PubMed  CAS  Google Scholar 

  • Botrell HH, Duncan A, Gliwicz ZM, Grygierek E, Herzig A, Hillbricht-Ilkowska A, Kurasawa H, Larsson P, Weglenska T (1976) A review of some problems in zooplankton production studies. Norwegian J Zool 24:419–456

    Google Scholar 

  • Brett MT, Kainz MJ, Taipale SJ, Seshan H (2009) Phytoplankton, not allochthonous carbon, sustains herbivorous zooplankton production. Proc Natl Acad Sci USA 106:21197–21201

    Article  PubMed  CAS  Google Scholar 

  • Caraco N, Bauer JE, Cole JJ, Petsch S, Raymond P (2010) Millennial-aged organic carbon subsidies to a modern river food web. Ecology 91:2385–2393

    Article  PubMed  Google Scholar 

  • Carpenter SR, Cole JJ, Kitchell JF, Pace ML (1998) Impact of dissolved organic carbon, phosphorus, and grazing on phytoplankton biomass and production in experimental lakes. Limnol Oceanogr 43:73–80

    Article  CAS  Google Scholar 

  • Carpenter SR, Cole JJ, Pace ML, Van de Bogert M, Bade DL, Bastviken D, Gille CM, Hodgson JR, Kitchell JF, Kritzberg ES (2005) Ecosystem subsidies: terrestrial support of aquatic food webs from C-13 addition to contrasting lakes. Ecology 86:2737–2750

    Article  Google Scholar 

  • Cole JJ, Caraco NF, Likens GE (1990) Short-range atmospheric transport-a significant source of phosphorus to an oligotrophic lake. Limnol Oceanogr 35:1230–1237

    Article  CAS  Google Scholar 

  • Cole JJ, Carpenter SR, Kitchell JF, Pace ML (2002) Pathways of organic carbon utilization in small lakes: results from a whole-lake C-13 addition and coupled model. Limnol Oceanogr 47:1664–1675

    Article  CAS  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

    Article  PubMed  Google Scholar 

  • Cole JJ, Carpenter SR, Kitchell JF, Pace ML, Solomon CT, Weidel B (2011) Strong evidence for terrestrial support of zooplankton in small lakes based on stable isotopes of carbon, nitrogen, and hydrogen. Proc Natl Acad Sci USA 108:1975–1980

    Article  PubMed  CAS  Google Scholar 

  • DeNiro MJ, Epstein S (1977) Mechanism of carbon isotope fractionation associated with lipid-synthesis. Science 197:261–263

    Article  PubMed  CAS  Google Scholar 

  • Dhital S, Shrestha AK, Gidley MJ (2010) Relationship between granule size and in vitro digestibility of maize and potato starches. Carbohydr Polym 82:480–488

    Article  CAS  Google Scholar 

  • Ducklow HW, Purdie DA, Williams PJL, Davies JM (1986) Bacterioplankton—a sink for carbon in a coastal marine plankton community. Science 232:865–867

    Article  PubMed  CAS  Google Scholar 

  • France RL (1996) Stable isotopic survey of the role of macrophytes in the carbon flow of aquatic foodwebs. Vegetatio 124:67–72

    Article  Google Scholar 

  • Francis TB, Schindler DE, Holtgrieve GW, Larson ER, Scheuerell MD, Semmens BX, Ward EJ (2011) Habitat structure determines resource use by zooplankton in temperate lakes. Ecol Lett 14:364–372

    Article  PubMed  Google Scholar 

  • Grey J, Jones RI, Sleep D (2000) Stable isotope analysis of the origins of zooplankton carbon in lakes of differing trophic state. Oecologia 123:232–240

    Article  Google Scholar 

  • Grey J, Jones RI, Sleep D (2001) Seasonal changes in the importance of the source of organic matter to the diet of zooplankton in Loch Ness, as indicated by stable isotope analysis. Limnol Oceanogr 46:505–513

    Article  Google Scholar 

  • Hansson LA, Tranvik LJ (2003) Food webs in sub-Antarctic lakes: a stable isotope approach. Polar Biol 26:783–788

    Article  Google Scholar 

  • Hecky RE, Hesslein RH (1995) Contributions of benthic algae to lake food webs as revealed by stable isotope analysis. J N Am Benthol Soc 14:631–653

    Article  Google Scholar 

  • Hessen D, Nygaard K (1992) Bacterial transfer of methane and detritus: implications for the pelagic carbon budget and gaseous state. Arch Hydrobiol 37:139–148

    CAS  Google Scholar 

  • Hoch MP, Fogel ML, Kirchman DL (1994) Isotope fractionation during ammonium uptake by marine microbial assemblages. Geomicrobiol J 12:113–127

    Article  CAS  Google Scholar 

  • Jansson M, Persson L, De Roos AM, Jones RI, Tranvik LJ (2007) Terrestrial carbon and intraspecific size-variation shape lake ecosystems. Trends Ecol Evol 22:316–322

    Article  PubMed  Google Scholar 

  • Johnston TA, Cunjak RA (1999) Dry mass-length relationships for benthic insects: a review with new data from Catamaran Brook, New Brunswick, Canada. Freshw Biol 41:653–674

    Article  Google Scholar 

  • Jones RI (1992) The influence of humic substances on lacustrine planktonic food chains. Hydrobiologia 229:73–91

    Article  CAS  Google Scholar 

  • Karlsson J (2007) Different carbon support for respiration and secondary production in unproductive lakes. Oikos 116:1691–1696

    Article  CAS  Google Scholar 

  • Karlsson J, Säwström C (2009) Benthic algae support zooplankton growth during winter in a clear-water lake. Oikos 118:539–544

    Google Scholar 

  • Karlsson J, Jonsson A, Meili M, Jansson M (2003) Control of zooplankton dependence on allochthonous organic carbon in humic and clear-water lakes in northern Sweden. Limnol Oceanogr 48:269–276

    Article  Google Scholar 

  • Karlsson J, Jonsson A, Meili M, Jansson M (2004) δ15N of zooplankton species in subarctic lakes in northern Sweden: effects of diet and trophic fractionation. Freshw Biol 49:526–534

    Article  Google Scholar 

  • Karlsson J, Ask J, Jansson M (2008) Winter respiration of allochthonous and autochthonous organic carbon in a subarctic clear-water lake. Limnol Oceanogr 53:948–954

    Article  CAS  Google Scholar 

  • Kiljunen M, Grey J, Sinisalo T, Harrod C, Immonen H, Jones RI (2006) A revised model for lipid-normalizing delta C-13 values from aquatic organisms, with implications for isotope mixing models. J Appl Ecol 43:1213–1222

    Article  CAS  Google Scholar 

  • Klug JL (2005) Bacterial response to dissolved organic matter affects resource availability for algae. Can J Fish Aquat Sci 62:472–481

    Article  CAS  Google Scholar 

  • Kortelainen P, Pajunen H, Rantakari M, Saarnisto M (2004) A large carbon pool and small sink in boreal Holocene lake sediments. Glob Change Biol 10:1648–1653

    Article  Google Scholar 

  • McConnaughey T, McRoy CP (1979) Food-web structure and the fractionation of carbon isotopes in the Bering Sea. Mar Biol 53:257–262

    Article  CAS  Google Scholar 

  • McGoldrick DJ, Barton DR, Power M, Scott RW, Butler BJ (2008) Dynamics of bacteria-substrate stable isotope separation: dependence on substrate availability and implications for aquatic food web studies. Can J Fish Aquat Sci 65:1983–1990

    Article  CAS  Google Scholar 

  • Pace ML, Cole JJ, Carpenter SR, Kitchell JF, Hodgson 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 427:240–243

    Article  PubMed  CAS  Google Scholar 

  • Phillips DL, Gregg JW (2001) Uncertainty in source partitioning using stable isotopes. Oecologia 127:171–179

    Article  Google Scholar 

  • Polis GA, Strong DR (1996) Food web complexity and community dynamics. Am Nat 147:813–846

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Porter ET, Sanford LP, Gust G, Porter FS (2004) Combined water-column mixing and benthic boundary-layer flow in mesocosms: key for realistic benthic-pelagic coupling studies. Mar Ecol Prog Ser 271:43–60

    Article  Google Scholar 

  • Post DM (2002) Using stable isotopes to estimate trophic position: models, methods, and assumptions. Ecology 83:703–718

    Article  Google Scholar 

  • Post DM, Layman CA, Arrington DA, Takimoto G, Quattrochi J, Montana CG (2007) Getting to the fat of the matter: models, methods and assumptions for dealing with lipids in stable isotope analyses. Oecologia 152:179–189

    Article  PubMed  Google Scholar 

  • Preston ND, Carpenter SR, Cole JJ, Pace ML (2008) Airborne carbon deposition on a remote forested lake. Aquat Sci 70:213–224

    Article  CAS  Google Scholar 

  • Rautio M, Vincent WF (2007) Isotopic analysis of the sources of organic carbon for zooplankton in shallow subarctic and arctic waters. Ecography 30:77–87

    Google Scholar 

  • Schindler DE, Scheuerell MD (2002) Habitat coupling in lake ecosystems. Oikos 98:177–189

    Article  Google Scholar 

  • Schmid-Araya JM, Schmid PE (2000) Trophic relationships: integrating meiofauna into a realistic benthic food web. Freshw Biol 44:149–163

    Article  Google Scholar 

  • Schmidt SN, Olden JD, Solomon CT, Vander Zanden MJ (2007) Quantitative approaches to the analysis of stable isotope food web data. Ecology 88:2793–2802

    Article  PubMed  Google Scholar 

  • Schmidt SN, Vander Zanden MJ, Kitchell JF (2009) Long-term food web change in Lake Superior. Can J Fish Aquat Sci 66:2118–2129

    Article  Google Scholar 

  • Smock LA (1980) Relationships between body size and biomass of aquatic insects. Freshw Biol 10:375–383

    Article  Google Scholar 

  • Smyntek PM, Teece MA, Schulz KL, Thackeray SJ (2007) A standard protocol for stable isotope analysis of zooplankton in aquatic food web research using mass balance correction models. Limnol Oceanogr 52:2135–2146

    Article  CAS  Google Scholar 

  • Solomon CT, Carpenter SR, Cole JJ, Pace ML (2008) Support of benthic invertebrates by detrital resources and current autochthonous primary production: results from a whole-lake C-13 addition. Freshw Biol 53:42–54

    CAS  Google Scholar 

  • Solomon CT, Carpenter SR, Clayton MK, Cole JJ, Coloso JJ, Pace ML, Vander Zanden MJ, Weidel BC (2011) Terrestrial, benthic, and pelagic resource use in lakes: results from a three-isotope Bayesian mixing model. Ecology 92:1115–1125

    Article  PubMed  Google Scholar 

  • Sommer U, Sommer F (2006) Cladocerans versus copepods: the cause of contrasting top-down controls on freshwater and marine phytoplankton. Oecologia 147:183–194

    Article  PubMed  Google Scholar 

  • Stets EG, Cotner JB (2008) The influence of dissolved organic carbon on bacterial phosphorus uptake and bacteria phytoplankton dynamics in two Minnesota lakes. Limnol Oceanogr 53:137–147

    Article  CAS  Google Scholar 

  • Tranvik LJ (1988) Availability of dissolved organic carbon for planktonic bacteria in oligotrophic lakes of different humic content. Microb Ecol 16:311–322

    Article  CAS  Google Scholar 

  • Vadeboncoeur Y, Vander Zanden MJ, Lodge DM (2002) Putting the lake back together: reintegrating benthic pathways into lake food web models. Bioscience 52:44–54

    Article  Google Scholar 

  • von Wachenfeldt E, Tranvik LJ (2008) Sedimentation in boreal lakes-the role of flocculation of allochthonous dissolved organic matter in the water column. Ecosystems 11:803–814

    Article  CAS  Google Scholar 

  • Zar JH (1996) Biostatistical analysis. Prentice Hall, Upper Saddle River

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Acknowledgments

We thank Erik Geibrink and Mercè Berga for their sampling assistance during the experiment and Amber Rice and two anonymous reviewers for helpful comments on the manuscript. This study is part of the project Lake Ecosystem Response to Environmental Change (LEREC) and was funded by the Swedish Research Council for Environmental, Agricultural and Spatial Planning (FORMAS).

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Correspondence to Pia Bartels.

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Communicated by Craig Osenberg.

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Bartels, P., Cucherousset, J., Gudasz, C. et al. Terrestrial subsidies to lake food webs: an experimental approach. Oecologia 168, 807–818 (2012). https://doi.org/10.1007/s00442-011-2141-7

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  • DOI: https://doi.org/10.1007/s00442-011-2141-7

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