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Whole-Lake Sugar Addition Demonstrates Trophic Transfer of Dissolved Organic Carbon to Top Consumers

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Abstract

Terrestrial dissolved organic carbon (DOC) provides an external carbon source to lake ecosystems. However, there is ongoing debate about whether external DOC that enters a lake can pass up the food web to support top consumers. We show, from experimental manipulation of a whole lake, that externally loaded DOC can contribute appreciably to fish biomass. Monthly additions of cane sugar with a distinct carbon stable isotope value during 2 years rapidly enriched the 13C content of zooplankton and macroinvertebrates, with a more gradual 13C enrichment of fish. After sugar addition stopped, the 13C content of consumers reverted towards original values. A simple isotope mixing model indicated that by the end of the sugar addition almost 20% of fish carbon in the lake was derived from the added sugar. Our results provide the first direct experimental demonstration at relevant ecological spatial and temporal scales that externally loaded DOC to lakes can indeed transfer to top consumers.

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References

  • Ask J, Karlsson J, Persson L, Ask P, Bystrom P, Jansson M. 2009. Whole-lake estimates of carbon flux through algae and bacteria in benthic and pelagic habitats of clearwater lakes. Ecology 90:1923–32.

    Article  PubMed  Google Scholar 

  • Arvola L, Kankaala P, Tulonen T, Ojala A. 1996. Effects of phosphorus and allochthonous humic matter enrichment on the metabolic processes and community structure of plankton in a boreal lake. Can J Fish Aquat Sci 53:1646–62.

    Article  Google Scholar 

  • Bade DL, Carpenter SR, Cole JJ, Pace ML, Kritzberg E, Van de Bogert MC, Cory RM, McKnight DM. 2007. Sources and fates of dissolved organic carbon in lakes as determined by whole-lake carbon isotope additions. Biogeochemistry 84:115–29.

    Article  CAS  Google Scholar 

  • Baines SB, Pace ML. 1991. The production of dissolved organic matter by phytoplankton and its importance to bacteria—patterns across marine and freshwater systems. Limnol Oceanogr 36:1078–90.

    Article  Google Scholar 

  • Bartels P, Cucherousset J, Gudasz C, Jansson M, Karlsson J, Persson L, Premke K, Rubach A, Steger K, Tranvik LJ, Eklöv P. 2012. Terrestrial subsidies to lake food webs: an experimental approach. Oecologia 168:807–18.

    Article  PubMed  Google Scholar 

  • Bartels P, Hirsch PE, Svanbäck R, Peter Eklöv P. 2016. Dissolved organic carbon reduces habitat coupling by top predators in lake ecosystems. Ecosystems 19:955–67.

    Article  CAS  Google Scholar 

  • Berggren M, Strom L, Laudon H, Karlsson J, Jonsson A, Giesler R, Bergström A-K, Jansson M. 2010. Lake secondary production fueled by rapid transfer of low molecular weight organic carbon from terrestrial sources to aquatic consumers. Ecol Lett 13:870–80.

    Article  CAS  PubMed  Google Scholar 

  • Berggren M, Bergström A-K, Karlsson J. 2015. Intraspecific autochthonous and allochthonous resource use by zooplankton in a humic lake during the transitions between winter, summer and fall. PLoS ONE 10(3):e0120575. doi:10.1371/journal.pone.0120575.

    Article  PubMed  PubMed Central  Google Scholar 

  • Brett MT, Arhonditsis GB, Chandra S, Kainz MJ. 2012. Mass flux calculations show strong allochthonous support of freshwater zooplankton production is unlikely. PLoS ONE 7(6):e39508. doi:10.1371/journal.pone.0039508.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brett MT, Bunn SE, Chandra S, Galloway AWE, Guo F, Kainz MJ, Kankaala P, Lau DCP, Moulton TP, Power ME, Rasmussen JB, Taipale SJ, Thorp JH, Wehr JD. 2017. How important are terrestrial organic carbon inputs for secondary production in freshwater ecosystems? Freshw Biol 62:833–53.

    Article  CAS  Google Scholar 

  • Brett MT, Kainz MJ, Taipale SJ, Seshan H. 2009. Phytoplankton, not allochthonous carbon, sustains herbivorous zooplankton production. Proc Natl Acad Sci USA 106:21197–201.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Carpenter SR, Cole JJ, Pace ML, Van de Bogert M, Bade DL, Bastviken D et al. 2005. Ecosystem subsidies: terrestrial support of aquatic food webs from C-13 addition to contrasting lakes. Ecology 86:2737–50.

    Article  Google Scholar 

  • Cole JJ. 2013. Freshwater ecosystems and the carbon cycle. Excellence in ecology 18. Oldendorf: International Ecology Institute. pp 1–125.

    Google Scholar 

  • Cole JJ, Caraco NF, Kling GW, Kratz T. 1994. Carbon dioxide supersaturation in the surface waters of lakes. Science 165:1568–70.

    Article  Google Scholar 

  • Cole JJ, Carpenter SR, Kitchell J, 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 108:1975–80.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cole JJ, Carpenter SC, 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 9:558–68.

    Article  PubMed  Google Scholar 

  • del Giorgio PA, Peters RH. 1994. Patterns in planktonic P:R ratios in lakes: influence of lake trophy and dissolved organic C. Limnol Oceanogr 39:772–87.

    Article  Google Scholar 

  • Dodds WK, Cole JJ. 2007. Expanding the concept of trophic state in aquatic ecosystems: it’s not just the autotrophs. Aquat Sci 69:427–39.

    Article  CAS  Google Scholar 

  • Einola E, Rantakari M, Kankaala P, Kortelainen P, Ojala O, Pajunen H, Mäkelä S, Arvola L. 2011. Carbon pools and fluxes in a chain of five boreal lakes: a dry and wet year comparison. J Geophys Res 116:G03009. doi:10.1029/2010JG001636.

    Article  Google Scholar 

  • Elton CS. 1927. Animal ecology. New York: MacMillan. pp 1–260.

    Google Scholar 

  • Faithfull CL, Huss M, Vrede T, Karlsson J, Bergström A-K. 2012. Transfer of bacterial production based on labile carbon to higher trophic levels in an oligotrophic pelagic system. Can J Fish Aquat Sci 69:85–93.

    Article  CAS  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 46:505–13.

    Article  Google Scholar 

  • Guillemette F, McCallister L, del Giorgio PA. 2015. Selective consumption and metabolic allocation of terrestrial and algal carbon determine allochthony in lake bacteria. ISME J 10:1373–82.

    Article  PubMed  PubMed Central  Google Scholar 

  • Henriksen A, Skjelvåle BL, Mannio J, Wilander A, Harriman R, Curtis C, Jensen JP, Fjeld E, Moiseenko T. 1998. Northern European lake survey, 1995. Ambio 27:80–91.

    Google Scholar 

  • Hulatt CJ, Kaartokallio H, Asmala E, Autio R, Stedmon CA, Sonninen E, Oinonen M, Thomas DT. 2014. Bioavailability and radiocarbon age of fluvial dissolved organic matter (DOM) from a northern peatland-dominated catchment: effect of land-use change. Aquat Sci 76:393–404.

    Article  CAS  Google Scholar 

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

    Article  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Jones RI. 1998. Phytoplankton, primary production and nutrient cycling, chapter 7. In: Hessen DO, Tranvik L, Eds. Aquatic humic substances: ecology and biogeochemistry. Ecological studies 133. Berlin: Springer. p 145–75.

    Chapter  Google Scholar 

  • Jones RI, Laybourn-Parry J, Walton MC, Young JM. 1997. The forms and distribution of carbon in a deep, oligotrophic lake (Loch Ness, Scotland). Verh Int Ver Theor Angew Limnol 26:330–4.

    CAS  Google Scholar 

  • Jones RI, Grey J, Quarmby C, Sleep D. 2001. Sources and fluxes of inorganic carbon in a deep, oligotrophic lake (Loch Ness, Scotland). Global Biogeochem Cycles 15:863–70.

    Article  CAS  Google Scholar 

  • Jones SE, Lennon J. 2015. A test of the subsidy–stability hypothesis: the effects of terrestrial carbon in aquatic ecosystems. Ecology 96:1550–60.

    Article  Google Scholar 

  • Kankaala P, Arvola L, Tulonen T, Ojala A. 1996. Carbon budget for the pelagic food web of the euphotic zone in a boreal lake (Lake Pääjärvi). Can J Fish Aquat Sci 5:1663–74.

    Article  Google Scholar 

  • Kankaala P, Peura S, Nykänen H, Sonninen E, Taipale S, Tiirola M, Jones RI. 2010a. Impacts of added dissolved organic carbon on boreal freshwater pelagic metabolism and food webs in mesocosm experiments. Fundam Appl Limnol 177:161–76.

    Article  CAS  Google Scholar 

  • Kankaala P, Taipale S, Li L, Jones RI. 2010b. Diets of crustacean zooplankton, inferred from stable carbon and nitrogen isotope analyses, in lakes with varying allochthonous dissolved organic carbon content. Aquat Ecol 44:781–95.

    Article  Google Scholar 

  • Karlsson J, Bergström A-K, Byström P, Gudasz C, Rodriguez P, Hein C. 2015. Terrestrial organic matter input suppresses biomass production in lake ecosystems. Ecology 96:2870–6.

    Article  PubMed  Google Scholar 

  • Karlsson J, Byström P, Ask J, Ask P, Persson L, Jansson M. 2009. Light limitation of nutrient-poor lake ecosystems. Nature 460:506–9.

    Article  CAS  PubMed  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 48:269–76.

    Article  Google Scholar 

  • Karlsson J, Lymer D, Vrede K, Jansson M. 2007. Differences in efficiency of carbon transfer from dissolved organic carbon to two zooplankton groups: an enclosure experiment in an oligotrophic lake. Aquat Sci 69:108–14.

    Article  CAS  Google Scholar 

  • Karlsson J, Berggren M, Ask J, Byström P, Jonsson A, Laudon H, Jansson M. 2012. Terrestrial organic matter support of lake food webs: evidence from lake metabolism and stable hydrogen isotopes of consumers. Limnol Oceanogr 57:1042–8.

    Article  CAS  Google Scholar 

  • Kelly PK, Craig N, Solomon CT, Weidel BC, Zwart JA, Jones SE. 2016. Experimental whole-lake increase of dissolved organic carbon concentration produces unexpected increase in crustacean zooplankton density. Glob Change Biol 22:2766–75.

    Article  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 43:1213–22.

    Article  CAS  Google Scholar 

  • LeCren ED. 1947. The determination of age and growth of the perch (Perca fluviatilis) from the opercular bone. J Anim Ecol 16:188–204.

    Article  Google Scholar 

  • McMeans BG, Koussoropolis A-M, Arts MT, Kainz MJ. 2015. Terrestrial dissolved organic matter supports growth and reproduction of Daphnia magna when algae are limiting. J Plankton Res 37:1201–9.

    CAS  Google Scholar 

  • Mehner T, Attermeyer K, Brauns M, Brothers S, Diekmann J, Gaedke U, Grossart H-P, Köhler J, Lischke B, Meyer N, Scharnweber K, Syväranta J, Vanni MJ, Hilt S. 2016. Weak response of animal allochthony and production to enhanced supply of terrestrial leaf litter in nutrient-rich lakes. Ecosystems 19:311–25.

    Article  CAS  Google Scholar 

  • Monteith DT, Stoddard JL, Evans CD, de Wit HA, Forsius M, Hogasen T et al. 2007. Dissolved organic carbon trends resulting from changes in atmospheric deposition chemistry. Nature 450:537–40.

    Article  CAS  PubMed  Google Scholar 

  • Pace ML, Cole JJ, Carpenter SR, Kitchell JF, Hodgson JR, Van de Bogert MC et al. 2004. Whole-lake carbon-13 additions reveal terrestrial support of aquatic food webs. Nature 427:240–3.

    Article  CAS  PubMed  Google Scholar 

  • Pace M, Carpenter SC, Cole JJ, Coloso J, Kitchell J, Hodgson J, Middelburg J, Preston N, Solomon CT, Weidel B. 2007. Does terrestrial organic carbon subsidize the planktonic food web in a clear-water lake? Limnol Oceanogr 52:2177–89.

    Article  CAS  Google Scholar 

  • Peura S, Nykänen H, Kankaala P, Eiler A, Tiirola M, Jones RI. 2014. Enhanced greenhouse gas emissions and changes in plankton communities following an experimental increase in organic carbon loading to a humic lake. Biogeochemistry 118:177–94.

    Article  CAS  Google Scholar 

  • Post DM. 2002. The long and short of food-chain length. Trends Ecol Evol 17:269–77.

    Article  Google Scholar 

  • Premke K, Karlsson J, Steger K, Gudasz C, von Wachenfeldt E, Tranvik LJ. 2010. Stable isotope analysis of benthic fauna and their food sources in boreal lakes. J N Am Benthol Soc 29:1339–48.

    Article  Google Scholar 

  • Rask M. 1983. Differences in growth of perch (Perca fluviatilis L.) in two small forest lakes. Hydrobiologia 101:139–44.

    Article  Google Scholar 

  • Rask M. 1984. The effect of low pH on perch, Perca fluviatilis L. III. The perch population in a small, acidic, extremely humic forest lake. Ann Zool Fenn 2:15–22.

    Google Scholar 

  • Rask M, Arvola L. 1985. The biomass and production of pike, perch and whitefish in two small lakes in southern Finland. Ann Zool Fenn 22:129–36.

    Google Scholar 

  • Rask M, Verta M, Korhonen M, Salo S, Forsius M, Arvola L, Jones RI, Kiljunen M. 2010. Does lake thermocline depth affect methyl mercury concentrations in fish? Biogeochemistry 101:311–22.

    Article  CAS  Google Scholar 

  • Roulet N, Moore TR. 2006. Environmental chemistry—browning the waters. Nature 444:283–4.

    Article  CAS  PubMed  Google Scholar 

  • Salonen K, Kononen K, Arvola L. 1983. Respiration of plankton in two small, polyhumic lakes. Hydrobiologia 101:65–70.

    Article  Google Scholar 

  • Scharnweber K, Syväranta J, Hilt S, Brauns M, Vanni MJ, Brothers S, Köhler J, Knezevic-Jaric J, Mehner T. 2014. Whole-lake experiments reveal the fate of terrestrial particulate organic carbon in benthic food webs of shallow lakes. Ecology 95:1496–505.

    Article  CAS  PubMed  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 

  • Spence JR, Andersen NM. 1994. Biology of water striders: interactions between systematics and ecology. Annu Rev Entomol 39:101–28.

    Article  Google Scholar 

  • Strandberg U, Hiltunen M, Taipale SJ, Yeung S, Kankaala P 2017. Planktivorous vendace (Coregonus albula) utilize algae-derived fatty acids for biomass increase and lipid deposition. Ecol Freshw Fish. doi:10.1111/eff.12367.

  • Taipale S, Kankaala P, Tiirola M, Jones RI. 2008. Whole-lake dissolved inorganic C-13 additions reveal seasonal shifts in zooplankton diet. Ecology 89:463–74.

    Article  PubMed  Google Scholar 

  • Taipale S, Kankaala P, Hämäläinen H, Jones RI. 2009. Seasonal shifts in the diet of lake zooplankton revealed by phospholipid fatty acid analysis. Freshw Biol 54:90–104.

    Article  CAS  Google Scholar 

  • Taipale SJ, Galloway AWE, Aalto SL, Kahilainen KK, Strandberg U, Kankaala P. 2016a. Terrestrial carbohydrates support freshwater zooplankton during phytoplankton deficiency. Sci Rep 6:30897. doi:10.1038/srep30897.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Taipale S, Vuorio K, Strandberg U, Kahilainen KK, Järvinen M, Hiltunen M, Peltomaa E, Kankaala P. 2016b. Lake eutrophication and brownification downgrade availability and transfer of essential fatty acids for human consumption. Environ Int 96:156–66.

    Article  CAS  PubMed  Google Scholar 

  • Tanentzap AJ, Kielstra BW, Wilkinson GM, Berggren M, Craig N, del Giorgio PA, Grey J, Gunn JM, Jones SE, Karlsson J, Solomon CT, Pace ML. 2017. Terrestrial support of lake food webs: synthesis reveals controls over cross-ecosystem resource use. Sci Adv 3:e1601765.

    Article  PubMed  PubMed Central  Google Scholar 

  • Tranvik LJ. 1988. Availability of dissolved organic carbon for planktonic bacteria in oligotrophic lakes of differing humic content. Microb Ecol 16:311–22.

    Article  CAS  PubMed  Google Scholar 

  • Tranvik LJ. 1992. Allochthonous dissolved organic matter as an energy source for pelagic bacteria and the concept of the microbial loop. Hydrobiologia 229:107–14.

    Article  CAS  Google Scholar 

  • Tranvik LJ. 1998. Degradation of dissolved organic matter in humic waters by bacteria, chapter 10. In: Hessen DO, Tranvik L, Eds. Aquatic humic substances: ecology and biogeochemistry. Ecological studies 133. Berlin: Springer. p 145–75.

    Google Scholar 

  • Vesterinen J, Devlin SP, Syväranta J, Jones RI. 2016a. Accounting for littoral primary production by periphyton shifts a highly humic boreal lake towards net autotrophy. Freshw Biol 61:265–76.

    Article  Google Scholar 

  • Vesterinen J. 2017. Littoral energy pathways in highly humic boreal lakes. PhD Thesis, University of Jyväskylä, Jyväskylä, Finland, pp 1–46.

  • von Wachenfeldt E, Tranvik LJ. 2008. Sedimentation in boreal lakes—the role of flocculation of allochthonous dissolved organic matter in the water column. Ecosystems 11:803–14.

    Article  CAS  Google Scholar 

  • Vuorenmaa J, Forsius M, Mannio J. 2006. Increasing trends of total organic carbon concentrations in small forest lakes in Finland from, 1987 to 2003. Sci Total Environ 36:47–65.

    Article  Google Scholar 

  • Weidel B, Carpenter SR, Cole JJ, Hodgson J, Kitchell J, Pace ML, Solomon CT. 2008. Carbon sources supporting fish growth in a north temperate lake. Aquat Sci 70:446–58.

    Article  CAS  Google Scholar 

  • Weidel BC, Carpenter SR, Kitchell JF, Vander Zanden MJ. 2011. Rates and components of carbon turnover in fish muscle: insights from bioenergetics models and a whole-lake 13C addition. Can J Fish Aquat Sci 68:387–99.

    Article  CAS  Google Scholar 

  • Wetzel RG. 2001. Limnology: Lake and River Ecosystems. 3rd edn. Academic Press, San Diego, pp 1–1006.

    Book  Google Scholar 

  • Wilkinson GM, Pace ML, Cole JJ. 2013a. Terrestrial dominance of organic matter in north temperate lakes. Glob Biogeochem Cycles 27:1–9.

    Article  Google Scholar 

  • Wilkinson GM, Carpenter SC, Cole JJ, Pace ML, Yang C. 2013b. Terrestrial support of pelagic consumers: patterns and variability revealed by a multilake study. Freshw Biol 58:2037–49.

    Article  Google Scholar 

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Acknowledgements

This work was funded by Academy of Finland Grants 114604 and 137671 to RJ. We are grateful for the support from staff and facilities at Lammi Biological Station, University of Helsinki, and the Evo Station of the Natural Resources Institute Finland.

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Correspondence to Roger I. Jones.

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RIJ conceived and planned the study with advice from MR, obtained funding, led the data analysis and wrote the first draft of the manuscript; PK, HN, SP and SV collected data; all authors contributed substantially to the final manuscript.

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Jones, R.I., Kankaala, P., Nykänen, H. et al. Whole-Lake Sugar Addition Demonstrates Trophic Transfer of Dissolved Organic Carbon to Top Consumers. Ecosystems 21, 495–506 (2018). https://doi.org/10.1007/s10021-017-0164-6

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