Skip to main content
SpringerLink
Log in

Dissolved Organic Carbon Reduces Habitat Coupling by Top Predators in Lake Ecosystems

  • Published:
Ecosystems Aims and scope Submit manuscript

Abstract

Increasing input of terrestrial dissolved organic carbon (DOC) has been identified as a widespread environmental phenomenon in many aquatic ecosystems. Terrestrial DOC influences basal trophic levels: it can subsidize pelagic bacterial production and impede benthic primary production via light attenuation. However, little is known about the impacts of elevated DOC concentrations on higher trophic levels, especially on top consumers. Here, we used Eurasian perch (Perca fluviatilis) to investigate the effects of increasing DOC concentrations on top predator populations. We applied stable isotope analysis and geometric morphometrics to estimate long-term resource and habitat utilization of perch. Habitat coupling, the ability to exploit littoral and pelagic resources, strongly decreased with increasing DOC concentrations due to a shift toward feeding predominantly on pelagic resources. Simultaneously, resource use and body morphology became increasingly alike for littoral and pelagic perch populations with increasing DOC, suggesting more intense competition in lakes with high DOC. Eye size of perch increased with increasing DOC concentrations, likely as a result of deteriorating visual conditions, suggesting a sensory response to environmental change. Increasing input of DOC to aquatic ecosystems is a common result of environmental change and might affect top predator populations in multiple and complex ways.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Figure 1
Figure 2
Figure 3

Similar content being viewed by others

References

  • Ask J, Karlsson J, Persson L, Ask P, Byström P, Jansson M. 2009. Terrestrial organic matter and light penetration: effects on bacterial and primary production in lakes. Limnol Oceanogr 54:2034–40.

    Article  Google Scholar 

  • Bartels P, Hirsch PE, Svanbäck R, Eklöv P. 2012. Water transparency drives intra-population divergence in Eurasian perch (Perca fluviatilis). PLoS One 7:e43641.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Batschelet E. 1981. Circular Statistics in Biology. London: Academic Press.

    Google Scholar 

  • Bolnick DI, Svanbäck R, Fordyce JA, Yang LH, Davis JM, Hulsey CD, Forister ML. 2003. The ecology of individuals: incidence and implications of individual specialization. Am Nat 161:1–28.

    Article  PubMed  Google Scholar 

  • Briand F, Cohen JE. 1987. Environmental correlates of food-chain length. Science 238:956–60.

    Article  CAS  PubMed  Google Scholar 

  • Bukaveckas PA, Robbins-Forbes M. 2000. Role of dissolved organic carbon in the attenuation of photosynthetically active and ultraviolet radiation in Adirondack lakes. Freshw Biol 43:339–54.

    Article  Google Scholar 

  • Carter MW, Shoup DE, Dettmers JM, Wahl DH. 2010. Effects of turbidity and cover on prey selectivity of adult smallmouth bass. Trans Am Fish Soc 139:353–61.

    Article  Google Scholar 

  • Clark JM, Bottrell SH, Evans CD, Monteith DT, Bartlett R, Rose R, Newton RJ, Chapman PJ. 2010. The importance of the relationship between scale and process in understanding long-term DOC dynamics. Sci Total Environ 408:2768–75.

    Article  CAS  PubMed  Google Scholar 

  • Craig N, Jones SE, Weidel BC, Solomon CT. 2015. Habitat, not resource availability, limits consumer production in lake ecosystems. Limnol Oceanogr 60:2079–89.

    Article  Google Scholar 

  • Dolson R, McCann K, Rooney N, Ridgway M. 2009. Lake morphometry predicts the degree of habitat coupling by a mobile predator. Oikos 118:1230–8.

    Article  Google Scholar 

  • Downing JA, Prairie YT, Cole JJ, Duarte CM, Tranvik LJ, Striegl RG, McDowell WH, Kortelainen P, Caraco NF, Melack JM, Middelburg JJ. 2006. The global abundance and size distribution of lakes, ponds, and impoundments. Limnol Oceanogr 51:2388–97.

    Article  Google Scholar 

  • Drinan TJ, McGinnity P, Coughlan JP, Cross TF, Harrison SSC. 2012. Morphological variability of Atlantic salmon Salmo salar and brown trout Salmo trutta in different river environments. Ecol Freshw Fish 21:420–32.

    Article  Google Scholar 

  • Duffy MA. 2010. Ecological consequences of intraspecific variation in lake Daphnia. Freshw Biol 55:995–1004.

    Article  Google Scholar 

  • Ehlinger T, Wilson D. 1988. Complex foraging polymorphism in bluegill sunfish. Proc Natl Acad Sci USA 85:1878–82.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Eklöv P, Svanbäck R. 2006. Predation risk influences adaptive morphological variation in fish populations. Am Nat 167:440–52.

    Article  PubMed  Google Scholar 

  • Von der Emde G, Mogdans J, Kapoor BG. 2004. The senses of fish: adaptations for the reception of natural stimuli. The Netherlands: Springer.

    Book  Google Scholar 

  • Estlander S, Nurminen L, Olin M, Vinni M, Immonen S, Rask M, Ruuhijarvi J, Horppila J, Lehtonen H. 2010. Diet shifts and food selection of perch Perca fluviatilis and roach Rutilus rutilus in humic lakes of varying water colour. J Fish Biol 77:241–56.

    Article  CAS  PubMed  Google Scholar 

  • Finstad AG, Helland IP, Ugedal O, Hesthagen T, Hessen DO. 2014. Unimodal response of fish yield to dissolved organic carbon. Ecol Lett 17:36–43.

    Article  PubMed  Google Scholar 

  • Ganz HH, Ebert D. 2010. Benefits of host genetic diversity for resistance to infection depend on parasite diversity. Ecology 91:1263–8.

    Article  PubMed  PubMed Central  Google Scholar 

  • Gregory RS, Northcote TG. 1993. Surface, planktonic, and benthic foraging by juvenile Chinook salmon (Oncorhynchus tshawytscha) in turbid laboratory conditions. Can J Fish Aquat Sci 50:233–40.

    Article  Google Scholar 

  • Hampton SE, Fradkin SC, Leavitt PR, Rosenberger EE. 2011. Disproportionate importance of nearshore habitat for the food web of a deep oligotrophic lake. Mar Freshw Res 62:350–8.

    Article  CAS  Google Scholar 

  • Harvey BC, White JL. 2008. Use of benthic prey by salmonids under turbid conditions in a laboratory stream. Trans Am Fish Soc 137:1756–63.

    Article  Google Scholar 

  • Herberich E, Sikorski J, Hothorn T. 2010. A robust procedure for comparing multiple means under heteroscedasticity in unbalanced designs. PLoS One 5:e9788.

    Article  PubMed  PubMed Central  Google Scholar 

  • Hjelm J, Svanbäck R, Byström P, Persson L, Wahlström E. 2001. Diet-dependent body morphology and ontogentic reaction norms in Eurasian perch. Oikos 95:311–23.

    Article  Google Scholar 

  • Hobson KA, Clark RG. 1992. Assessing avian diets using stable isotopes I: Turnover of 13C in tissues. Condor 94:181–8.

    Article  Google Scholar 

  • Jackson AL, Inger R, Parnell AC, Bearhop S. 2011. Comparing isotopic niche widths among and within communities: SIBER—Stable Isotope Bayesian Ellipses in R. J Anim Ecol 80:595–602.

    Article  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Karlsson J, Byström P. 2005. Littoral energy mobilization dominates energy supply for top consumers in subarctic lakes. Limnol Oceanogr 50:538–43.

    Article  CAS  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 

  • Kelly PT, Solomon CT, Weidel BC, Jones SE. 2014. Terrestrial carbon is a resource, but not a subsidy, for lake zooplankton. Ecology 95:1236–42.

    Article  PubMed  Google Scholar 

  • Kent C, Wong J. 1982. An index of littoral-zone complexity and its measurement. Can J Fish Aquat Sci 39:847–53.

    Article  Google Scholar 

  • Layman CA, Arrington DA, Montana CG, Post DM. 2007. Can stable isotope ratios provide for community-wide measures of trophic structure? Ecology 88:42–8.

    Article  PubMed  Google Scholar 

  • Monteith DT, Stoddard JL, Evans CD, de Wit HA, Forsius M, Hogasen T, Wilander A, Skjelkvale BL, Jeffries DS, Vuorenmaa J, Keller B, Kopacek J, Vesely J. 2007. Dissolved organic carbon trends resulting from changes in atmospheric deposition chemistry. Nature 450:537–40.

    Article  CAS  PubMed  Google Scholar 

  • Northcote D, Volkman F, Yager D. 1978. Vision in fishes: color and pattern. In: Mostotsky D, Ed. The behavior of fish and other aquatic animals. New York: Academic Press. p 79–136.

    Google Scholar 

  • Oksanen L, Fretwell SD, Arruda J, Niemela P. 1981. Exploitation ecosystems in gradients of primary productivity. Am Nat 118:240–61.

    Article  Google Scholar 

  • Olsson J, Svanbäck R, Eklöv P. 2006. Growth rate constrain morphological divergence when driven by competition. Oikos 115:15–22.

    Article  Google Scholar 

  • Parnell AC, Inger R, Bearhop S, Jackson AL. 2010. Source partitioning using stable isotopes: coping with too much variation. PLoS One 5:e9672.

    Article  PubMed  PubMed Central  Google Scholar 

  • Persson L, Byström P, Wahlström E. 2000. Cannibalism and competition in Eurasian perch: population dynamics of an ontogenetic omnivore. Ecology 81:1058–71.

    Article  Google Scholar 

  • Persson L, De Roos AM, Claessen D, Byström P, Lövgren J, Sjögren S, Svanbäck R, Wahlström E, Westman E. 2003. Gigantic cannibals driving a whole-lake trophic cascade. Proc Natl Acad Sci 100:4035–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Phillips DL, Gregg JW. 2001. Uncertainty in source partitioning using stable isotopes. Oecologia 127:171–9.

    Article  CAS  PubMed  Google Scholar 

  • Pinnegar JK, Polunin NVC. 1999. Differential fractionation of δ13C and δ15N among fish tissues: implications for the study of trophic interactions. Funct Ecol 13:225–31.

    Article  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. Annu Rev Ecol Syst 28:289–316.

    Article  Google Scholar 

  • Post DM. 2002. Using stable isotopes to estimate trophic position: models, methods, and assumptions. Ecology 83:703–18.

    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 152:179–89.

    Article  PubMed  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 

  • Quevedo M, Svanbäck R, Eklöv P. 2009. Intrapopulation niche partitioning in a generalist predator limits food web connectivity. Ecology 90:2263–74.

    Article  PubMed  Google Scholar 

  • R Core Team. 2014. R: a language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing. http://111.r-project.org/.

  • Ranåker L, Jönsson M, Nilsson PA, Brönmark C. 2012. Effects of brown and turbid water on piscivore-prey fish interactions along a visibility gradient. Freshw Biol 57:1761–8.

    Article  Google Scholar 

  • Rooney N, McCann K, Gellner G, Moore JC. 2006. Structural asymmetry and the stability of diverse food webs. Nature 442:265–9.

    Article  CAS  PubMed  Google Scholar 

  • Rooney N, McCann KS, Moore JC. 2008. A landscape theory for food web architecture. Ecol Lett 11:867–81.

    Article  PubMed  Google Scholar 

  • Schindler DE, Scheuerell MD. 2002. Habitat coupling in lake ecosystems. Oikos 98:177–89.

    Article  Google Scholar 

  • Seekell DA, Lapierre J-F, Ask J, Bergström A-K, Deininger A, Rodriguez P, Karlsson J. 2015. The influence of dissolved organic carbon on primary production in northern lakes. Limnol Oceanogr 60:1276–85.

    Article  CAS  Google Scholar 

  • Smith TB, Skúlason S. 1996. Evolutionary significance of resource polymorphisms in fishes, amphibians, and birds. Annu Rev Ecol Syst 27:111–33.

    Article  Google Scholar 

  • Solomon CT, Jones SE, Weidel BC, Buffam I, Fork ML, Karlsson J, Larsen S, Lennon JT, Read JS, Sadro S, Saros JE. 2015. Ecosystem consequences of changing inputs of terrestrial dissolved organic matter to lakes: current knowledge and future challenges. Ecosystems 18:376–89.

    Article  Google Scholar 

  • Svanbäck R, Eklöv P. 2002. Effects of habitat and food resources on morphology and ontogenetic growth trajectories in perch. Oecologia 131:61–70.

    Article  Google Scholar 

  • Svanbäck R, Eklöv P. 2003. Morphology dependent foraging efficiency in perch: a trade-off for ecological specialization? Oikos 102:273–84.

    Article  Google Scholar 

  • Svanbäck R, Eklöv P. 2004. Morphology in perch affects habitat specific feeding efficiency. Funct Ecol 18:503–10.

    Article  Google Scholar 

  • Svanbäck R, Eklöv P, Fransson R, Holmgren K. 2008. Intraspecific competition drives multiple species resource polymorphism in fish communities. Oikos 117:114–24.

    Article  Google Scholar 

  • Svanbäck R, Persson L. 2009. Population density fluctuations change the selection gradient in Eurasian perch. Am Nat 173:507–16.

    Article  PubMed  Google Scholar 

  • Thomas SM, Crowther TW. 2015. Predicting rates of isotopic turnover across the animal kingdom: a synthesis of existing data. J Anim Ecol 84:861–70.

    Article  PubMed  Google Scholar 

  • Tranvik L. 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 

  • Vadeboncoeur Y, McCann KS, Vander Zanden MJ, Rasmussen JB. 2005. Effects of multi-chain omnivory on the strength of trophic control in lakes. Ecosystems 8:682–93.

    Article  Google Scholar 

  • Vadeboncoeur Y, Peterson G, Vander Zanden MJ, Kalff J. 2008. Benthic algal production across lake size gradients: interactions among morphometry, nutrients, and light. Ecology 89:2542–52.

    Article  PubMed  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 

  • Vander Zanden MJ, Vadeboncoeur Y. 2002. Fishes as integrators of benthic and pelagic food webs in lakes. Ecology 83:2152–61.

    Article  Google Scholar 

  • Vander Zanden MJ, Vadeboncoeur Y, Chandra S. 2011. Fish reliance on littoral-benthic resources and the distribution of primary production in lakes. Ecosystems 14:894–903.

    Article  Google Scholar 

  • Zelditch M, Swiderski D, Sheets H, Fink W. 2004. Geometric morphometrics for biologists. Burlington: Elsevier Academic Press Inc.

    Google Scholar 

Download references

Acknowledgements

We thank J Malmberg, E Geibrink, M Puffer, M Möst, and A Klaussén for help in the field and in the lab and the two anonymous reviewers for their highly valuable comments on a previous version of the manuscript. This study was financed by grants from the Swedish Research Council for Environment, Agricultural Sciences, and Spatial Planning (FORMAS) to PB and PE, the Swedish Research Council (VR) to PE and RS, the Uppsala Graduate School to PEH, and the Malmén´s Foundation to PB and PEH.

Author information

Author notes

    Authors and Affiliations

    1. Department of Ecology and Environmental Science, Umeå University, Umeå, Sweden

      Pia Bartels

    2. Department of Ecology and Genetics, Uppsala University, Uppsala, Sweden

      Pia Bartels, Philipp Emanuel Hirsch, Richard Svanbäck & Peter Eklöv

    3. Program Man-Society-Environment, University of Basel, Basel, Switzerland

      Philipp Emanuel Hirsch

    Authors
    1. Pia Bartels
      View author publications

      You can also search for this author in PubMed Google Scholar

    2. Philipp Emanuel Hirsch
      View author publications

      You can also search for this author in PubMed Google Scholar

    3. Richard Svanbäck
      View author publications

      You can also search for this author in PubMed Google Scholar

    4. Peter Eklöv
      View author publications

      You can also search for this author in PubMed Google Scholar

    Corresponding author

    Correspondence to Pia Bartels.

    Additional information

    Authors’ contribution

    Pia Bartels and Peter Eklöv conceived, designed, and conducted the study. Philipp Emanuel Hirsch and Richard Svanbäck contributed data. Pia Bartels analyzed the data and wrote the manuscript. All authors contributed substantially to the final version of the manuscript.

    Electronic supplementary material

    Below is the link to the electronic supplementary material.

    Supplementary material 1 (DOCX 542 kb)

    Rights and permissions

    Reprints and permissions

    About this article

    Check for updates. Verify currency and authenticity via CrossMark

    Cite this article

    Bartels, P., Hirsch, P.E., Svanbäck, R. et al. Dissolved Organic Carbon Reduces Habitat Coupling by Top Predators in Lake Ecosystems. Ecosystems 19, 955–967 (2016). https://doi.org/10.1007/s10021-016-9978-x

    Download citation

    • Received:

    • Accepted:

    • Published:

    • Issue Date:

    • DOI: https://doi.org/10.1007/s10021-016-9978-x

    Keywords

    Search

    Navigation