Abstract
Fish can alter food web structure through trophic cascades. While most studies conducted in oligotrophic subarctic lakes show strong top–down control on consumers in the presence of fish, several studies undertaken in eutrophic subarctic Lake Mývatn, Iceland, suggest that it is consumer–resource interactions that drive the whole-lake community. Here, we used stable isotopes of carbon and nitrogen from the main food web compartments derived from a 3-month in situ-controlled mesocosm experiment involving two treatments (with and without fish) with three replicates each to determine the effects of fish on the trophic structure of the Lake Mývatn food web. We found that the whole food web trophic structure shifted towards the upper part of the water column (more planktonic habitat) in fishless enclosures. Additionally, the trophic niche of organisms occupying the base of the food web became more diversified when fish were absent, and the trophic redundancy of all taxa decreased (more dissimilar trophic niches). Stronger top–down effects may also result from global warming, producing increased abundance of planktivorous fish in subarctic lakes. Our results indicate that this could lead to a shift in trophic niche and reduced trophic diversity of most food web organisms.
Similar content being viewed by others
References
Abrams, P. A., 2007. Defining and measuring the impact of dynamic traits on interspecific interactions. Ecology 88: 2555–2562.
Adalsteinsson, H., 1979. Size and food of arctic char Salvelinus alpinus and stickleback Gasterosteus aculeatus in Lake Mývatn. Oikos 32: 228–231.
Bartrons, M., A. Einarsson, R. L. G. G. Nobre, Á. Einarsson, R. L. G. G. Nobre, C. M. Herren, K. C. Webert, S. Brucet, S. R. Ólafsdóttir & A. R. Ives, 2015. Spatial patterns reveal strong abiotic and biotic drivers of zooplankton community composition in Lake Myvatn, Iceland. Ecosphere 6: 1–20.
Boecklen, W. J., C. T. Yarnes, B. A. Cook & A. C. James, 2011. On the use of stable isotopes in trophic ecology. Annual Review of Ecology, Evolution, and Systematics Annual Reviews 42: 411–440.
Brodersen, J., H. J. Malmquist, F. Landkildehus, T. L. Lauridsen, S. L. Amsinck, R. Bjerring, M. Søndergaard, L. S. Johansson, K. S. Christoffersen & E. Jeppesen, 2012. Short-and long term niche segregation and individual specialization of brown trout (Salmo trutta) in species poor Faroese lakes. Environmental Biology of Fishes 93: 305–318.
Brucet, S., D. Boix, L. W. Nathansen, X. D. Quintana, E. Jensen, D. Balayla, M. Meerhoff & E. Jeppesen, 2012. Effects of temperature, salinity and fish in structuring the macroinvertebrate community in shallow lakes: implications for effects of climate change. PLoS ONE 7: e30877.
Burks, R. L., D. M. Lodge, E. Jeppesen & T. L. Lauridsen, 2002. Diel horizontal migration of zooplankton: costs and benefits of inhabiting the littoral. Freshwater Biology 47: 343–365.
Cañedo-Argüelles, M., S. Sgarzi, I. Arranz, X. D. Quintana, Z. Ersoy, F. Landkildehus, T. L. Lauridsen, E. Jeppesen & S. Brucet, 2017. Role of predation in biological communities in naturally eutrophic sub-Arctic Lake Mývatn, Iceland. Hydrobiologia 790: 213–223.
Carpenter, S. R. & J. F. Kitchell, 1993. The Trophic Cascade in Lakes. Cambridge University Press, Cambridge.
Deniro, M. J. & S. Epstein, 1978. Influence of the diet on the distribution of carbon isotopes in animals. Geochimica et Cosmochimica Acta 45: 495–506.
Dickman, M., K. Stewart & M. Servant-Vildary, 1993. Spatial heterogeneity of summer phytoplankton and water chemistry in a large volcanic spring-fed lake in northern Iceland. Arctic and Alpine Research INSTAAR, University of Colorado 25: 228–239.
Einarsson, Á., 2004. Lake Myvatn and the River Laxá: An introduction. Aquatic Ecology 38: 111–114.
Einarsson, Á. & E. B. Örnólfsdóttir, 2004. Long-term changes in benthic Cladocera populations in Lake Myvatn, Iceland. Aquatic Ecology 38: 253–262.
Einarsson, Á., A. Gardarsson, G. M. Gíslason & A. R. Ives, 2002. Consumer-resource interactions and cyclic population dynamics of Tanytarsus gracilentus (Diptera: Chironomidae). Journal of Animal Ecology 71: 832–845.
Einarsson, Á., G. Stefánsdóttir, H. Jóhannesson, J. S. Ólafsson, G. Már Gíslason, I. Wakana, G. Gudbergsson & A. Gardarsson, 2004. The ecology of Lake Myvatn and the River Laxá: variation in space and time. Aquatic Ecology 38: 317–348.
Einarsson, Á., U. Hauptfleisch, P. R. Leavitt & A. R. Ives, 2016. Identifying consumer-resource population dynamics using paleoecological data. Ecology 97: 361–371.
Epanchin, P. N., R. A. Knapp & S. P. Lawler, 2010. Nonnative trout impact an alpine-nesting bird by altering aquatic-insect subsidies. Ecology 91: 2406–2415.
Ersoy, Z., E. Jeppesen, S. Sgarzi, I. Arranz, M. Cañedo-Argüelles, X. D. Quintana, F. Landkildehus, T. L. Lauridsen, M. Bartrons & S. Brucet, 2017. Size based interactions and trophic transfer efficiency are modified by fish predation and cyanobacteria blooms in Lake Mývatn, Iceland. Freshwater Biology 62: 1942–1952.
Flecker, A. S. & C. R. Townsend, 1994. Community-Wide Consequences of Trout Introduction in New Zealand Streams. Ecological Applications Wiley Ecological Society of America 4: 798–807.
Fry, B., 2006. Stable Isotope Ecology. Springer, New York.
Gardarsson, A., Á. Einarsson, G. M. Gíslason, T. Hrafnsdóttir, H. R. Ingvason, E. Jónsson & J. S. Ólafsson, 2004. Population fluctuations of chironomid and simuliid Diptera at Myvatn in 1977–1996. Aquatic Ecology 38: 209–217.
Gelman, A. & J. Hill, 2007. Data Analysis Using Regression and Multilevel/Hierarchical Models. Cambridge University Press, Cambridge.
Gislason, G. M., A. Gudmundsson & A. Einarsson, 1998. Population densities of the three-spined stickleback (Gasterosteus aculeatus L.) in a shallow lake. Verhandlungen Internationale Verein Limnologie 26: 2244–2250.
González-Bergonzoni, I., F. Landkildehus, M. Meerhoff, T. L. Lauridsen, K. Özkan, T. A. Davidson, N. Mazzeo & E. Jeppesen, 2014. Fish determine macroinvertebrate food webs and assemblage structure in Greenland subarctic streams. Freshwater Biology 59: 1830–1842.
Graham, C. T. & C. Harrod, 2009. Implications of climate change for the fishes of the British Isles. Journal of Fish Biology Blackwell Publishing Ltd 74: 1143–1205.
Gu, B., C. L. Schelske & M. Brenner, 2006. Relationship between sediment and plankton isotope ratios (d13C and d15 N) and primary productivity in Florida lakes. Canadian Journal of Fisheries and Aquatic Sciences 883: 875–883.
Gudbergsson, G., 2004. Arctic charr in Lake Myvatn: the centennial catch record in the light of recent stock estimates. Aquatic Ecology Kluwer Academic Publishers 38: 271–285.
Gudmundsson, A., 1996. Hornsíli í Mývatni (Three-spined sticklebacks in Lake Myvatn). M. Sc. thesis. University of Iceland.
Hairston, N., F. Smith & L. Slobodkin, 1960. Community structure, population control, and competition. The American Naturalist 94: 421–425.
Hayden, B., J.-P. Myllykangas, R. J. Rolls & K. K. Kahilainen, 2017. Climate and productivity shape fish and invertebrate community structure in subarctic lakes. Freshwater Biology 62: 990–1003.
Hecky, R. E. & R. H. Hesslein, 1995. Contributions of benthic algae to lake food webs as revealed by stable isotope analysis. Journal of the North American Benthological Society 14: 631–653.
Herren, C. M., K. C. Webert, M. D. Drake, A. Einarsson, A. R. Ives & C. Gratton, 2017. Positive feedback between chironomids and algae creates net mutualism between benthic primary consumers and producers. Ecology 98: 447–455.
Huang, C. & A. Sih, 1990. Experimental studies on behaviorally mediated, indirect interactions through a shared predator. Ecology 71: 1515–1522.
Inger, R., A. Jackson, A. Parnell & S. Bearhop, 2014. SIAR V4 stable isotope analysis in R. Matrix 4: 1–14.
Ives, A. R., A. Einarsson, V. A. A. Jansen & A. Gardarsson, 2008. High-amplitude fluctuations and alternative dynamical states of midges in Lake Myvatn. Nature 452: 84–87.
Jackson, A. L., R. Inger, S. Bearhop & A. Parnell, 2009. Erroneous behaviour of MixSIR, a recently published Bayesian isotope mixing model: a discussion of Moore & Semmens (2008). Ecology letters 12: E1–E5.
Jackson, A. L., R. Inger, A. C. Parnell & S. Bearhop, 2011. Comparing isotopic niche widths among and within communities: SIBER—stable isotope bayesian ellipses in R. Journal of Animal Ecology 80: 595–602.
Jackson, M. M., M. G. Turner, S. M. Pearson & A. R. Ives, 2012. Seeing the forest and the trees: multilevel models reveal both species and community patterns. Ecosphere 3: art79.
Jeppesen, E., J. P. Jensen, C. Jensen, B. Faafeng, D. O. Hessen, M. Søndergaard, T. Lauridsen, P. Brettum & K. Christoffersen, 2003. The impact of nutrient state and lake depth on top-down control in the pelagic zone of lakes: a study of 466 lakes from the temperate zone to the Arctic. Ecosystems 6: 313–325.
Jeppesen, E., T. Mehner, I. J. Winfield, K. Kangur, J. Sarvala, D. Gerdeaux, M. Rask, H. J. Malmquist, K. Holmgren, P. Volta, S. Romo, R. Eckmann, A. Sandström, S. Blanco, A. Kangur, H. Ragnarsson Stabo, M. Tarvainen, A. M. Ventelä, M. Søndergaard, T. L. Lauridsen & M. Meerhoff, 2012. Impacts of climate warming on the long-term dynamics of key fish species in 24 European lakes. Hydrobiologia 694: 1–39.
Jeppesen, E., T. L. Lauridsen, K. S. Christoffersen, F. Landkildehus, P. Geertz-Hansen, S. L. Amsinck, M. Søndergaard, T. A. Davidson & F. Rigét, 2017. The structuring role of fish in Greenland lakes: an overview based on contemporary and paleoecological studies of 87 lakes from the low and the high Arctic. Hydrobiologia Springer International Publishing 800: 99–113.
Jónasson, P. M., 1979. Ecology of eutrophic, subarctic Lake Mývatn and the River Laxá. Icelandic Literature Society in Copenhagen.
Kohler, S. L. & M. A. McPeek, 1989. Predation risk and the foraging behavior of competing stream insects. Ecology Wiley Ecological Society of America 70: 1811–1825.
Lancaster, J., A. G. Hildrew & C. R. Townsend, 1988. Competition for space by predators in streams: field experiments on a net spinning caddisfly. Freshwater Biology 20: 185–193.
Layman, C. A., D. A. Arrington, C. G. Montana & D. M. Post, 2007. Can stable isotope ratios provide for community-wide measures of trophic structure? Ecology 88: 42–48.
Layman, C. A., M. S. Araujo, R. Boucek, C. M. Hammerschlag-Peyer, E. Harrison, Z. R. Jud, P. Matich, A. E. Rosenblatt, J. J. Vaudo, L. A. Yeager, D. M. Post & S. Bearhop, 2012. Applying stable isotopes to examine food-web structure: an overview of analytical tools. Biological Reviews 83: 545–562.
Leopold, A., L. K. Sowls & D. L. Spencer, 1947. A survey of over-populated deer ranges in the United States. The Journal of Wildlife Management 11: 162–177.
Lindegaard, C., P. M. Jónasson & P. M. Jonasson, 1979. Abundance, population dynamics and production of zoobenthos in lake Mývatn, Iceland. Oikos 32: 202–227.
Matley, J., A. Tobin, C. Simpfendorfer, A. Fisk & M. Heupel, 2017. Trophic niche and spatio-temporal changes in the feeding ecology of two sympatric species of coral trout (Plectropomus leopardus and P laevis). Marine Ecology Progress Series 563: 197–210.
McCutchan, J. H., W. M. Lewis, C. Kendall & C. C. McGrath, 2003. Variation in trophic shift for stable isotope ratios of carbon, nitrogen, and sulfur. Oikos 102: 378–390.
Mingawa, M., 1984. Stepwise enrichment of N-15 along food-chains—further evidence and the relation between delta-N-15 and animal age. Geochimica et Cosmochimica Acta 48: 1135–1140.
Moore, J. W. & B. X. Semmens, 2008. Incorporating uncertainty and prior information into stable isotope mixing models. Ecology letters 11: 470–480.
Naeem, S., R. Costanza, P. Ehrlich, F. Golley, D. Hooper, J. H. Lawton, R. O’Neill, H. Mooney, O. Sala, A. Symstad & D. Tilmam, 1999. Invasiones biológicas: Causas, epidemiología, consecuencias globales y control. Tópicos en ecología Wiley Ecological Society of America 5: 1–22.
Ólafsson, J., 1979a. Physical characteristics of Lake Myvatn and River Laxa. Oikos 32: 38–66.
Ólafsson, J., 1979b. The Chemistry of Lake Mývatn and River Laxá. Oikos 32: 82–112.
Orrock, J. L., L. M. Dill, A. Sih, J. H. Grabowski, S. D. Peacor, B. L. Peckarsky, E. L. Preisser, J. R. Vonesh & E. E. Werner, 2010. Predator effects in predator-free space: the remote effects of predators on prey. Open Journal of Ecology 3: 22–30.
Pace, M. L., J. J. Cole, S. R. Carpenter & J. F. Kitchell, 1999. Trophic cascades revealed in diverse ecosystems. Trends in Ecology & Evolution 14: 483–488.
Paine, R. T., 1966. Food web complexity and species diversity. The American Naturalist 100: 65–75.
Peckarsky, B. L. & A. R. McIntosh, 1998. Fitness and community consequences of avoiding multiple predators. Oecologia 113: 565–576.
Rigler, F. H., 1975. The Char Lake project, an introduction to limnology in the Canadian Arctic In Cameron. In Billingsley, L. W. (ed), Energy Flow—Its Biological Dimension A Summary of IBP in Canada, 1964–1974. Published for the Canadian Committee for the International Biological Programme by the Royal Society of Canada, Ottawa: 171–198.
Rist, S., 1979. Water level fluctuations and icecover of Lake Mývatn. Oikos 32: 67–81.
Takahashi, K., T. Yoshioka, E. Wada & M. Sakamoto, 1990. Temporal variations in carbon isotope ratio of phytoplankton in a eutrophic lake. Journal of Plankton Research 12: 799–808.
Team, R. C., 2017. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria, http://www.r-project.org.
Tiberti, R., A. von Hardenberg & G. Bogliani, 2014. Ecological impact of introduced fish in high altitude lakes: a case of study from the European Alps. Hydrobiologia 724: 1–19.
Vanni, M. J. & C. D. Layne, 1997. Nutrient recycling and herbivory as mechanisms in the “top-down” effects of fish on phytoplankton in lakes. Ecology Ecological Society of America 78: 21–40.
Webert, K. C., C. M. Herren, Á. Einarsson, M. Bartrons, U. Hauptfleisch & A. R. Ives, 2017. Midge-stabilized sediment drives the composition of benthic cladoceran communities in Lake Mývatn. Iceland. Ecosphere 8: e01659.
Woodward, G. & A. G. Hildrew, 2008. Invasion of a stream food web by a new top predator. Journal of Animal Ecology 70: 273–288.
Acknowledgements
We are grateful to Árni Einarsson from Mývatn Research Station (Iceland) for his advice, assistance and loan of facilities, to Elisabeth Badosa, Sergi Carrasco, Mariona Munné, Gisela Solà and Beatriz Tintoré for field and laboratory assistance, to Nicolas Vidal for help with the laboratory analyses of the stable isotopes and to the anonymous reviewers that helped to improve the manuscript. This project was supported by the Carlsberg Foundation (Project 2013_01_0535) and the MARS project (Managing Aquatic ecosystems and water Resources under multiple Stress) funded under the 7th EU Framework Programme, Theme 6 (Environment including Climate Change), Contract No.: 603378. EJ and TLL were further supported by AU Centre for Water Technology (WATEC). SB was supported by the Marie Curie Intra European Fellowship No. 330249 (CLIMBING) and by the project DFG, Me 1686/7-1. Xavier D. Quintana was supported by a Grant of the Spanish Ministerio de Economía y Competividad (CGL2016-76024-R).
Author information
Authors and Affiliations
Corresponding author
Additional information
Handling editor: Michael Power
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Bartrons, M., Arranz, I., Cañedo-Argüelles, M. et al. Fish shift the feeding behaviour and trophic niche diversification of their prey in subarctic Lake Mývatn, Iceland. Hydrobiologia 816, 243–254 (2018). https://doi.org/10.1007/s10750-018-3588-x
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10750-018-3588-x