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Stable isotope analysis confirms substantial differences between subtropical and temperate shallow lake food webs

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Abstract

Differences in trophic web structure in otherwise similar ecosystems as a consequence of direct or indirect effects of ambient temperature differences can lead to changes in ecosystem functioning. Based on nitrogen and carbon stable isotope analysis, we compared the food-web structure in a series of subtropical (Uruguay, 30–35°S) and temperate (Denmark, 55–57°N) shallow lakes. The food-web length was on average one trophic position shorter in the subtropical shallow lakes compared with their temperate counterparts. This may reflect the fact that the large majority of subtropical fish species are omnivores (i.e., feed on more than one trophic level) and have a strong degree of feeding niche overlap. The shapes of the food webs of the subtropical lakes (truncated and trapezoidal) suggest that they are fuelled by a combination of different energy pathways. In contrast, temperate lake food webs tended to be more triangular, likely as a result of more simple pathways with a top predator integrating different carbon sources. The effects of such differences on ecosystem functioning and stability, and the connection with ambient temperature as a major underlying factor, are, however, still incipiently known.

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References

  • Arim, M., F. Bozinovic & P. A. Marquet, 2007a. On the relationship between trophic position, body mass and temperature: reformulating the energy limitation hypothesis. Oikos 116: 1524–1530.

    Article  Google Scholar 

  • Arim, M., P. A. Marquet & F. M. Jaksic, 2007b. On the relationship between productivity and food chain length at different ecological levels. The American Naturalist 169: 62–72.

    Article  PubMed  Google Scholar 

  • Beisner, B. E., E. McCauley & F. J. Wrona, 1997. The influence of temperature and food chain length on plankton predator prey dynamics. Canadian Journal of Fisheries and Aquatic Sciences 54: 586–595.

    Google Scholar 

  • Brown, J. H., J. F. Gillooly, A. P. Allen, V. M. Savage & G. B. West, 2004. Toward a metabolic theory of ecology. Ecology 85: 1771–1789.

    Article  Google Scholar 

  • Bunn, S. E., C. Leigh & T. D. Jardine, 2013. Diet-tissue fractionation of δ 15N by consumers from streams and rivers. Limnology and Oceanography 58: 765–773.

    Article  CAS  Google Scholar 

  • Danger, M., G. Lacroix, S. Ka, D. Corbin & X. Lazzaro, 2009. Food-web structure and functioning of temperate and tropical lakes: a stoichiometric viewpoint. Annales de Limnologie-International Journal of Limnology 45: 11–21.

    Article  Google Scholar 

  • Dodson, S. I., S. E. Arnott & K. L. Cottingham, 2000. The relationship in lake communities between primary productivity and species richness. Ecology 81(10): 2662–2679.

    Article  Google Scholar 

  • Doi, H., M. J. Vander Zanden & H. Hillebrand, 2012. Shorter food chain length in ancient lakes: evidence from a global synthesis. PLoS One 7(6): e37856.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Elton, C. S., 1927. Animal Ecology. Sidgwick and Jackson, London.

    Google Scholar 

  • Emmerson, M. C., 2012. The importance of body size, abundance, and food-web structure for ecosystem functioning. In: Solan, M., Aspden, R. J., Paterson, D. M. (Eds.), Marine biodiversity and ecosystem functioning: frameworks, methodologies, and integration. Oxford University Press, Oxford, pp 85–100.

  • Fry, B., 1991. Stable isotope diagrams of freshwater food webs. Ecology 72: 2293–2297.

    Article  Google Scholar 

  • Gelós, M., F. Teixeira-de Mello, G. Goyenola, C. Iglesias, C. Fosalba, F. García-Rodríguez, J. Pacheco, S. García & M. Meerhoff, 2010. Seasonal and diel changes in fish activity and potential cascading effects in subtropical shallow lakes with different water transparency. Hydrobiologia 646: 173–185.

    Article  Google Scholar 

  • Glazier, D. S., 2012. Temperature affects food-chain length and macroinvertebrate species richness in spring ecosystems. Freshwater Science 31: 575–585.

    Article  Google Scholar 

  • González-Bergonzoni, I., M. Meerhoff, T. Davidson, F. Teixeira-de Mello, A. Baattrup-Pedersen & E. Jeppesen, 2012. Meta-analysis shows a consistent and strong latitudinal pattern in fish omnivory across ecosystems. Ecosystems 15: 492–503.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • González-Bergonzoni, I., E. Jeppesen, N. Vidal, F. Teixeira-de Mello, G. Goyenola, A. López-Rodríguez & M. Meerhoff, 2016. Potential drivers of seasonal shifts in fish omnivory in a subtropical stream. Hydrobiologia 768: 183–196.

    Article  Google Scholar 

  • Goyenola, G., C. Iglesias, N. Mazzeo & E. Jeppesen, 2011. Analysis of the reproductive strategy of Jenynsia multidentata (Cyprinodontiformes, Anablepidae) with focus on sexual differences in growth, size, and abundance. Hydrobiologia 673: 245–257.

    Article  Google Scholar 

  • Hammer, Ø., D. A. T. Harper & P. D. Ryan 2001. Past: Paleontological Statistics Software Package for Education and Data Analysis. Palaeontologia Electronica. http://www.palaeo-electronicaorg/2001_1/past/issue1_01htm. 4(1, art. 4):9 pp.

  • Heady, W. N. & J. W. Moore, 2012. Tissue turnover and stable isotope clocks to quantify resource shifts in anadromous rainbow trout. Oecologia 172(1): 21–34.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • Jardine, T. D., 2016. A top predator forages low on species-rich tropical food chains. Freshwater Science. doi:10.1086/685858.

    Google Scholar 

  • Jardine, T. D., W. L. Hadwen, S. K. Hamilton, S. Hladyz, S. M. Mitrovic, K. A. Kidd, W. Y. Tsoi, M. Spears, D. P. Westhorpe, V. M. Fry, F. Sheldon & S. E. Bunn, 2014. Understanding and overcoming baseline isotopic variability in running waters. River Research and Applications 30(2): 155–165.

    Article  Google Scholar 

  • Jepsen, D. B. & K. O. Winemiller, 2002. Structure of tropical river food webs revealed by stable isotope ratios. Oikos 96: 46–55.

    Article  Google Scholar 

  • Jeppesen, E., T. Mehner, I. Winfield, K. Kangur, J. Sarvala, D. Gerdeaux, M. Rask, H. 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. 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.

    Article  CAS  Google Scholar 

  • Jones, J. I. & S. Waldron, 2003. Combined stable isotope and gut contents analysis of food webs in plant dominated, shallow lakes. Freshwater Biology 48: 1396–1407.

    Article  Google Scholar 

  • Kruk, C., L. RodrÍGuez-Gallego, M. Meerhoff, F. Quintans, G. Lacerot, N. Mazzeo, F. Scasso, J. C. Paggi, E. T. H. M. Peeters & M. Scheffer, 2009. Determinants of biodiversity in subtropical shallow lakes (Atlantic coast, Uruguay). Freshwater Biology 54: 2628–2641.

    Article  CAS  Google Scholar 

  • Lawton, J. H., 1999. Are there general laws in ecology? Oikos 84: 177–192.

    Article  Google Scholar 

  • Layman, C. A., K. O. Winemiller, D. A. Arrington & D. B. Jepsen, 2005. Body size and trophic position in a diverse tropical food web. Ecology 86: 2530–2535.

    Article  Google Scholar 

  • Layman, C. A., D. A. Arrington, C. G. Montaña & D. M. Post, 2007. Can stable isotope ratios provide for community-wide measures of trophic structure? Ecology 88: 42–48.

    Article  PubMed  Google Scholar 

  • Lazzaro, X., M. Bouvy, R. A. Ribeiro-Filho, V. S. Oliviera, L. T. Sales, A. R. M. Vasconcelos & M. R. Mata, 2003. Do fish regulate phytoplankton in shallow eutrophic Northeast Brazilian reservoirs? Freshwater Biology 48: 649–668.

    Article  Google Scholar 

  • Lazzaro, X., G. Lacroix, B. Gauzens, J. Gignoux & S. Legendre, 2009. Predator foraging behaviour drives food-web topological structure. Journal of Animal Ecology 78: 1307–1317.

    Article  PubMed  Google Scholar 

  • Lindeman, R. L., 1942. The trophic-dynamic aspect of ecology. Ecology 23: 399–417.

    Article  Google Scholar 

  • Meerhoff, M., J. M. Clemente, F. Teixeira-de Mello, C. Iglesias, A. R. Pedersen & E. Jeppesen, 2007. Can warm climate-related structure of littoral predator assemblies weaken the clear water state in shallow lakes? Global Change Biology 13: 1888–1897.

    Article  Google Scholar 

  • Pacheco, J., C. Iglesias, M. Meerhoff, C. Fosalba, G. Goyenola, F. Teixeira-de Mello, S. García, M. Gelós & F. García-Rodríguez, 2010. Phytoplankton community structure in five subtropical shallow lakes with different trophic status (Uruguay): a morphology-based approach. Hydrobiologia 646: 187–197.

    Article  CAS  Google Scholar 

  • Persson, L., 1986. Temperature-induced shift in foraging ability in two fish species, roach (Rutilus rutilus) and perch (Perca fluviatilis): implications for coexistence between poikilotherms. Journal of Animal Ecology 55(3): 829–839.

    Article  Google Scholar 

  • Petchey, O. L., P. T. McPhearson, T. M. Casey & P. J. Morin, 1999. Environmental warming alters food-web structure and ecosystem function. Nature 402: 69–72.

    Article  CAS  Google Scholar 

  • Pimm, S. L., 1991. The Balance of Nature?: Ecological Issues in the Conservation of Species and Communities. University of Chicago Press, Chicago.

    Google Scholar 

  • Polis, G. A. & D. R. Strong, 1996. Food web complexity and community dynamics. American Naturalist 147: 813–846.

    Article  Google Scholar 

  • Post, D. M., 2002a. The long and short of food-chain length. Trends in Ecology and Evolution 17: 269–277.

    Article  Google Scholar 

  • Post, D. M., 2002b. Using stable isotopes to estimate trophic position: models, methods, and assumptions. Ecology 83: 703–718.

    Article  Google Scholar 

  • Post, D. & G. Takimoto, 2007. Proximate structural mechanisms for variation in food-chain length. Oikos 116(5): 775–782.

    Article  Google Scholar 

  • Post, D. M., M. L. Pace & N. G. Hairston, 2000. Ecosystem size determines food-chain length in lakes. Nature 405: 1047–1049.

    Article  CAS  PubMed  Google Scholar 

  • Rosenzweig, M. L., 1995. Species Diversity in Space and Time. Cambridge University Press, Cambridge.

    Book  Google Scholar 

  • Takimoto, G., D. Post, D. Spiller & R. Holt, 2012. Effects of productivity, disturbance, and ecosystem size on food-chain length: insights from a metacommunity model of intraguild predation. Ecological Research 27: 481–493.

    Article  Google Scholar 

  • Teixeira-de Mello, F., M. Meerhoff, Z. Pekcan-Hekim & E. Jeppesen, 2009. Substantial differences in littoral fish community structure and dynamics in subtropical and temperate shallow lakes. Freshwater Biology 54: 1202–1215.

    Article  CAS  Google Scholar 

  • Vadeboncoeur, Y., E. Jeppesen, M. J. Vander Zanden, H. H. Schierup, K. Christoffersen & D. M. Lodge, 2003. From Greenland to green lakes: cultural eutrophication and the loss of benthic pathways in lakes. Limnology and Oceanography 48: 1408–1418.

    Article  Google Scholar 

  • Vadeboncoeur, Y., K. McCann, M. Zanden & J. Rasmussen, 2005. Effects of multi-chain omnivory on the strength of trophic control in lakes. Ecosystems 8: 682–693.

    Article  Google Scholar 

  • Vander Zanden, M. J. & Y. Vadeboncoeur, 2002. Fishes as integrators of benthic and pelagic food webs in lakes. Ecology 83: 2152–2161.

    Article  Google Scholar 

  • Vander Zanden, M. J. & W. W. Fetzer, 2007. Global patterns of aquatic food chain length. Oikos 116: 1378–1388.

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Vanderklift, M. A. & S. Ponsard, 2003. Sources of variation in consumer-diet 15N enrichment: a meta-analysis. Oecologia 136: 169–182.

    Article  PubMed  Google Scholar 

  • Watson, L. C., D. J. Stewart & M. A. Teece, 2013. Trophic ecology of Arapaima in Guyana: giant omnivores in Neotropical floodplains. Neotropical Ichthyology 11: 341–349.

    Article  Google Scholar 

  • Woodward, G., 2009. Biodiversity, ecosystem functioning and food webs in fresh waters: assembling the jigsaw puzzle. Freshwater Biology 54: 2171–2187.

    Article  Google Scholar 

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Acknowledgments

We are grateful to Anne Mette Poulsen for manuscript editing and to Tinna Christensen for improving the figures. We also thank Frank Landkildehus, Kirsten Landkildehus Thomsen, and Mette E. Bramm in Denmark; and Juan M. Clemente, Claudia Fosalba, Soledad García, Nicolas Vidal, Natalia Barberán, Malvina Masdeu, Mariana Vianna, and Alejandra Kroger in Uruguay, for valuable field assistance. The project was supported by the Ministry of Science, Technology and Innovation of Denmark. EU-WISER and EU-REFRESH, “CLEAR” (a Villum Kann Rasmussen Centre of Excellence project), CRES, CIRCE, and The Research Council for Nature and Universe (272-08-0406 and FNU 16-7745) supported EJ. CI was supported by a PhD Scholarship from Aarhus University-Danish Research Agency. NM was supported by Maestría en Ciencias Ambientales, and NM, MM, and CI were supported by PEDECIBA. NM, MM, FTM, and CI were supported by SNI (ANII) and MM also by ANII-FCE 2009-2749 and the L´Oréal-UNESCO (supported by DICYT) for Women in Science national award. We deeply acknowledge the constructive comments of two anonymous reviewers and the handling editor Katya Kovalenko.

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Authors and Affiliations

  1. Grupo de Ecología y Rehabilitación de Sistemas Acuáticos, Departamento de Ecología Teórica y Aplicada, Centro Universitario de la Región Este-Facultad de Ciencias, Universidad de la República, Tacuarembó s/n CP 20000, Maldonado, Uruguay

    Carlos Iglesias, Mariana Meerhoff, Ivan González-Bergonzoni, Néstor Mazzeo, Juan Pablo Pacheco, Franco Teixeira-de Mello & Guillermo Goyenola

  2. Department of Bioscience, Aarhus University, Vejlsøvej 25, 8600, Silkeborg, Denmark

    Carlos Iglesias, Mariana Meerhoff, Liselotte S. Johansson, Ivan González-Bergonzoni, Torben L. Lauridsen, Martin Søndergaard, Thomas A. Davidson & Erik Jeppesen

  3. Departamento de Ecología y Evolución, Facultad de Ciencias Universidad de la República, Montevideo, Uruguay

    Ivan González-Bergonzoni

  4. Arctic Research Centre, Aarhus University, Building 1110, C. F. Møllers Alle 8, 8000, Aarhus, Denmark

    Torben L. Lauridsen, Thomas A. Davidson & Erik Jeppesen

  5. Sino-Danish Education and Research Centre, Beijing, China

    Torben L. Lauridsen, Martin Søndergaard & Erik Jeppesen

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  1. Carlos Iglesias
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Correspondence to Carlos Iglesias.

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Handling editor: Katya E. Kovalenko

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Iglesias, C., Meerhoff, M., Johansson, L.S. et al. Stable isotope analysis confirms substantial differences between subtropical and temperate shallow lake food webs. Hydrobiologia 784, 111–123 (2017). https://doi.org/10.1007/s10750-016-2861-0

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