, Volume 646, Issue 1, pp 327–336 | Cite as

Stable isotope variation of a highly heterogeneous shallow freshwater system

  • Luis Zambrano
  • Elsa Valiente
  • M. Jake Vander Zanden


Food web structure is well known to vary widely among ecosystems. Recent research indicates that there can be a high degree of spatial heterogeneity within ecosystems as well. Xochimilco is a small heterogeneous freshwater system that has been transformed into a network of canals, small lakes, and wetlands. Located within Mexico City, this ecosystem has been intensively managed and highly impacted for more than 50 years. This system receives urban and agricultural runoff, with resulting impacts on water quality. The aquatic community is dominated by exotics such as carp (Cyprinus carpio) and tilapia (Oreocrhomis niloticus), though the system still supports endemic species such as the aquatic salamander, axolotl (Ambystoma mexicanum), and crayfish (Cambarellus montezumae), which are both endangered. In this study, we used carbon and nitrogen stable isotopes for the whole food web and gut content analysis from the exotic fishes to describe food web structure in different canals within Xochimilco. There were significant isotopic differences among canals. These differences may result from isotopic baseline differences as well as differences in actual food web structure: both are related to local spatial variation in water quality driven by nutrient inputs and exotic fishes. Within-ecosystem variability is likely to be seen in other perturbed shallow systems as well, and should be explicitly considered in future food web studies.


Exotic fish Carp Isotopes Tilapia Urban lake Xochimilco 



Thanks to Roberto Altamirano for the help during sampling and Victoria Contreras for the map and her suggestions to the manuscript. Thanks to anonymous referees whose suggestions increased the quality of this manuscript. Part of this study was supported by Canadian Association of Zoos and Aquarium (CAZA), Darwin Initiative Indesol, CONABIO, and el Posgrado en Ciencias Biológicas.


  1. Abrantes, K. & M. Sheaves, 2008. Incorporation of terrestrial wetland material into aquatic food webs in a tropical estuarine wetland. Estuarine Coastal and Shelf Science 80: 401–412.CrossRefGoogle Scholar
  2. Alvarez, F. & R. Rangel, 2007. Population study of the crayfish Cambarellus montezumae (Crustacea: Decapoda: Cambaridae) in Xochimilco, Mexico. Revista Mexicana de Biodiversidad 78: 431–437.Google Scholar
  3. Amundsen, P. A., H. M. Gabler & F. J. Staldvik, 1996. A new approach to graphical analysis of feeding strategy from stomach contents data-modification of the Costello method. Journal of Fish Biology 48: 607–614.Google Scholar
  4. APHA, A. P. H. A., American Water Works Association, Water Environment Federation 1998. Standard Methods for the Examination of Water and Wastewater, Washington, DC.Google Scholar
  5. Bucci, J. P., W. J. Showers, S. Rebach, D. DeMaster & B. Genna, 2007. Stable isotope analyses (delta N-15 and delta C-13) of the trophic relationships of Callinectes sapidus in two North Carolina estuaries. Estuaries and Coasts 30: 1049–1059.Google Scholar
  6. Campbell, L. M., S. B. Wandera, R. J. Thacker, D. G. Dixon & R. E. Hecky, 2005. Trophic niche segregation in the Nilotic ichthyofauna of Lake Albert (Uganda, Africa). Environmental Biology of Fishes 74: 247–260.CrossRefGoogle Scholar
  7. Cifuentes, L. A., R. B. Coffin, L. Solorzano, W. Cardenas, J. Espinoza & R. R. Twilley, 1996. Isotopic and elemental variations of carbon and nitrogen in a mangrove estuary. Estuarine Coastal and Shelf Science 43: 781–800.CrossRefGoogle Scholar
  8. Contreras, R. E. A. V., E. Valiente, E. Martinez-Meyer & L. Zambrano, 2009. Recent decline and potential distribution in the last remnant area of the microendemic Mexican axolotl (Ambystoma mexicanum). Biological Conservation 142: 2881–2885.CrossRefGoogle Scholar
  9. Crossley, P. L., 2004. Sub-irrigation in wetland agriculture. Agriculture and Human Values 21: 191–205.CrossRefGoogle Scholar
  10. Douglas, M. M., S. E. Bunn & P. M. Davies, 2005. River and wetland food webs in Australia’s wet-dry tropics: general principles and implications for management. Marine and Freshwater Research 56: 329–342.CrossRefGoogle Scholar
  11. Fry, B., P. L. Mumford, F. Tam, D. D. Fox, G. L. Warren, K. E. Havens & A. D. Steinman, 1999. Trophic position and individual feeding histories of fish from Lake Okeechobee, Florida. Canadian Journal of Fisheries and Aquatic Sciences 56: 590–600.CrossRefGoogle Scholar
  12. Gu, B., 2009. Variations and controls of nitrogen stable isotopes in particulate organic matter of lakes. Oecologia 160: 421–431.CrossRefPubMedGoogle Scholar
  13. Gu, B. H., C. L. Schelske & M. V. Hoyer, 1997. Intrapopulation feeding diversity in blue tilapia: evidence from stable-isotope analyses. Ecology 78: 2263–2266.Google Scholar
  14. Hecky, R. E. & R. Hesslein, 1995. Contributions of benthic algae to lake food webs as revealed by stable isotope analysis. Journal of North American Benthological Society 14: 631–653.CrossRefGoogle Scholar
  15. Hesslein, R. H., K. A. Hallard & P. Ramlal, 1993. Replacement of sulfur, carbon, and nitrogen in tissue of growing broad whitefish (Coregonus nasus) in response to a change in diet traced by δ34S, δ13C, and δ15N. Canadian Journal of Fisheries and Aquatic Sciences 50: 2071–2076.CrossRefGoogle Scholar
  16. Jackson, D. A., P. R. Peres-Neto & J. D. Olden, 2001. What controls who is where in freshwater fish communities – the roles of biotic, abiotic and spatial factors. Canadian Journal of Fisheries and Aquatic Sciences 58: 157–170.CrossRefGoogle Scholar
  17. Jiménez, J., T. Rojas-Rabiela, S. del Amo & A. Gómez-Pompa. 1995. Conclusiones y recomendaciones del Taller In: Presente, pasado y futuro de las chinampas, Centro de Investigacions y estudios Superiores de Antroplogia social ed. México DF: 19–43.Google Scholar
  18. Kiljunen M., J. Grey, T. Sinisalo, C. Harrod, H. Immonen & R. I. Jones, 2006. A revised model for lipid-normalizing δ13C values from aquatic organisms, with implications for isotope mixing models. Journal of Applied Ecology 43: 1213–1222.CrossRefGoogle Scholar
  19. Kondoh, M., 2003. Foraging adaptation and the relationship between food-web complexity and stability. Science 299: 1388–1391.CrossRefPubMedGoogle Scholar
  20. Layman, C. A. & D. M. Post, 2008. Can stable isotope ratios provide for community-wide measures of trophic structure? Reply. Ecology 89: 2358–2359.CrossRefGoogle Scholar
  21. Layman, C. A., 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.CrossRefPubMedGoogle Scholar
  22. López, A., M. Guerrero, C. Hernández & A. Aguilar, 2006. Rehabilitación de la zona chinampera. In Carballo, C. (ed.), Xochimilco. Un proceso de gestión participativa. GDF-UNESCO, México: 201–218.Google Scholar
  23. MacAvoy, S. E., S. A. Macko & G. C. Garman, 2001. Isotopic turnover in aquatic predators: quantifying the exploitation of migratory prey. Canadian Journal of Fisheries and Aquatic Sciences 58: 923–932.CrossRefGoogle Scholar
  24. Magnuson, J. J., W. M. Tonn, A. Banerjee, J. Toivonen, O. Sanchez & M. Rask, 1998. Isolation vs. extinction in the assembly of fishes in small northern lakes. Ecology 79: 2941–2956.CrossRefGoogle Scholar
  25. March, J. G. & C. M. Pringle, 2003. Food web structure and basal resource utilization along a tropical island stream continuum, Puerto Rico. Biotropica 35: 84–93.Google Scholar
  26. Mazari-Hiriart, M., S. Ponce-de-Leon, Y. Lopez-Vidal, P. Islas-Macias, R. I. Amieva-Fernandez & F. Quinones-Falconi, 2008. Microbiological implications of periurban agriculture and water reuse in Mexico City. PLoS One 3: 2305.CrossRefGoogle Scholar
  27. Méndez, A., 2006. Rehabilitación de la zona chinampera. In Carballo, C. (ed.), Xochimilco. Un proceso de gestión participativa. GDF-UNESCO, México: 219–221.Google Scholar
  28. Mercado-Silva, N., M. R. Helmus, & M. J. Vander Zanden, 2009. The effects of impoundment and invasive species on a river food web in Mexico’s central plateau. River Research and Applications 25: 1090–1108.CrossRefGoogle Scholar
  29. Moore, J. C., 2004. Detritus, trophic dynamics and biodiversity. Ecology Letters 7: 584–600.CrossRefGoogle Scholar
  30. Ogutuohwayo, R. & R. E. Hecky, 1991. Fish Introductions in Africa and Some of Their Implications. Canadian Journal of Fisheries and Aquatic Sciences. 48: 8–12.Google Scholar
  31. Peterson, B. J. & B. Fry, 1987. Stable isotopes in ecosystem studies. Annual Review of Ecology and Systematics 18: 293–320.CrossRefGoogle Scholar
  32. Questad, E. J. & B. L. Foster, 2008. Coexistence through spatio-temporal heterogeneity and species sorting in grassland plant communities. Ecological Letters 11: 717–726.CrossRefGoogle Scholar
  33. Roach, K. A., K. O. Winemiller, C. A. Layman & S. C. Zeug, 2009. Consistent trophic patterns among fishes in lagoon and channel habitats of a tropical floodplain river: evidence from stable isotopes. Acta Oecologica-International Journal of Ecology 35: 513–522.CrossRefGoogle Scholar
  34. Solis, C., J. Sandoval, H. Perez-Vega & M. Mazari-Hiriart, 2006. Irrigation water quality in southern Mexico City based on bacterial and heavy metal analyses. Nuclear Instruments & Methods in Physics Research Section B-Beam Interactions with Materials and Atoms 249: 592–595.CrossRefGoogle Scholar
  35. Steffy, L. Y. & S. S. Kilham, 2004. Elevated delta N-15 in stream biota in areas with septic tank systems in an urban watershed. Ecological Applications 14: 637–641.CrossRefGoogle Scholar
  36. Stephan-Otto, E., 2005. El Parque Ecológico de Xochimilco. In UNESCO (ed.), Xochimilco, un proceso de gestión participativa. UNESCO, Puebla: 67–68.Google Scholar
  37. Thompson, R. M. & C. R. Townsend, 2005. Food-web topology varies with spatial scale in a patchy environment. Ecology 86: 1916–1925.CrossRefGoogle Scholar
  38. Tonn, W. M. & J. J. Magnuson, 1982. Patterns in the species composition and richness of fish assemblages in Northern Wisconsin Lakes. Ecology 63: 1149–1166.CrossRefGoogle Scholar
  39. Valiente, E., 2006. Efecto de las especies introducidas en Xochimilco para la rehabilitación del hábitat del ajolote (Ambystoma mexicanum). Maestria en Restauracion. Universidad Nacional Autónoma de México, Mexico.Google Scholar
  40. Vanbergen, A. J., A. D. Watt, R. Mitchell, A. M. Truscott, S. C. F. Palmer, E. Ivits, P. Eggleton, T. H. Jones & J. P. Sousa, 2007. Scale-specific correlations between habitat heterogeneity and soil fauna diversity along a landscape structure gradient. Oecologia 153: 713–725.CrossRefPubMedGoogle Scholar
  41. Vander Zanden, M. J., J. M. Casselman & J. B. Rasmussen, 1999. Stable isotope evidence for the food web consequences of species invasions in lakes. Nature 401: 464–467.CrossRefGoogle Scholar
  42. Vander Zanden, M. J., S. Chandra, S. K. Park, Y. Vadeboncoeur & C. R. Goldman, 2006a. Efficiencies of benthic and pelagic trophic pathways in a subalpine lake. Canadian Journal of Fisheries and Aquatic Sciences 63: 2608–2620.CrossRefGoogle Scholar
  43. Vander Zanden, M. J., J. D. Olden & C. Gratton, 2006b. Food-web approaches in restoration ecology. In Falk, D. A., M. A. Palmer & J. B. Zedler (eds), Foundations of restoration ecology. Island Press, Washington, DC, USA: 165–189.Google Scholar
  44. Zambrano, L., M. R. Perrow, C. D. Sayer, M. L. Tomlinson & T. A. Davidson, 2006. Relationships between fish feeding guild and trophic structure in English lowland shallow lakes subject to anthropogenic influence: implications for lake restoration. Aquatic Ecology 40: 391–405.CrossRefGoogle Scholar
  45. Zambrano, L., E. Vega, L. Herrera, E. Prado & V. Reynoso, 2007. A population matrix model and population viability analysis to predict the fate of endangered species in highly managed water systems. Animal Conservation 10: 297–303.CrossRefGoogle Scholar
  46. Zambrano, L., V. Contreras, M. Mazari-Hiriart & A. E. Zarco-Arista, 2009. Spatial heterogeneity of water quality in a highly degraded tropical freshwater ecosystem. Environmental Management 43: 249–263.CrossRefPubMedGoogle Scholar
  47. Zambrano, L., E. Valiente & M. J. Vander Zanden, 2010. Food web overlap between the native axolotl (Ambystoma mexicanum) and the exotics carp (Cyprinus carpio) and tilapia (Oreochromis niloticus). Biological Invasions. doi: 10.1007/s10530-010-9697-8.
  48. Zaret, T. M. & R. T. Paine, 1973. Species introduction in a Tropical Lake. Science 182: 449–455.CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2010

Authors and Affiliations

  • Luis Zambrano
    • 1
  • Elsa Valiente
    • 1
  • M. Jake Vander Zanden
    • 2
  1. 1.Departamento de Zoologia, Instituto de BiologiaUniversidad Nacional Autonoma de MexicoMexico DFMexico
  2. 2.Center for LimnologyUniversity of Wisconsin–MadisonMadisonUSA

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