, Volume 174, Issue 3, pp 953–965 | Cite as

Complex life cycles in a pond food web: effects of life stage structure and parasites on network properties, trophic positions and the fit of a probabilistic niche model

  • Daniel L. Preston
  • Abigail Z. Jacobs
  • Sarah A. Orlofske
  • Pieter T. J. Johnson
Community ecology - Original research


Most food webs use taxonomic or trophic species as building blocks, thereby collapsing variability in feeding linkages that occurs during the growth and development of individuals. This issue is particularly relevant to integrating parasites into food webs because parasites often undergo extreme ontogenetic niche shifts. Here, we used three versions of a freshwater pond food web with varying levels of node resolution (from taxonomic species to life stages) to examine how complex life cycles and parasites alter web properties, the perceived trophic position of organisms, and the fit of a probabilistic niche model. Consistent with prior studies, parasites increased most measures of web complexity in the taxonomic species web; however, when nodes were disaggregated into life stages, the effects of parasites on several network properties (e.g., connectance and nestedness) were reversed, due in part to the lower trophic generality of parasite life stages relative to free-living life stages. Disaggregation also reduced the trophic level of organisms with either complex or direct life cycles and was particularly useful when including predation on parasites, which can inflate trophic positions when life stages are collapsed. Contrary to predictions, disaggregation decreased network intervality and did not enhance the fit of a probabilistic niche model to the food webs with parasites. Although the most useful level of biological organization in food webs will vary with the questions of interest, our results suggest that disaggregating species-level nodes may refine our perception of how parasites and other complex life cycle organisms influence ecological networks.


Community ecology Wetland Food web model Topology Host–parasite interaction 



We thank N. Martinez for providing Network3D, M. Baragona, K. Richgels, B. Goodman and C. Boland for assistance in the field, East Bay Regional Parks for access to the field site, and N. Martinez, the Johnson Lab and two anonymous reviewers for comments on the manuscript. This research was supported by a fellowship from the David and Lucile Packard Foundation and funds from the National Science Foundation (DEB-0841758 and graduate fellowships to D. L. P. and S. A. O.), the US Air Force Office of Scientific Research and the Defense Advanced Research Projects Agency (grant FA9550-12-1-0432).

Supplementary material

442_2013_2806_MOESM1_ESM.docx (18 kb)
Supplementary material 1 (DOCX 117 kb)


  1. Amundsen P, Lafferty KD, Knudsen R, Primicerio R, Klemetsen A, Kuris AM (2009) Food web topology and parasites in the pelagic zone of a subarctic lake. J Anim Ecol 78:563–572PubMedCrossRefGoogle Scholar
  2. Bascompte J, Jordano P, Melian CJ, Olesen JM (2003) The nested assembly of plant-animal mutualistic networks. Proc Natl Acad Sci USA 100:9383–9387PubMedCrossRefGoogle Scholar
  3. Berlow EL, Neutel A-M, Cohen JE, De Ruiter PC, Ebenman B, Emmerson M, Fox JW, Jansen VAA, Jones JI, Kokkoris GD, Logofet DO, McKane AJ, Montoya JM, Petchey O (2004) Interaction strengths in food webs: issues and opportunities. J Anim Ecol 73:585–598CrossRefGoogle Scholar
  4. Chen H-W, Shao K-T, Liu CW-J, Lin W-H, Liu W-C (2011) The reduction of food web robustness by parasitism: fact and artifact. Int J Parasitol 41:627–634PubMedCrossRefGoogle Scholar
  5. Cohen JE, Briand F (1984) Trophic links of community food webs. Proc Natl Acad Sci USA 81:4105–4109PubMedCrossRefGoogle Scholar
  6. Cohen JE, Beaver RA, Cousins SH, DeAngelis DL, Goldwasser L, Heong KL, Holt RD, Kohn RJ, Lawton JH, Marinez N, O’Malley R, Page LM, Patten BC, Pimm SL, Polis GA, Rejmanek M, Schoener TW, Schoenly K, Sprules WG, Teal JM, Ulanowicz RE, Warren PH, Wilbur HM, Yodzis P (1993) Improving food webs. Ecology 74:252–258CrossRefGoogle Scholar
  7. Cohen JE, Jonsson T, Carpenter SR (2003) Ecological community description using the food web, species abundance, and body size. Proc Natl Acad Sci USA 100:1781–1786PubMedCrossRefGoogle Scholar
  8. Dunne JA (2006) The network structure of food webs. In: Pascual M, Dunne JA (eds) Ecological networks: linking structure to dynamics in food webs. Oxford University Press, New York, pp 27–86Google Scholar
  9. Dunne JA, Williams RJ, Martinez ND (2002) Food-web structure and network theory: the role of connectance and size. Proc Natl Acad Sci USA 99:12917–12922PubMedCrossRefGoogle Scholar
  10. Dunne JA, Lafferty KD, Dobson AP, Hechinger RF, Kuris AM, Martinez ND, McLaughlin JP, Mouritsen KN, Poulin R, Reise K, Stouffer DB, Thieltges DW, Williams RJ, Dieter Zander C (2013) Parasites affect food web structure primarily through increased diversity and complexity. PLOS Biol 11:e1001579PubMedCentralPubMedCrossRefGoogle Scholar
  11. Fontaine C, Guimaraes PR, Kefi S, Loeuille N, Memmott J, van der Putten WH, van Veen FJF, Thebault E (2011) The ecological and evolutionary implications of merging different types of networks. Ecol Lett 14:1170–1181PubMedCrossRefGoogle Scholar
  12. Fried B, Graczyk TK (1997) Advances in trematode biology. CRC, FloridaGoogle Scholar
  13. Guimaraes PR, Guimaraes P (2006) Improving the analyses of nestedness for large sets of matrices. Environ Model Softw 21:1512–1513CrossRefGoogle Scholar
  14. Hagberg AA, Schult DA, Swart PJ (2008) Exploring network structure, dynamics, and function using NetworkX. In: Varoquaux G, Vaught T, Millman J (eds) Proceedings of the 7th Python in Science Conference, Pasadena, pp 11–15Google Scholar
  15. Hernandez AD, Sukhdeo MVK (2008) Parasites alter the topology of a stream food web across seasons. Oecologia 156:613–624PubMedCrossRefGoogle Scholar
  16. Hudson L, Reuman D, Emerson R (2013) Cheddar: analysis and visualization of ecological communities. R package (
  17. Huxham M, Raffaelli D, Pike A (1995) Parasites and food web patterns. J Anim Ecol 64:168–176CrossRefGoogle Scholar
  18. Ings TC, Montoya JM, Bascompte J, Bluthgen N, Brown L, Dormann CF, Edwards F, Figueroa D, Jacob U, Jones JI, Lauridsen RB, Ledger ME, Lewis HM, Olesen JM, Van Veen FJF, Warren PH, Woodward G (2009) Ecological networks—beyond food webs. J Anim Ecol 78:253–269PubMedCrossRefGoogle Scholar
  19. Ives AR, Carpenter SR (2007) Stability and diversity of ecosystems. Science 317:58–62PubMedCrossRefGoogle Scholar
  20. Johnson PTJ, Dobson A, Lafferty KD, Marcogliese DJ, Memmott J, Orlofske SA, Poulin R, Thieltges DW (2010) When parasites become prey: ecological and epidemiological significance of eating parasites. Trends Ecol Evol 25:362–371PubMedCrossRefGoogle Scholar
  21. Lafferty KD (2012) Biodiversity loss decreases parasite diversity: theory and patterns. Philos Trans R Soc B 367:2814–2827CrossRefGoogle Scholar
  22. Lafferty KD, Kuris AM (2009) Parasites reduce food web robustness because they are sensitive to secondary extinctions as illustrated by an invasive estuarine snail. Philos Trans R Soc B 364:1659–1663CrossRefGoogle Scholar
  23. Lafferty KD, Dobson AP, Kuris AM (2006) Parasites dominate food web links. Proc Natl Acad Sci USA 103:11211–11216PubMedCrossRefGoogle Scholar
  24. Lafferty KD, Allesina S, Arim M, Briggs CJ, De Leo G, Dobson AP, Dunne JA, Johnson PTJ, Kuris AM, Marcogliese DJ, Martinez ND, Memmott J, Marquet PA, McLaughlin JP, Mordacai EA, Pascual M, Poulin R, Thieltges DW (2008) Parasites in food webs: the ultimate missing links. Ecol Lett 11:533–546PubMedCentralPubMedCrossRefGoogle Scholar
  25. Lima DP, Giacomini HC, Takemoto RM, Agostino AA, Bini LM (2012) Patterns of interactions of a large fish-parasite network in a tropical floodplain. J Anim Ecol 81:905–913PubMedCrossRefGoogle Scholar
  26. Lunde KB, Resh VH (2012) Development and validation of a macroinvertebrate index of biotic integrity (IBI) for assessing urban impacts to Northern California freshwater wetlands. Environ Monit Assess 184:3653–3674PubMedCrossRefGoogle Scholar
  27. Martinez ND (1991) Artifacts or attributes? Effects of resolution on the Little Rock Lake food web. Ecol Monogr 61:367–392CrossRefGoogle Scholar
  28. Martinez ND (1993) Effects of scale on food web structure. Science 260:242–243PubMedCrossRefGoogle Scholar
  29. Martinez ND (1994) Scale-dependent constraints on food web structure. Am Nat 144:935–953CrossRefGoogle Scholar
  30. May RM (1973) Stability and complexity in model ecosystems. Princeton University Press, New JerseyGoogle Scholar
  31. McCann K, Hastings A, Huxel GR (1998) Weak trophic interactions and the balance of nature. Nature 395:794–798CrossRefGoogle Scholar
  32. Orlofske SA, Jadin RC, Preston DL, Johnson PTJ (2012) Parasite transmission in complex communities: predators and alternative hosts alter pathogenic infections in amphibians. Ecology 93:1247–1253PubMedCrossRefGoogle Scholar
  33. Paine RT (1988) Food webs: road maps of interactions or grist for theoretical development? Ecology 69:1648–1654CrossRefGoogle Scholar
  34. Pimm SL, Rice JS (1987) The dynamics of multispecies, multi-stage models of aquatic food webs. Theor Popul Biol 32:303–325CrossRefGoogle Scholar
  35. Polis GA (1991) Complex desert food webs: an empirical critique of food-web theory. Am Nat 138:123–155CrossRefGoogle Scholar
  36. Preston DL, Orlofske SA, McLaughlin JP, Johnson PTJ (2012) Food web including infectious agents for a California freshwater pond. Ecology 93:1760 CrossRefGoogle Scholar
  37. Preston DL, Orlofske SA, Lambden JP, Johnson PTJ (2013) Biomass and productivity of trematode parasites in pond ecosystems. J Anim Ecol 82:509–517PubMedCrossRefGoogle Scholar
  38. Rooney N, McCann KS (2012) Integrating food web diversity, structure and stability. Trends Ecol Evol 27:40–46PubMedCrossRefGoogle Scholar
  39. Rudolf VHW (2008) Impact of cannibalism on predator prey dynamics: size-structured interactions and apparent mutualism. Ecology 89:1650–1660PubMedCrossRefGoogle Scholar
  40. Rudolf VHW, Lafferty KD (2011) Stage structure alters how complexity affects stability of ecological networks. Ecol Lett 14:75–79PubMedCrossRefGoogle Scholar
  41. Schoener TW (1989) Food webs from the small to the large. Ecology 70:1559–1589CrossRefGoogle Scholar
  42. Skerratt LF, Berger L, Speare R, Cashins S, McDonald KR, Phillott AD, Hines HB, Kenyon N (2007) Spread of chytridiomycosis has caused the rapid global decline and extinction of frogs. Eco Health 4:125–134Google Scholar
  43. Stouffer DB, Camacho J, Amaral LAN (2006) A robust measure of food web intervality. Proc Natl Acad Sci USA 103:10915–19020CrossRefGoogle Scholar
  44. Thebault E, Fontaine C (2010) Stability of ecological communities and the architecture of mutualistic and trophic networks. Science 329:853–856PubMedCrossRefGoogle Scholar
  45. Thieltges DW, Amundsen P-A, Hechinger RF, Johnson PTJ, Lafferty KD, Mouritsen KN, Preston DL, Reise K, Dieter Zander C, Poulin R (2013) Parasites as prey in aquatic food webs: implications for predator infection and parasite transmission. Oikos 122:1473–1482Google Scholar
  46. Thompson RM, Townsend CR (2000) Is resolution the solution? The effects of taxonomic resolution on the calculated properties of three stream food webs. Fresh Biol 44:413–422CrossRefGoogle Scholar
  47. Thompson RM, Mouritsen KN, Poulin R (2005) Importance of parasites and their life cycle characteristics in determining the structure of a large marine food web. J Anim Ecol 74:77–85CrossRefGoogle Scholar
  48. Thompson RM, Hemberg M, Starzomski BM, Shurin JB (2007) Trophic levels and trophic tangles: the prevalence of omnivory in real food webs. Ecology 88:612–617PubMedCrossRefGoogle Scholar
  49. Tylianakis JM, Didham RK, Bascompte J, Wardle DA (2008) Global change and species interactions in terrestrial ecosystems. Ecol Lett 11:1351–1363PubMedCrossRefGoogle Scholar
  50. Ulrich W, Almeida-Neto M, Gotelli NJ (2009) A consumer’s guide to nestedness analysis. Oikos 118:3–17CrossRefGoogle Scholar
  51. Van Veen FJF, Muller CB, Pell JK, Godfray HCJ (2008) Food web structure of three guilds of natural enemies: predators, parasitoids and pathogens of aphids. J Anim Ecol 77:191–200CrossRefGoogle Scholar
  52. Werner EE, Gilliam JF (1984) The ontogenetic niche and species interactions in size-structured populations. Annu Rev Ecol Syst 15:393–425CrossRefGoogle Scholar
  53. Wilbur HM (1980) Complex life cycles. Annu Rev Ecol Syst 11:67–93CrossRefGoogle Scholar
  54. Williams RJ, Martinez ND (2000) Simple rules yield complex food webs. Nature 404:180–183PubMedCrossRefGoogle Scholar
  55. Williams RJ, Martinez ND (2004) Limits to trophic levels and omnivory in complex food webs: theory and data. Am Nat 163:458–468PubMedCrossRefGoogle Scholar
  56. Williams RJ, Purves D (2011) The probabilistic niche model reveals substantial variation in the niche structure of empirical food webs. Ecology 92:1849–1857PubMedCrossRefGoogle Scholar
  57. Williams RJ, Anandanadesan A, Purves D (2010) The probabilistic niche model reveals the niche structure and role of body size in a complex food web. PLoS One 5:e12092PubMedCentralPubMedCrossRefGoogle Scholar
  58. Winemiller KO (1989) Must connectance decrease with species richness? Am Nat 134:960–968CrossRefGoogle Scholar
  59. Woodward G (2007) Body size and predatory interactions in freshwaters: scaling from individuals to communities. In: Hildrew AG, Raffaelli D (eds) Body size: the structure and function of aquatic ecosystems. Cambridge University Press, CambridgeGoogle Scholar
  60. Yoon I, Williams RJ, Levine E, Yoon S, Dunne JA, Martinez ND (2004) Webs on the web (WOW): 3D visualization of ecological networks on the WWW for collaborative research and education. Proc IS&T/SPIE Symp 5295:124–132Google Scholar
  61. Zook AE, Eklof A, Ute J, Allesina S (2011) Food webs: ordering species according to body size yields high degree of intervality. J Theor Biol 271:106–113CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • Daniel L. Preston
    • 1
  • Abigail Z. Jacobs
    • 2
  • Sarah A. Orlofske
    • 3
  • Pieter T. J. Johnson
    • 1
  1. 1.Department of Ecology and Evolutionary BiologyUniversity of ColoradoBoulderUSA
  2. 2.Department of Computer ScienceUniversity of ColoradoBoulderUSA
  3. 3.Department of BiologyNortheastern Illinois UniversityChicagoUSA

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