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

Abstract

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.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

References

  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 78:563–572

    PubMed  Article  Google Scholar 

  2. Bascompte J, Jordano P, Melian CJ, Olesen JM (2003) The nested assembly of plant-animal mutualistic networks. Proc Natl Acad Sci USA 100:9383–9387

    CAS  PubMed  Article  Google 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 73:585–598

    Article  Google 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 41:627–634

    PubMed  Article  Google Scholar 

  5. Cohen JE, Briand F (1984) Trophic links of community food webs. Proc Natl Acad Sci USA 81:4105–4109

    CAS  PubMed  Article  Google 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 74:252–258

    Article  Google 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 100:1781–1786

    CAS  PubMed  Article  Google 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 27–86

    Google 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 99:12917–12922

    CAS  PubMed  Article  Google 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:e1001579

    CAS  PubMed Central  PubMed  Article  Google 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 14:1170–1181

    PubMed  Article  Google Scholar 

  12. Fried B, Graczyk TK (1997) Advances in trematode biology. CRC, Florida

    Google Scholar 

  13. Guimaraes PR, Guimaraes P (2006) Improving the analyses of nestedness for large sets of matrices. Environ Model Softw 21:1512–1513

    Article  Google 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 11–15

  15. Hernandez AD, Sukhdeo MVK (2008) Parasites alter the topology of a stream food web across seasons. Oecologia 156:613–624

    PubMed  Article  Google Scholar 

  16. Hudson L, Reuman D, Emerson R (2013) Cheddar: analysis and visualization of ecological communities. R package (http://cran.r-project.org/web/packages/cheddar/index.html)

  17. Huxham M, Raffaelli D, Pike A (1995) Parasites and food web patterns. J Anim Ecol 64:168–176

    Article  Google 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 78:253–269

    PubMed  Article  Google Scholar 

  19. Ives AR, Carpenter SR (2007) Stability and diversity of ecosystems. Science 317:58–62

    CAS  PubMed  Article  Google 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 25:362–371

    PubMed  Article  Google Scholar 

  21. Lafferty KD (2012) Biodiversity loss decreases parasite diversity: theory and patterns. Philos Trans R Soc B 367:2814–2827

    Article  Google 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 364:1659–1663

    Article  Google Scholar 

  23. Lafferty KD, Dobson AP, Kuris AM (2006) Parasites dominate food web links. Proc Natl Acad Sci USA 103:11211–11216

    CAS  PubMed  Article  Google 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 11:533–546

    PubMed Central  PubMed  Article  Google 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 81:905–913

    PubMed  Article  Google 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 184:3653–3674

    CAS  PubMed  Article  Google Scholar 

  27. Martinez ND (1991) Artifacts or attributes? Effects of resolution on the Little Rock Lake food web. Ecol Monogr 61:367–392

    Article  Google Scholar 

  28. Martinez ND (1993) Effects of scale on food web structure. Science 260:242–243

    CAS  PubMed  Article  Google Scholar 

  29. Martinez ND (1994) Scale-dependent constraints on food web structure. Am Nat 144:935–953

    Article  Google Scholar 

  30. May RM (1973) Stability and complexity in model ecosystems. Princeton University Press, New Jersey

    Google Scholar 

  31. McCann K, Hastings A, Huxel GR (1998) Weak trophic interactions and the balance of nature. Nature 395:794–798

    CAS  Article  Google 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 93:1247–1253

    PubMed  Article  Google Scholar 

  33. Paine RT (1988) Food webs: road maps of interactions or grist for theoretical development? Ecology 69:1648–1654

    Article  Google Scholar 

  34. Pimm SL, Rice JS (1987) The dynamics of multispecies, multi-stage models of aquatic food webs. Theor Popul Biol 32:303–325

    Article  Google Scholar 

  35. Polis GA (1991) Complex desert food webs: an empirical critique of food-web theory. Am Nat 138:123–155

    Article  Google Scholar 

  36. Preston DL, Orlofske SA, McLaughlin JP, Johnson PTJ (2012) Food web including infectious agents for a California freshwater pond. Ecology 93:1760

    Article  Google Scholar 

  37. Preston DL, Orlofske SA, Lambden JP, Johnson PTJ (2013) Biomass and productivity of trematode parasites in pond ecosystems. J Anim Ecol 82:509–517

    PubMed  Article  Google Scholar 

  38. Rooney N, McCann KS (2012) Integrating food web diversity, structure and stability. Trends Ecol Evol 27:40–46

    PubMed  Article  Google Scholar 

  39. Rudolf VHW (2008) Impact of cannibalism on predator prey dynamics: size-structured interactions and apparent mutualism. Ecology 89:1650–1660

    PubMed  Article  Google Scholar 

  40. Rudolf VHW, Lafferty KD (2011) Stage structure alters how complexity affects stability of ecological networks. Ecol Lett 14:75–79

    CAS  PubMed  Article  Google Scholar 

  41. Schoener TW (1989) Food webs from the small to the large. Ecology 70:1559–1589

    Article  Google 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 4:125–134

    Google Scholar 

  43. Stouffer DB, Camacho J, Amaral LAN (2006) A robust measure of food web intervality. Proc Natl Acad Sci USA 103:10915–19020

    Article  Google Scholar 

  44. Thebault E, Fontaine C (2010) Stability of ecological communities and the architecture of mutualistic and trophic networks. Science 329:853–856

    CAS  PubMed  Article  Google 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 122:1473–1482

    Google 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 44:413–422

    Article  Google 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 74:77–85

    Article  Google 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 88:612–617

    PubMed  Article  Google Scholar 

  49. Tylianakis JM, Didham RK, Bascompte J, Wardle DA (2008) Global change and species interactions in terrestrial ecosystems. Ecol Lett 11:1351–1363

    PubMed  Article  Google Scholar 

  50. Ulrich W, Almeida-Neto M, Gotelli NJ (2009) A consumer’s guide to nestedness analysis. Oikos 118:3–17

    Article  Google 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 77:191–200

    CAS  Article  Google Scholar 

  52. Werner EE, Gilliam JF (1984) The ontogenetic niche and species interactions in size-structured populations. Annu Rev Ecol Syst 15:393–425

    Article  Google Scholar 

  53. Wilbur HM (1980) Complex life cycles. Annu Rev Ecol Syst 11:67–93

    Article  Google Scholar 

  54. Williams RJ, Martinez ND (2000) Simple rules yield complex food webs. Nature 404:180–183

    CAS  PubMed  Article  Google Scholar 

  55. Williams RJ, Martinez ND (2004) Limits to trophic levels and omnivory in complex food webs: theory and data. Am Nat 163:458–468

    PubMed  Article  Google Scholar 

  56. Williams RJ, Purves D (2011) The probabilistic niche model reveals substantial variation in the niche structure of empirical food webs. Ecology 92:1849–1857

    PubMed  Article  Google 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:e12092

    PubMed Central  PubMed  Article  Google Scholar 

  58. Winemiller KO (1989) Must connectance decrease with species richness? Am Nat 134:960–968

    Article  Google 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, Cambridge

    Google 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 5295:124–132

    Google 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 271:106–113

    Article  Google Scholar 

Download references

Acknowledgments

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).

Author information

Affiliations

Authors

Corresponding author

Correspondence to Daniel L. Preston.

Additional information

Communicated by David Marcogliese.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 117 kb)

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Preston, D.L., Jacobs, A.Z., Orlofske, S.A. et al. 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. Oecologia 174, 953–965 (2014). https://doi.org/10.1007/s00442-013-2806-5

Download citation

Keywords

  • Community ecology
  • Wetland
  • Food web model
  • Topology
  • Host–parasite interaction