, Volume 186, Issue 2, pp 517–528 | Cite as

Fire and grazing modulate the structure and resistance of plant–floral visitor networks in a tallgrass prairie

  • Ellen A. R. WeltiEmail author
  • Anthony Joern
Community ecology – original research


Significant loss of pollinator taxa and their interactions with flowering plants has resulted in growing reductions to pollination services globally. Ecological network analysis is a useful tool for evaluating factors that alter the interaction structure and resistance of systems to species loss, but is rarely applied across multiple empirical networks sampled within the same study. The non-random arrangement of species interactions within a community, or “network structure” such as nested or modular organization, is predicted to prevent extinction cascades in ecological networks. How ecological gradients such as disturbance regimes shape network structural properties remains poorly understood despite significant efforts to quantify interaction structure in natural systems. Here, we examine changes in the structure of plant–floral visitor networks in a tallgrass prairie using a decadal and landscape-scale experiment that manipulates prescribed burn frequency and ungulate grazing, resulting in different grassland states. Plant and floral visitor communities and accompanying network structure were impacted by grassland fire and grazing regimes. The presence of grazers increased flowering plant species richness, network floral visitor species richness, and decreased network nestedness. Fire frequency affected flowering plant and floral visitor community composition; community composition impacted network specialization and modularity. Grassland state resulting from fire-grazing interactions has important implications for the resistance of flowering plant and floral visitor communities to species loss.


Pollinators Interactions Ecological networks Community ecology Disturbance 



We thank Jan Metlevski for identification of Lepidoptera and Chyna Pei for identification of Apoidea. We are grateful to Savannah Putnam, Kelsey Girvin and Vera Smirnova for their assistance with fieldwork. Keith Gido, John Blair and Gregory Zolnerowich provided insightful comments that greatly improved the quality of this manuscript. Grants from National Science Foundation (NSF) Division of Experimental Biology, NSF Research Experience for Undergraduates, NSF Long Term Ecological Research and Konza Prairie Biological Station supported this research.

Author contribution statement

EARW and AJ formulated the idea. EARW conducted the fieldwork, insect sorting, analyzed data and drafted the manuscript. AJ provided conceptual advice and edited the manuscript.

Supplementary material

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  1. Archibald S, Bond WJ, Stock WD, Fairbanks DHK (2005) Shaping the landscape: fire-grazer interactions in an African savanna. Ecol Appl 15:96–109. CrossRefGoogle Scholar
  2. Bartoń K (2016) Package ‘MuMIn’. Model selection and model averaging based on information criteria (AICc and alike). R package version 3.2.4Google Scholar
  3. Bascompte J (2010) Structure and dynamics of ecological networks. Science 329(5993):765–766. CrossRefPubMedGoogle Scholar
  4. 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. CrossRefPubMedPubMedCentralGoogle Scholar
  5. Bastolla U, Fortuna MA, Pascual-García A, Ferrera A, Luque B, Bascompte J (2009) The architecture of mutualistic networks minimizes competition and increases biodiversity. Nature 458:1018–1020. CrossRefPubMedGoogle Scholar
  6. Baum KA, Wallen KE (2011) Potential bias in pan trapping as a function of floral abundance. J Kans Entomol Soc 84:144–159. CrossRefGoogle Scholar
  7. Bersier L, Banašek-Richter C, Cattin M (2002) Quantitative descriptors of food-web matrices. Ecology 83:2394–2407.[2394:QDOFWM]2.0.CO;2 CrossRefGoogle Scholar
  8. Blüthgen N, Klein AM (2011) Functional complementarity and specialisation: the role of biodiversity in plant-pollinator interactions. Basic Appl Ecol 12:282–291. CrossRefGoogle Scholar
  9. Blüthgen N, Menzel F, Blüthgen N (2006) Measuring specialization in species interaction networks. BMC Ecol 6:9. CrossRefPubMedPubMedCentralGoogle Scholar
  10. Blüthgen N, Menzel F, Hovestadt T, Fiala B, Blüthgen N (2007) Specialization, constraints and conflicting interests in mutualistic networks. Curr Biol 17:1–6. CrossRefGoogle Scholar
  11. Blüthgen N, Fründ J, Vázquez DP, Menzel F (2008) What do interaction network metrics tell us about specialization and biological traits? Ecology 89:3387–3399. CrossRefPubMedGoogle Scholar
  12. Bond WJ, Keeley JE (2005) Fire as a global ‘herbivore’: the ecology and evolution of flammable ecosystems. Trends Ecol Evol 20:387–394. CrossRefPubMedGoogle Scholar
  13. Brown J, York A, Christie F, McCarthy M (2017) Effects of fire on pollinators and pollination. J Appl Ecol 54:313–322. CrossRefGoogle Scholar
  14. Burgos E, Ceva H, Perazzo RP, Devoto M, Medan D, Zimmermann M, María Delbue A (2007) Why nestedness in mutualistic networks? J Theor Biol 249:307–313. CrossRefPubMedGoogle Scholar
  15. Burkle LA, Marlin JC, Knight TM (2013) Plant-pollinator interactions over 120 years: loss of species, co-occurrence and function. Science 339:1611–1615. CrossRefPubMedGoogle Scholar
  16. Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information-theoretical approach. Springer, New YorkGoogle Scholar
  17. Collins SL, Calabrese LB (2012) Effects of fire, grazing and topographic variation on vegetation structure in tallgrass prairie. J Veg Sci 23:563–575. CrossRefGoogle Scholar
  18. Collins SL, Smith MD (2006) Scale-dependent interaction of fire and grazing on community heterogeneity in tallgrass prairie. Ecology 87:2058–2067.[2058:SIOFAG]2.0.CO;2 CrossRefPubMedGoogle Scholar
  19. Connell JH (1978) Diversity in tropical rain forests and coral reefs. Science 199:1302–1310. CrossRefPubMedGoogle Scholar
  20. Connell JH, Sousa WP (1983) On the evidence needed to judge ecological stability or persistence. Am Nat 121:789–824. CrossRefGoogle Scholar
  21. Dalsgaard B, Trøjelsgaard K, Martín-González AM, Nogués-Bravo D, Ollerton J, Petanidou T, Sandel B, Schleuning M, Wang Z, Rahbek C, Sutherland WJ, Svenning J, Olesen JM (2013) Historical climate-change influences modularity and nestedness of pollination networks. Ecography 36:001–010. CrossRefGoogle Scholar
  22. Devoto M, Bailey S, Craze P, Memmott J (2012) Understanding and planning ecological restoration of plant-pollinator networks. Ecol Lett 15:319–328. CrossRefPubMedGoogle Scholar
  23. Dormann CF, Gruber B, Fründ J (2008) Introducing the bipartite package: analysing ecological networks. R News 8:8–11Google Scholar
  24. Dormann CF, Fründ J, Blüthgen N, Gruber B (2009) Indices, graphs and null models: analyzing bipartite ecological networks. Open Ecol J 2:7–24. CrossRefGoogle Scholar
  25. Dupont YL, Olesen JM (2012) Stability of modular structure in temporal cumulative plant-flower-visitor networks. Ecol Complexity 11:89–90. CrossRefGoogle Scholar
  26. Ebeling A, Klein A, Schumacher J, Weisser WW, Tscharntke T (2008) How does plant richness affect pollinator richness and temporal stability of flower visits? Oikos 117:1808–1815. CrossRefGoogle Scholar
  27. Fantinato E, Del Vecchio S, Slaviero A, Acosta ATR, Buffa G (2016) Does flowering synchrony contribute to the sustainment of dry grassland biodiversity? Flora Morphol Distrib Funct Ecol Plants 222:96–103. CrossRefGoogle Scholar
  28. Fortuna MA, Bascompte J (2006) Habitat loss and the structure of plant-animal mutualistic networks. Ecol Lett 9:281–286. CrossRefPubMedGoogle Scholar
  29. Fuhlendorf SD, Engle DM (2004) Application of the fire-grazing interaction to restore a shifting mosaic on tallgrass prairie. J Appl Ecol 41:604–624. CrossRefGoogle Scholar
  30. Ghazoul J (2006) Floral diversity and the facilitation of pollination. J Ecol 94:295–304. CrossRefGoogle Scholar
  31. Gross J (2003) Variance inflation factors. R News 3:13–15 ISSN 1609-3631Google Scholar
  32. Grundel R, Frohnapple KJ, Jean RP, Pavlovic NB (2011) Effectiveness of bowl trapping and netting for inventory of a bee community. Environ Entomol 40:374–380. CrossRefGoogle Scholar
  33. Hoekstra JM, Boucher TM, Ricketts TH, Roberts C (2005) Confronting a biome crisis: global disparities of habitat loss and protection. Ecol Lett 8:23–29. CrossRefGoogle Scholar
  34. Huston MA (1994) Biological diversity: the coexistence of species on changing landscapes. Cambridge University Press, Cambridge, pp 215–231Google Scholar
  35. Ives AR, Carpenter SR (2007) Stability and diversity of ecosystems. Science 317:58–62. CrossRefPubMedGoogle Scholar
  36. Jakobsson A, Ågren J (2014) Distance to semi-natural grassland influences seed production of insect-pollinated herbs. Oecologia 175:199–208. CrossRefPubMedGoogle Scholar
  37. Joppa L, Montoya J, Sole R, Sanderson J, Pimm S (2010) On nestedness in ecological networks. Evol Ecol 12:35–46. Google Scholar
  38. Lázaro A, Tscheulin T, Devalez J, Nakas G, Stefanaki A, Hanlidou E, Petanidou T (2016) Moderation is best: effects of grazing intensity on plant-flower networks in Mediterranean communities. Ecol Appl 26:796–807. CrossRefPubMedGoogle Scholar
  39. Legendre P, Anderson MJ (1999) Distance-based redundancy analysis: testing multispecies responses in multifactorial ecological experiments. Ecol Monogr 69:1–24.[0001:DBRATM]2.0.CO;2 CrossRefGoogle Scholar
  40. Memmott J, Waser N, Price M (2004) Tolerance of pollination networks to species extinctions. Proc Biol Sci 271:2605–2611. CrossRefPubMedPubMedCentralGoogle Scholar
  41. Moranz RA, Debinski DM, McGranahan DA, Engle DM, Miller JR (2012) Untangling the effects of fire, grazing, and land-use legacies on grassland butterfly communities. Biodivers Conserv 21:2719–2746CrossRefGoogle Scholar
  42. Newman MEJ (2004) Analysis of weighted networks. Phys Rev E 70:056131. CrossRefGoogle Scholar
  43. Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, O’Hara RB, Simpson GL, Solymos P, Stevens MHH, Wagner H (2015) Vegan: community ecology package. R package version 2.2-1.
  44. Olesen JM, Jordano P (2002) Geographic patterns in plant-pollinator mutualistic networks. Ecology 83:2416–2424. Google Scholar
  45. Olesen JM, Bascompte J, Dupont YL, Jordano P (2007) The modularity of pollination networks. Proc Natl Acad Sci USA 104:19891–19896. CrossRefPubMedPubMedCentralGoogle Scholar
  46. Oliver I, Beattie AJ (1996) Invertebrate morphospecies as surrogates for species: a case study. Conserv Biol 10:99–109. CrossRefGoogle Scholar
  47. Ollerton J, Winfree R, Tarrant S (2011) How many flowering plants are pollinated by animals? Oikos 120:321–326. CrossRefGoogle Scholar
  48. Pickett STA, White PS (eds) (1985) The ecology of natural disturbance and patch dynamics. Academic Press, OrlandoGoogle Scholar
  49. Pocock MJO, Evans DM, Memmott J (2012) The robustness and restorations of a network of ecological networks. Science 335:973–977. CrossRefPubMedGoogle Scholar
  50. Potts SG, Biesmeijer JC, Kremen C, Neumann P, Schweiger O, Kunin WE (2010) Global pollinator declines: trends, impacts and drivers. Trends Ecol Evol 25:345–353. CrossRefPubMedGoogle Scholar
  51. R Development Core Team (2016) R: a language and environment for statistical computing R Foundation for Statistical Computing, Vienna. ISBN 3-900051-07-0.
  52. Rezende E, Albert E, Fortuna M, Bascompte J (2009) Compartments in a marine food web associated with phylogeny, body mass, and habitat structure. Ecol Lett 12:779–788. CrossRefPubMedGoogle Scholar
  53. Rodríguez-Girónes MA, Santamaría L (2006) A new algorithm to calculate the nestedness temperature of presence–absence matrices. J Biogeogr 33:924–935. CrossRefGoogle Scholar
  54. Roulston TH, Smith SA, Brewster AL (2007) A comparison of pan trap and intensive net sampling techniques for documenting a bee (Hymenoptera: Apiformes) fauna. J Kans Entomol Soc 80:179–181CrossRefGoogle Scholar
  55. Samson F, Knopf F (1994) Prairie conservation in North-America. Bioscience 44:418–421.[179:ACOPTA]2.0.CO;2 CrossRefGoogle Scholar
  56. Schleuning M, Fründ J, Klein A, Abrahamczyk S, Alarcón R, Albrecht M, Andersson GKS, Bazarian S, Böhning-Gaese K, Bommarco R, Dalsgaard B, Dehling DM, Gotlieb A, Hagen M, Hickler T, Holzschuh A, Kaiser-Bunbury CN, Kreft H, Morris RJ, Sandel B, Sutherland WJ, Svenning J, Tscharntke T, Watts S, Weiner CN, Werner M, Williams NM, Winqvist C, Dormann CF, Blüthgen N (2012) Specialization of mutualistic interaction networks decreases toward tropical latitudes. Curr Biol 22:1925–1931. CrossRefPubMedGoogle Scholar
  57. Sousa WP (1984) The role of disturbance in natural communities. Annu Rev Ecol Syst 15:353–391. CrossRefGoogle Scholar
  58. Spasojevic MJ, Aicher RJ, Koch GR, Marquardt ES, Mirotchnick N, Troxler TG, Collins SL (2010) Fire and grazing in a mesic tallgrass prairie: impacts on plant species and functional traits. Ecology 91:1651–1659. CrossRefPubMedGoogle Scholar
  59. Steuter AA, Steinauer EM, Hill GP, Bowers PA, Tieszen LL (1995) Distribution and diet of bison and pocket gophers in a sandhills prairie. Ecol Appl 5:756–766. CrossRefGoogle Scholar
  60. Swengel SR, Schlicht D, Olsen F, Swengel AB (2011) Declines of prairie butterflies in the Midwestern USA. J Insect Conserv 15:327–339. CrossRefGoogle Scholar
  61. Thébault E, Fontaine C (2010) Stability of ecological communities and the architecture of mutualistic and trophic networks. Science 329:853–856. CrossRefPubMedGoogle Scholar
  62. Vanbergen AJ, Woodcock BA, Gray A, Grant F, Telford A, Lambdon P, Chapman DS, Pywell RF, Heard MS, Cavers S (2014) Grazing alters insect visitation networks and plant mating systems. Funct Ecol 28:178–189. CrossRefGoogle Scholar
  63. Vinton MA, Hartnett DC, Finck EJ, Briggs J (1993) Interactive effects of fire, bison (Bison bison) grazing and plant community composition in tallgrass prairie. Am Midl Nat 129:10–18. CrossRefGoogle Scholar
  64. Volker G, Wissel C (1997) Babel, or the ecological stability discussions: an inventory and analysis of terminology and a guide for avoiding confusion. Oecologia 109:323–334. CrossRefGoogle Scholar
  65. Welti E, Joern A (2015) Structure of trophic and mutualistic networks across broad environmental gradients. Ecol Evol 5:326–334. CrossRefPubMedGoogle Scholar
  66. Yoshihara Y, Chimeddorj B, Buuveibaatar B, Lhagvasuren B, Takatsuki S (2008) Effects of livestock grazing on pollination on a steppe in eastern Mongolia. Biol Conserv 141:2376–2386. CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2017

Authors and Affiliations

  1. 1.Department of BiologyUniversity of OklahomaNormanUSA
  2. 2.Division of BiologyKansas State UniversityManhattanUSA

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