Biological Invasions

, Volume 21, Issue 12, pp 3505–3519 | Cite as

Experimental species introduction shapes network interactions in a plant-pollinator community

  • L. RussoEmail author
  • R. Albert
  • C. Campbell
  • K. Shea
Original Paper


Invasive species that form mutualistic interactions can perturb resident communities by creating new interactions, or weakening the strength of existing interactions via competition. We hypothesized that introducing a super-generalist plant species to bee-plant networks would lead to (1) increases in the weighted and unweighted average degree, nestedness, and connectance and (2) decreases in the modularity. We constructed visitation networks of bees to five native plant species in experimental research plots, in the presence and absence of an invasive thistle and while varying thistle abundance and time/duration of introduction. Species introduction did not change the visitation rate of bees to co-occurring native plants, or the interaction structure between the native plant species and bee visitors; seed set of a focal native plant species was also unaffected. We found the number of bee species with which the introduced species interacted (generality) correlated with significant increases in unweighted and weighted average degree, nestedness, and connectance, but not modularity. When comparing the impact of the introduced species either early or late in the season, we found similar relationships between introduced species generality and weighted and unweighted average degree and connectance; there was a significant negative relationship between introduced species generality and modularity early in the season, and a significant positive relationship with nestedness late in the season, suggesting introduction timing within a season may affect some measures differently. Overall, the native community was robust to the introduction of the super-generalist; our experimental test of network theory predictions demonstrates an improving mechanistic understanding of how mutualistic networks respond to ecological perturbations.


Disturbance timing/duration Invader abundance Management Pollination services 



We would like to thank the farmers at the Russell Larson Research Farm, especially S. Smiles and W. S. Harkcom, greenhouse manager, L.S. Burghard, field assistants D. Brough, C.J. Fisher, and K. McIlroy, S. Droege for identifications, and J. Keller for additional field assistance. KS was supported by NSF Grant #1556444 and NSF Grant #DMS-1313115. LR was supported by National Science Foundation grant #DMS-1313115 and a Marie Curie Fellowship (FOMN-705287).

Supplementary material

10530_2019_2064_MOESM1_ESM.docx (405 kb)
Supplementary material 1 (DOCX 406 kb)


  1. Aizen M, Morales C, Morales J (2008) Invasive mutualists erode native pollination webs. PLoS Biol 6:396–403. CrossRefGoogle Scholar
  2. Allen MR, Shea K (2006) Spatial segregation of congeneric invaders in central Pennsylvania, USA. Biol Invasions 8:509–521. CrossRefGoogle Scholar
  3. Almeida-Neto M, Guimaraes P, Guimaraes PR Jr, Loyola RD, Ulrich W (2008) A consistent metric for nestedness analysis in ecological systems: reconciling concept and measurement. Oikos 117:1227–1239CrossRefGoogle Scholar
  4. Bartomeus I, Vilà M, Santamaría L (2008) Contrasting effects of invasive plants in plant–pollinator networks. Oecologia 155:761–770. CrossRefGoogle Scholar
  5. Barton K (2018) MuMIn: multi-model inference. In: R Packag. version 1.42.1Google Scholar
  6. Bates D, Mächler M, Bolker B, Walker S (2014) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48Google Scholar
  7. Blüthgen N, Menzel F, Blüthgen N (2006) Measuring specialization in species interaction networks. BMC Ecol 6:9. CrossRefPubMedPubMedCentralGoogle Scholar
  8. Bond W, Lawton J, May R (1994) Do mutualisms matter? Assessing the impact of pollinator and disperser disruption on plant extinction. Philos Trans R Soc Lond Ser B Biol Sci 344:83–90. CrossRefGoogle Scholar
  9. Burkle LA, Marlin JC, Knight TM (2013) Plant-pollinator interactions over 120 years: loss of species, co-occurrence, and function. Science 339:1611–1615. CrossRefGoogle Scholar
  10. Campbell C, Yang S, Shea K, Albert R (2012) Topology of plant-pollinator networks that are vulnerable to collapse from species extinction. Phys Rev E 86(2):021924Google Scholar
  11. Campbell C, Yang S, Albert R, Shea K (2015) Plant-pollinator community network response to species invasion depends on both invader and community characteristics. Oikos 124:406–413. CrossRefGoogle Scholar
  12. Cariveau DP, Winfree R (2015) Causes of variation in wild bee responses to anthropogenic drivers. Curr Opin Insect Sci 10:104–109. CrossRefPubMedGoogle Scholar
  13. Carvalheiro LG, Biesmeijer JC, Benadi G et al (2014) The potential for indirect effects between co-flowering plants via shared pollinators depends on resource abundance, accessibility and relatedness. Ecol Lett 17:1389–1399. CrossRefPubMedGoogle Scholar
  14. Crone EE (2013) Responses of social and solitary bees to pulsed floral resources. Am Nat 182:465–473. CrossRefPubMedGoogle Scholar
  15. DeBarros N (2010) Floral resource provisioning for bees in Pennsylvania and the mid-Atlantic region, Masters Th. Pennsylvania State UniversityGoogle Scholar
  16. Desrochers AM, Bain JF, Warwick SI (1988) The biology of Canadian weeds: Carduus nutans L. and Carduus acanthoides L. Can J Plant Sci 68:1053–1068. CrossRefGoogle Scholar
  17. Dormann CF, Fründ J, Blüthgen N, Gruber B (2009) Indices, graphs and null models: analyzing bipartite ecological networks. Open Ecol J 2:7–24CrossRefGoogle Scholar
  18. Droege S, Tepedino VJ, Lebuhn G et al (2010) Spatial patterns of bee captures in North American bowl trapping surveys. Insect Conserv Divers 3:15–23. CrossRefGoogle Scholar
  19. Ehrenfeld JG (2010) Ecosystem consequences of biological invasions. Annu Rev Ecol Evol Syst 41:59–80. CrossRefGoogle Scholar
  20. Fortuna MA, Stouffer DB, Olesen JM et al (2010) Nestedness versus modularity in ecological networks: two sides of the same coin? J Anim Ecol 79:811–817. CrossRefPubMedGoogle Scholar
  21. Forup ML, Henson KSE, Craze PG, Memmott J (2007) The restoration of ecological interactions: plant-pollinator networks on ancient and restored heathlands. J Appl Ecol 45:742–752. CrossRefGoogle Scholar
  22. Hegland SJ, Nielsen A, Lázaro A et al (2009) How does climate warming affect plant-pollinator interactions? Ecol Lett 12:184–195. CrossRefPubMedGoogle Scholar
  23. Kaiser-Bunbury CN, Muff S, Memmott J et al (2010) The robustness of pollination networks to the loss of species and interactions: a quantitative approach incorporating pollinator behaviour. Ecol Lett 13:442–452. CrossRefGoogle Scholar
  24. Kaiser-Bunbury CNCN, Valentin T, Mougal J et al (2011) The tolerance of island plant-pollinator networks to alien plants. J Ecol 99:202–213. CrossRefGoogle Scholar
  25. Kiers E, Palmer T, Ives A et al (2010) Mutualisms in a changing world: an evolutionary perspective. Ecol Lett 13:1459–1474. CrossRefGoogle Scholar
  26. Lopezaraiza-Mikel M, Hayes R, Whalley M, Memmott J (2007) The impact of an alien plant on a native plant-pollinator network: an experimental approach. Ecol Lett 10:539–550CrossRefGoogle Scholar
  27. McKinney AM, Goodell K (2011) Plant–pollinator interactions between an invasive and native plant vary between sites with different flowering phenology. Plant Ecol 212:1025–1035. CrossRefGoogle Scholar
  28. Memmott J, Waser NM (2002) Integration of alien plants into a native flower–pollinator visitation web. Proc R Soc Lond B Biol Sci 269:2395–2399. CrossRefGoogle Scholar
  29. Montero-Castaño A, Vilà M (2016) Influence of the honeybee and trait similarity on the effect of a non-native plant on pollination and network rewiring. Funct Ecol 31:142–152. CrossRefGoogle Scholar
  30. Moragues E, Traveset A (2005) Effect of Carpobrotus spp. on the pollination success of native plant species of the Balearic Islands. Biol Conserv 122:611–619. CrossRefGoogle Scholar
  31. Morales C, Aizen M (2005) Invasive mutualisms and the structure of plant–pollinator interactions in the temperate forests of north-west Patagonia, Argentina. J Ecol 94:171–180CrossRefGoogle Scholar
  32. Morente-López J, Lara-Romero C, Ornosa C, Iriondo JM (2018) Phenology drives species interactions and modularity in a plant-flower visitor network. Sci Rep 8:9386. CrossRefPubMedPubMedCentralGoogle Scholar
  33. Newman MEJ, Girvan M (2004) Finding and evaluating community structure in networks. Phys Rev E 69:026113. CrossRefGoogle Scholar
  34. Russo L, Shea K (2016) Deliberately increased network connectance in a plant-pollinator community experiment. J Complex Netw. CrossRefGoogle Scholar
  35. Russo L, Memmott J, Montoya D et al (2014) Patterns of introduced species interactions affect multiple aspects of network structure in plant-pollinator communities. Ecology 95:2953–2963. CrossRefGoogle Scholar
  36. Russo L, Nichol C, Shea K (2016) Pollinator floral provisioning by a plant invader: Quantifying beneficial effects of detrimental species. Divers Distrib 22:189–198. CrossRefGoogle Scholar
  37. Russo L, Vaudo AD, Fisher CJ, Grozinger CM, Shea K (2019) Bee community preference for an invasive thistle associated with higher pollen protein content. Oecologia. CrossRefPubMedGoogle Scholar
  38. Shea K, Roxburgh SH, Rauschert ESJ (2004) Moving from pattern to process: coexistence mechanisms under intermediate disturbance regimes. Ecol Lett 7:491–508. CrossRefGoogle Scholar
  39. Skarpaas O, Shea K (2007) Dispersal patterns, dispersal mechanisms, and invasion wave speeds for invasive thistles. Am Nat 170:421–430. CrossRefPubMedGoogle Scholar
  40. Sofaer HR, Jarnevich CS, Pearse IS (2018) The relationship between invader abundance and impact. Ecosphere 9:e02415. CrossRefGoogle Scholar
  41. Stinson KA, Campbell SA, Powell JR et al (2006) Invasive plant suppresses the growth of native tree seedlings by disrupting belowground mutualisms. PLoS Biol 4:e140. CrossRefPubMedPubMedCentralGoogle Scholar
  42. Thébault E, Fontaine C (2010) Stability of ecological communities and the architecture of mutualistic and trophic networks. Science 329(5993):853–856CrossRefGoogle Scholar
  43. Tipping PW (1992) Density of Carduus and Cirsium thistles in selected areas of Maryland. Weed Technol 6:434–436. CrossRefGoogle Scholar
  44. Tylianakis JM, Laliberté E, Nielsen A, Bascompte J (2010) Conservation of species interaction networks. Biol Conserv 143:2270–2279. CrossRefGoogle Scholar
  45. Vaudo AD, Patch HM, Mortensen DA et al (2014) Bumble bees exhibit daily behavioral patterns in pollen foraging. Arthropod Plant Interact 8:273–283. CrossRefGoogle Scholar
  46. Vilà M, Bartomeus I, Dietzsch AC et al (2009) Invasive plant integration into native plant–pollinator networks across Europe. Proc R Soc B: Biol Sci 276:3887–3893. CrossRefGoogle Scholar
  47. Walsworth TE, Budy P, Thiede GP (2013) Longer food chains and crowded niche space: effects of multiple invaders on desert stream food web structure. Ecol Freshw Fish 22:439–452. CrossRefGoogle Scholar
  48. Weiner CN, Werner M, Linsenmair KE, Blüthgen N (2014) Land-use impacts on plant–pollinator networks: interaction strength and specialization predict pollinator declines. Ecology 95:466–474. CrossRefPubMedGoogle Scholar
  49. Williams NM, Regetz J, Kremen C (2012) Landscape-scale resources promote colony growth but not reproductive performance of bumble bees. Ecology 93:1049–1058. CrossRefGoogle Scholar
  50. Yang S, Ferrari MJ, Shea K (2011) Pollinator behavior mediates negative interactions between two congeneric invasive plant species. Am Nat 177:110–118. CrossRefPubMedGoogle Scholar
  51. Zhang R, Shea K (2012) Integrating multiple disturbance aspects: management of an invasive thistle, Carduus nutans. Ann Bot 110:1395–1401. CrossRefPubMedGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.Department of BiologyPennsylvania State UniversityUniversity ParkUSA
  2. 2.Department of Entomology and Plant PathologyUniversity of Tennessee Institute of AgricultureKnoxvilleUSA
  3. 3.Department of PhysicsPennsylvania State UniversityUniversity ParkUSA
  4. 4.Department of Physics and AstronomyUniversity of Mount UnionAllianceUSA

Personalised recommendations