Species roles in plant–pollinator communities are conserved across native and alien ranges

Diversity and Distributions

Volumn 22, Issue 8, 2016, Pages 841-852

  Emer, Carine ^a,b   Memmott, Jane ^a   Vaughan, Ian P ^c   Montoya, Daniel ^a,d,e   Tylianakis, Jason M ^f,g  

^a UNIVERSITY OF BRISTOL   (United Kingdom)

^b SÃO PAULO STATE UNIVERSITY UNESP   (Brazil)

^c CARDIFF UNIVERSITY   (United Kingdom)

^d Station d'Ecologie Expérimentale du Centre National de la Recherche Scientifique   (France)

^e UNIV BOURGOGNE FRANCHE COMTÉ   (France)

^f UNIVERSITY OF CANTERBURY   (New Zealand)

^g IMPERIAL COLLEGE LONDON   (United Kingdom)

Author keywords

biological invasions; centrality; conservatism; ecological networks; pollination; predicting invasion

Indexed keywords

BIOLOGICAL INVASION; COMMUNITY ECOLOGY; ECOLOGICAL IMPACT; ECOLOGICAL MODELING; FUNCTIONAL ROLE; GLOBAL PERSPECTIVE; INTRODUCED SPECIES; NATIVE SPECIES; PLANT-POLLINATOR INTERACTION; POLLINATION; REGRESSION ANALYSIS;

EID: 84977111525     PISSN: 13669516     EISSN: 14724642     Source Type: Journal    
DOI: 10.1111/ddi.12458     Document Type: Article

References (83)

1. Aizen, M.A., Morales, C.L. & Morales, J.M. (2008) Invasive mutualists erode native pollination webs. Plos Biology, 6, 396–403.
2. Aizen, M.A., Sabatino, M. & Tylianakis, J.M. (2012) Specialization and rarity predict nonrandom loss of interactions from mutualist networks. Science, 335, 1486–1489.
3. Albrecht, M. & Gotelli, N.J. (2001) Spatial and temporal niche partitioning in grassland ants. Oecologia, 126, 134–141.
4. Albrecht, M., Padrón, B., Bartomeus, I. & Traveset, A. (2014) Consequences of plant invasions on compartmentalization and species’ roles in plant–pollinator networks. Proceedings of the Royal Society B: Biological Sciences, 281, 20140773.
5. Ashman, T.L. & Arceo-Gómez, G. (2013) Toward a predictive understanding of the fitness costs of heterospecific pollen receipt and its importance in co-flowering communities. American Journal of Botany, 100, 1061–1070.
6. Baker, N.J., Kaartinen, R., Roslin, T. & Stouffer, D.B. (2015) Species’ roles in food webs show fidelity across a highly variable oak forest. Ecography, 38, 130–139.
7. Bartomeus, I., Bosch, J. & Vila, M. (2008) High invasive pollen transfer, yet low deposition on native stigmas in a Carpobrotus-invaded community. Annals of Botany, 102, 417–424.
8. Barton, K. (2013) MuMIn: multi-model inference. R package version 1.15.1. Available at: https://cran.r-project.org/web/packages/MuMIn/index.html (accessed 15 July 2015).
9. Bascompte, J., Jordano, P., Melián, C.J. & Olesen, J.M. (2003) The nested assembly of plant-animal mutualistic networks. Proceedings of the National Academy of Sciences USA, 100, 9383–9387.
10. Bascompte, J. & Jordano, P. (2007) Plant-animal mutualistic networks: the architecture of biodiversity. Annual Review of Ecology Evolution and Systematics, 38, 567–593.
11. Bates, D., Maechler, M., Bolker, B. & Walker, S. (2014) lme4: Linear mixed-effects models using Eigen and S4. R package version 1.1-10. Available at: http://CRAN.R-project.org/package=lme4 (accessed 19 February 2016).
12. Blüthgen, N., Menzel, F., Hovestadt, T., Fiala, B. & Blüthgen, N. (2007) Specialization, constraints, and conflicting interests in mutualistic networks. Current Biology, 17, 341–346.
13. Brosi, B.J. & Briggs, H.M. (2013) Single pollinator species losses reduce floral fidelity and plant reproductive function. Proceedings of the National Academy of Sciences USA, 110, 13044–13048.
14. Carpintero, S., Reyes-Lopez, J. & De Reyna, L.A. (2005) Impact of Argentine ants (Linepithema humile) on an arboreal ant community in Doñana National Park, Spain. Biodiversity and Conservation, 14, 151–163.
15. Carvalheiro, L.G., Biesmeijer, J.C., Benadi, G. et al. (2014) The potential for indirect effects between co-flowering plants via shared pollinators depends on resource abundance, accessibility and relatedness. Ecology Letters, 17, 1389–1399.
16. Center for Invasive Species & Ecosystem HealthAvailable at: http://www.bugwood.org/ (accessed 10 July 2014).
17. Chittka, L. & Schurkens, S. (2001) Successful invasion of a floral market – an exotic Asian plant has moved in on Europe's river-banks by bribing pollinators. Nature, 411, 653.
18. Crawley, M.J. (2013) The R book, 2 edn. John Wiley & Sons Ltd, Singapore.
19. Delivering alien invasive species inventories for Europe (DAISIE)Available at: http://www.europe-aliens.org/ (accessed 10 July 2014).
20. Dorado, J., Vazquez, D.P., Stevani, E.L. & Chacoff, N.P. (2011) Rareness and specialization in plant–pollinator networks. Ecology, 92, 19–25.
21. Dormann, C.F., Jochen, F., Blüthgen, N. & Gruber, B. (2009) Indices, graphs and null models: analyzing bipartite ecological networks. The Open Ecology Journal, 2, 7–24.
22. Dostal, P., Mullerova, J., Pysek, P., Pergl, J. & Klinerova, T. (2013) The impact of an invasive plant changes over time. Ecology Letters, 16, 1277–1284.
23. Doulcier, G. & Stouffer, D. (2015) Fast network modularity and roles computation by simulated annealing. R package version 0.2.4. Available at: https://cran.r-project.org/web/packages/rnetcarto/index.html (accessed 10 December 2015).
24. Dunne, J.A., Williams, R.J. & Martinez, N.D. (2002) Food-web structure and network theory: the role of connectance and size. Proceedings of the National Academy of Sciences USA, 99, 12917–12922.
25. Efron, B. (1983) Estimating the error rate of a prediction rule – improvement on cross-validation. Journal of the American Statistical Association, 78, 316–331.
26. Eklöf, A., Jacob, U., Kopp, J., Bosch, J., Castro-Urgal, R., Chacoff, N.P., Dalsgaard, B., de Sassi, C., Galetti, M., Guimarães, P.R., Beatriz Lomascolo, S., Gonzalez, A.M.M., Pizo, M.A., Rader, R., Rodrigo, A., Tylianakis, J.M., Vazquez, D.P. & Allesina, S. (2013) The dimensionality of ecological networks. Ecology Letters, 16, 577–583.
27. Emer, C., Vaughan, I.P., Hiscock, S. & Memmott, J. (2015) The impact of the invasive alien plant, Impatiens glandulifera, on pollen transfer networks. PLoS ONE, 10, e0143532.
28. Fang, Q. & Huang, S.Q. (2013) A directed network analysis of heterospecific pollen transfer in a biodiverse community. Ecology, 94, 1176–1185.
29. Fort, H., Vazquez, D.P. & Lan, B.L. (2016) Abundance and generalisation in mutualistic networks: solving the chicken-and-egg dilemma. Ecology Letters, 19, 4–11.
30. Freeman, L.C. (1979) Centrality in social networks conceptual clarification. Social Networks, 1, 215–239.
31. Garcia, D., Martinez, D., Stouffer, D.B. & Tylianakis, J.M. (2014) Exotic birds increase generalization and compensate for native bird decline in plant-frugivore assemblages. Journal of Animal Ecology, 83, 1441–1450.
32. Gilljam, D., Curtsdotter, A. & Ebenman, B. (2015) Adaptive rewiring aggravates the effects of species loss in ecosystems. Nature Communications, 6, 10.
33. Global Invasive Species Information Network (GISIN)Available at: http://www.gisin.org (accessed 10 July 2014).
34. Gómez, J.M., Verdu, M. & Perfectti, F. (2010) Ecological interactions are evolutionarily conserved across the entire tree of life. Nature, 465, 918–921.
35. Guimera, R. & Amaral, L.A.N. (2005) Cartography of complex networks: modules and universal roles. Journal of Statistical Mechanics: Theory and Experiment, P02001, 1–3. PO2001.
36. Hobbs, R.J., Arico, S., Aronson, J., Baron, J.S., Bridgewater, P., Cramer, V.A., Epstein, P.R., Ewel, J.J., Klink, C.A., Lugo, A.E., Norton, D., Ojima, D., Richardson, D.M., Sanderson, E.W., Valladares, F., Vila, M., Zamora, R. & Zobel, M. (2006) Novel ecosystems: theoretical and management aspects of the new ecological world order. Global Ecology and Biogeography, 15, 1–7.
37. Huang, Z.-H., Liu, H.-L. & Huang, S.-Q. (2015) Interspecific pollen transfer between two coflowering species was minimized by bumblebee fidelity and differential pollen placement on the bumblebee body. Journal of Plant Ecology, 8, 109–115.
38. Hulme, P.E. (2012) Weed risk assessment: a way forward or a waste of time? Journal of Applied Ecology, 49, 10–19.
39. Invasive species of Japan Available at: https://www.nies.go.jp (accessed 10 July 2014).
40. Jordano, P., Bascompte, J. & Olesen, J.M. (2003) Invariant properties in coevolutionary networks of plant–animal interactions. Ecology Letters, 6, 69–81.
41. Kaiser-Bunbury, C.N., Valentin, T., Mougal, J., Matatiken, D. & Ghazoul, J. (2011) The tolerance of island plant–pollinator networks to alien plants. Journal of Ecology, 99, 202–213.
42. Lopezaraiza-Mikel, M.E., Hayes, R.B., Whalley, M.R. & Memmott, J. (2007) The impact of an alien plant on a native plant–pollinator network: an experimental approach. Ecology Letters, 10, 539–550.
43. Madjidian, J.A., Morales, C.L. & Smith, H.G. (2008) Displacement of a native by an alien bumblebee: lower pollinator efficiency overcome by overwhelmingly higher visitation frequency. Oecologia, 156, 835–845.
44. Martín Gonzalez, A.M., Dalsgaard, B. & Olesen, J.M. (2010) Centrality measures and the importance of generalist species in pollination networks. Ecological Complexity, 7, 36–43.
45. Maruyama, P.K., Vizentin-Bugoni, J., Sonne, J. et al. (2016) The integration of alien plants in mutualistic plant-hummingbird networks across the Americas: the importance of species traits and insularity. Diversity and Distributions, 22, 672–681.
46. Memmott, J. & Waser, N.M. (2002) Integration of alien plants into a native flower-pollinator visitation web. Proceedings of the Royal Society B: Biological Sciences, 269, 2395–2399.
47. Montgomery, B.R. & Rathcke, B.J. (2012) Effects of floral restrictiveness and stigma size on heterospecific pollen receipt in a prairie community. Oecologia, 168, 449–458.
48. Morales, C.L. & Traveset, A. (2008) Interspecific pollen transfer: magnitude, prevalence and consequences for plant fitness. Critical Reviews in Plant Sciences, 27, 221–238.
49. Moran, M.D. (2003) Arguments for rejecting the sequential Bonferroni in ecological studies. Oikos, 100, 403–405.
50. Nakagawa, S. & Schielzeth, H. (2013) A general and simple method for obtaining R2 from generalized linear mixed-effects models. Methods in Ecology and Evolution, 4, 133–142.
51. Olesen, J.M. & Jordano, P. (2002) Geographic patterns in plant–pollinator mutualistic networks. Ecology, 83, 2416–2424.
52. Olesen, J.M., Eskildsen, L.I. & Venkatasamy, S. (2002) Invasion of pollination networks on oceanic islands: importance of invader complexes and endemic super generalists. Diversity and Distributions, 8, 181–192.
53. Olesen, J.M., Bascompte, J., Dupont, Y.L. & Jordano, P. (2007) The modularity of pollination networks. Proceedings of the National Academy of Sciences USA, 104, 19891–19896.
54. Olesen, J.M., Bascompte, J., Dupont, Y.L., Elberling, H., Rasmussen, C. & Jordano, P. (2011) Missing and forbidden links in mutualistic networks. Proceedings of the Royal Society B: Biological Sciences, 278, 725–732.
55. Ollerton, J., Winfree, R. & Tarrant, S. (2011) How many flowering plants are pollinated by animals? Oikos, 120, 321–326.
56. Ortega, R. (2014) Web of life. Available at: http://www.web-of-life.es (accessed 15 July 2014).
57. Pysek, P. & Richardson, D.M. (2007) Traits associated with invasiveness in alien plants: where do we stand? Ecological studies (ed. by M.M. Caldwell, D. Diaz, G. Heldmaier, R.B. Jackson, O.L. Lange, D.F. Levia, H.A. Mooney, E.D. Schulze and U. Sommer), pp. 97–125. Springer-Verlag, Berlin & Heidelberg.
58. R Core Team (2014) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Available at: http://www.R-project.org (accessed 5 April 2016).
59. Rezende, E.L., Lavabre, J.E., Guimarães, P.R. Jr, Jordano, P. & Bascompte, J. (2007) Non-random coextinctions in phylogenetically structured mutualistic networks. Nature, 448, 925–928.
60. Richardson, D.M. & Pysek, P. (2006) Plant invasions: merging the concepts of species invasiveness and community invasibility. Progress in Physical Geography, 30, 409–431.
61. Romanuk, T.N., Zhou, Y., Brose, U., Berlow, E.L., Williams, R.J. & Martinez, N.D. (2009) Predicting invasion success in complex ecological networks. Philosophical Transactions of the Royal Society B: Biological Sciences, 364, 1743–1754.
62. Roy, H.E., Adriaens, T., Isaac, N.J.B., Kenis, M., Onkelinx, T., San Martin, G., Brown, P.M.J., Hautier, L., Poland, R., Roy, D.B., Comont, R., Eschen, R., Frost, R., Zindel, R., Van Vlaenderen, J., Nedved, O., Ravn, H.P., Gregoire, J.-C., de Biseau, J.-C. & Maes, D. (2012) Invasive alien predator causes rapid declines of native European ladybirds. Diversity and Distributions, 18, 717–725.
63. Santos, G.M.d.M., Aguiar, C.M.L., Genini, J., Martins, C.F., Zanella, F.C.V. & Mello, M.A.R. (2012) Invasive Africanized honeybees change the structure of native pollination networks in Brazil. Biological Invasions, 14, 2369–2378.
64. Schleuning, M., Frund, J., Klein, A.M. et al. (2012) Specialization of mutualistic interaction networks decreases toward tropical latitudes. Current Biology, 22, 1925–1931.
65. Solé, R.V. & Montoya, J.M. (2001) Complexity and fragility in ecological networks. Proceedings of the Royal Society B: Biological Sciences, 268, 2039–2045.
66. Staniczenko, P.P.A., Lewis, O.T., Jones, N.S. & Reed-Tsochas, F. (2010) Structural dynamics and robustness of food webs. Ecology Letters, 13, 891–899.
67. Staniczenko, P.P.A., Kopp, J. & Allesina, S. (2013) The ghost of nestedness in ecological networks. Nature Communications, 4, 1391.
68. Stouffer, D.B., Sales-Pardo, M., Sirer, M.I. & Bascompte, J. (2012) Evolutionary conservation of species’ roles in food webs. Science, 335, 1489–1492.
69. Stouffer, D.B., Cirtwill, A.R. & Bascompte, J. (2014) How exotic plants integrate into pollination networks. Journal of Ecology, 102, 1442–1450.
70. The Global Invasive Species Database (GISD)Available at: http://www.issg.org/database/welcome/ (accessed 10 July 2014).
71. The Non-native Species Secretariat (NNSS)Available at: http://www.nonnativespecies.org (accessed 10 July 2014).
72. The Plant Pest Information Network (PPIN)Available at: http://archive.mpi.govt.nz/applications/ppin (accessed 10 July 2014).
73. Thuiller, W., Richardson, D.M., Pysek, P., Midgley, G.F., Hughes, G.O. & Rouget, M. (2005) Niche-based modeling as a tool for predicting the risk of alien plant invasions at a global scale. Global Change Biology, 11, 2234–2250.
74. Traveset, A. & Richardson, D.M. (2006) Biological invasions as disruptors of plant reproductive mutualisms. Trends in Ecology and Evolution, 21, 208–216.
75. Traveset, A. & Richardson, D.M. (2014) Mutualistic interactions and biological invasions. Annual Review of Ecology, Evolution, and Systematics, 45, 89–113.
76. Traveset, A., Heleno, R., Chamorro, S., Vargas, P., McMullen, C.K., Castro-Urgal, R., Nogales, M., Herrera, H.W. & Olesen, J.M. (2013) Invaders of pollination networks in the Galapagos Islands: emergence of novel communities. Proceedings of the Royal Society B: Biological Sciences, 280, 20123040.
77. Trøjelsgaard, K., Jordano, P., Carstensen, D.W. & Olesen, J.M. (2015) Geographical variation in mutualistic networks: similarity, turnover and partner fidelity. Proceedings of the Royal Society B: Biological Sciences, 282, 20142925.
78. Tylianakis, J.M., Didham, R.K., Bascompte, J. & Wardle, D.A. (2008) Global change and species interactions in terrestrial ecosystems. Ecology Letters, 11, 1351–1363.
79. Warton, D.I. & Hui, F.K.C. (2011) The arcsine is asinine: the analysis of proportions in ecology. Ecology, 92, 3–10.
80. Waser, N.M. & Ollerton, J. (2006) Plant–pollinator interactions: from specialization to generalization, 1st edn. University of Chicago Press, Chicago, IL.
81. Weeds in AustraliaAvailable at: http://www.environment.gov.au/biodiversity/invasive/weeds/ (accessed 10 July 2014).
82. Willmer, P.G. & Finlayson, K. (2014) Big bees do a better job: intraspecific size variation influences pollination effectiveness. Journal of Pollination Ecology, 14, 244–254.
83. Zuur, A.F., Ieno, E.N., Walker, N.J., Saveliev, A.A. & Smith, G.M. (2009) Mixed effects models and extensions in ecology with R, 1st edn. Springer, New York, NY.