Abstract
The Anthropocene is marked by an unprecedented homogenisation of the world’s biota, confronting species that never co-occurred during their evolutionary histories. Interactions established in these novel communities may affect ecosystem functioning; however, most research has focused on the impacts of a minority of aggressive invasive species, while changes inflicted by a less conspicuous majority of non-invasive alien species on community structure are still poorly understood. This information is critical to guide conservation strategies, and instrumental to advance ecological theory, particularly to understand how non-native species integrate in recipient communities and affect the interactions of native species. We evaluated how the structure of 50 published pollination networks changes with the proportion of alien plant species and found that network structure is largely unaffected. Although some communities were heavily invaded, the proportion of alien plant species was relatively low (mean = 10%; max. = 38%). We further characterized the pollination network in a botanic garden with a plant community dominated by non-invasive alien species (85%). We show that the structure of this novel community is also not markedly different from native-dominated communities. Plant–pollinator interactions revealed no obvious differences regarding plant origin (native vs. alien) or the native bioregion of the introduced plants. This overall similarity between native and alien plants is likely driven by the contrasting patterns of invasive plants (promoting generalism), and non-invasive aliens, suggested here to promote specialization.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Aizen MA, Morales CL, Morales JM (2008) Invasive mutualists erode native pollination webs. PLoS Biol 6:e31. https://doi.org/10.1371/journal.pbio.0060031
Albrecht M, Padron B, Bartomeus I, Traveset A (2014) Consequences of plant invasions on compartmentalization and species’ roles in plant-pollinator networks. Proc R Soc B Biol Sci 281:20140773. https://doi.org/10.1098/rspb.2014.0773
Barnosky AD, Hadly EA, Bascompte J, Berlow EL, Brown JH, Fortelius M, Getz WM, Harte J, Hastings A, Marquet PA et al (2012) Approaching a state shift in Earth/’s biosphere. Nature 486:52–58. https://doi.org/10.1038/nature11018
Bartomeus I, Vilà M, Santamaría L (2008) Contrasting effects of invasive plants in plant–pollinator networks. Oecologia 155:761–770. https://doi.org/10.1007/s00442-007-0946-1
Blüthgen N, Menzel F, Blüthgen N (2006) Measuring specialization in species interaction networks. BMC Ecol 6:9. https://doi.org/10.1186/1472-6785-6-9
Cantoni E, Ronchetti E (2001) Robust inference for generalized linear models. J Am Stat Assoc 96:1022–1030. https://doi.org/10.1198/016214501753209004
Cantoni E, Ronchetti E (2006) A robust approach for skewed and heavy-tailed outcomes in the analysis of health care expenditures. J Health Econ 25:198–213. https://doi.org/10.1016/j.jhealeco.2005.04.010
Carvalheiro LG, Barbosa ERM, Memmott J (2008) Pollinator networks, alien species and the conservation of rare plants: trinia glauca as a case study. J Appl Ecol 45:1419–1427
Castro-Urgal R, Tur C, Albrecht M, Traveset A (2012) How different link weights affect the structure of quantitative flower-visitation networks. Basic Appl Ecol 13:500–508. https://doi.org/10.1016/j.baae.2012.08.002
Chittka L, Schürkens S (2001) Successful invasion of a floral market. Nature 411:653. https://doi.org/10.1038/35079676
Costa JM, da Silva LP, Ramos JA, Heleno RH (2015) Sampling completeness in seed dispersal networks: when enough is enough. Basic Appl Ecol. https://doi.org/10.1016/j.baae.2015.09.008
Cox B (2001) The biogeographic regions reconsidered. J Biogeogr 28:511–523. https://doi.org/10.1046/j.1365-2699.2001.00566.x
de Buffon G-LL (1761) Histoire naturelle générale et particulière. L’Imprimerie de F. Dufart, Paris
Devictor V, Clavel J, Julliard R, Lavergne S, Mouillot D, Thuiller W, Venail P, Villéger S, Mouquet N (2010) Defining and measuring ecological specialization. J Appl Ecol 47:15–25. https://doi.org/10.1111/j.1365-2664.2009.01744.x
Dormann CF (2011) How to be a specialist? Quantifying specialisation in pollination networks. Netw Biol 1:1–20
Dormann CF, Gruber B, Fründ J (2008) Introducing the bipartite package: analysing ecological networks. R News 8:8–11
Dormann CF, Fründ J, Bluthgen N, Gruber B (2009) Indices, graphs and null models: analysing bipartite ecological networks. Open Ecol J 2:7–24. https://doi.org/10.2174/1874213000902010007
Dormann CF, Fründ J, Schaefer HM (2017) Identifying causes of patterns in ecological networks: opportunities and limitations. Annu Rev Ecol Evol Syst 48:559–584. https://doi.org/10.1146/annurev-ecolsys-110316-022928
Fründ J, McCann KS, Williams NM (2016) Sampling bias is a challenge for quantifying specialization and network structure: lessons from a quantitative niche model. Oikos 125:502–513. https://doi.org/10.1111/oik.02256
Galeano J, Pastor JM, Iriondo JM (2009) weighted-interaction nestedness estimator (WINE): a new estimator to calculate over frequency matrices. Environ Model Softw 24:1342–1346. https://doi.org/10.1016/j.envsoft.2009.05.014
GBIF (2017) GBIF: the global biodiversity information facility.https://www.gbif.org/what-is-gbif. Accessed 28 Dec 2017
Grass I, Berens DG, Peter F, Farwig N (2013) Additive effects of exotic plant abundance and land-use intensity on plant-pollinator interactions. Oecologia 173:913–923. https://doi.org/10.1007/s00442-013-2688-6
Hansen DM, Donlan CJ, Griffiths CJ, Campbell KJ (2010) Ecological history and latent conservation potential: large and giant tortoises as a model for taxon substitutions. Ecography 33:272–284. https://doi.org/10.1111/j.1600-0587.2010.06305.x
Heleno RH, Ceia RS, Ramos JA, Memmott J (2009) Effects of alien plants on insect abundance and biomass: a food-web approach. Conserv Biol 23:410–419. https://doi.org/10.1111/j.1523-1739.2008.01129.x
Heleno R, Garcia C, Jordano P, Traveset A, Gomez JM, Bluthgen N, Memmott J, Moora M, Cerdeira J, Rodriguez-Echeverria S, Freitas H, Olesen JM (2014) Ecological networks: delving into the architecture of biodiversity. Biol Let 10:20131000. https://doi.org/10.1098/rsbl.2013.1000
Hobbs RJ, Arico S, Aronson J, Baron JS, Bridgewater P, Cramer VA, Epstein PR, Ewel JJ, Klink CA, Lugo AE, Norton D, Ojima D, Richardson DM, Sanderson EW, Valladares F, Vila M, Zamora R, Zobel M (2006) Novel ecosystems: theoretical and management aspects of the new ecological world order. Glob Ecol Biogeogr 15:1–7. https://doi.org/10.1111/j.1466-822X.2006.00212.x
Hothorn T, Bretz F, Westfall P (2008) Simultaneous inference in general parametric models. Biom J 50:346–363
Hui C, Richardson DM, Landi P, Minoarivelo HO, Garnas J, Roy HE (2016) Defining invasiveness and invasibility in ecological networks. Biol Invasions 18:971–983. https://doi.org/10.1007/s10530-016-1076-7
Kaiser-Bunbury CN, Valentin T, Mougal J, Matatiken D, Ghazoul J (2011) The tolerance of island plant–pollinator networks to alien plants. J Ecol 99:202–213. https://doi.org/10.1111/j.1365-2745.2010.01732.x
Kaiser-Bunbury CN, Mougal J, Whittington AE, Valentin T, Gabriel R, Olesen JM, Blüthgen N (2017) Ecosystem restoration strengthens pollination network resilience and function. Nature 542:223–227. https://doi.org/10.1038/nature21071
Le Roux JJ, Hui C, Keet JH, Ellis AG (2017) Co-introduction vs ecological fitting as pathways to the establishment of effective mutualisms during biological invasions. New Phytol 215:1354–1360. https://doi.org/10.1111/nph.14593
Lopezaraiza-Mikel ME, Hayes RB, Whalley MR, Memmott J (2007) The impact of an alien plant on a native plant–pollinator network: an experimental approach. Ecol Lett 10:539–550. https://doi.org/10.1111/j.1461-0248.2007.01055.x
López-Núñez FA, Heleno RH, Ribeiro S, Marchante H, Marchante E (2017) Four-trophic level food webs reveal the cascading impacts of an invasive plant targeted for biocontrol. Ecology 98:782–793. https://doi.org/10.1002/ecy.1701
Lurgi M, Lopez BC, Montoya JM (2012) Novel communities from climate change. Philos Trans R Soc B Biol Sci 367:2913–2922. https://doi.org/10.1098/rstb.2012.0238
Marchante H, Morais M, Freitas H, Marchante E (2014) Guia prático para a identificação de plantas invasoras em Portugal. Imprensa da Universidade de Coimbra, Coimbra
McKinney ML, Lockwood JL (1999) Biotic homogenization: a few winners replacing many losers in the next mass extinction. Trends Ecol Evol 14:450–453. https://doi.org/10.1016/S0169-5347(99)01679-1
Memmott J, Waser NM (2002) Integration of alien plants into a native flower-pollinator visitation web. Proc R Soc B: Biol Sci 269:2395–2399. https://doi.org/10.1098/rspb.2002.2174
Memmott J, Waser NM, Price MV (2004) Tolerance of pollination networks to species extinctions. Proc R Soc B Biol Sci 271:2605–2611. https://doi.org/10.1098/rspb.2004.2909
Morales CL, Aizen MA (2006) Invasive mutualisms and the structure of plant–pollinator interactions in the temperate forests of north-west Patagonia, Argentina. J Ecol 94:171–180. https://doi.org/10.1111/j.1365-2745.2005.01069.x
Morton EM, Rafferty NE (2017) Plant–pollinator interactions under climate change: the use of spatial and temporal transplants. Appl Plant Sci 5:1600133. https://doi.org/10.3732/apps.1600133
Olden JD, Poff NL, McKinney ML (2006) Forecasting faunal and floral homogenization associated with human population geography in North America. Biol Cons 127:261–271. https://doi.org/10.1016/j.biocon.2005.04.027
Padrón B, Traveset A, Biedenweg T, Díaz D, Nogales M, Olesen JM (2009) Impact of alien plant invaders on pollination networks in two archipelagos. PLoS ONE. https://doi.org/10.1371/journal.pone.0006275
Patefield WM (1981) Algorithm AS 159: an Efficient Method of Generating Random R × C Tables with Given Row and Column Totals. Appl Stat 30:91–97. https://doi.org/10.2307/2346669
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. https://doi.org/10.1016/j.tree.2010.01.007
Primack RB, Miller-Rushing AJ (2009) The role of botanical gardens in climate change research. New Phytol 182:303–313. https://doi.org/10.1111/j.1469-8137.2009.02800.x
R Core Team (2017) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/
Razanajatovo M, Föhr C, Fischer M, Prati D, van Kleunen M (2015) Non-naturalized alien plants receive fewer flower visits than naturalized and native plants in a Swiss botanical garden. Biol Cons 182:109–116. https://doi.org/10.1016/j.biocon.2014.11.043
Razanajatovo M, Föhr C, van Kleunen M, Fischer M (2018) Phenological shifts and flower visitation of 185 lowland and alpine species in a lowland botanical garden. Alpine Bot. https://doi.org/10.1007/s00035-018-0201-x
Richardson DM (2010) Fifty years of invasion ecology. Wiley-Blackwell, Oxford
Richardson DM, Allsopp N, D’Antonio CM, Milton SJ, Rejmánek M (2000a) Plant invasions—the role of mutualisms. Biol Rev 75:65–93
Richardson DM, Pyšek P, Rejmánek M, Barbour MG, Dane Panetta F, West CJ (2000b) Naturalization and invasion of alien plants: concepts and definitions. Divers Distrib 6:93–107. https://doi.org/10.1046/j.1472-4642.2000.00083.x
Rousseeuw P, Croux C, Todorov V, Ruckstuhl A, Salibian-Barrera M, Verbeke T, Koller M, Concieção E, di Palma MA (2017) Robustbase: basic robust statistics R package version 0.92-8. 169
Rumeu B, Devoto M, Traveset A, Olesen JM, Vargas P, Nogales M, Heleno R (2017) Predicting the consequences of disperser extinction: richness matters the most when abundance is low. Funct Ecol. https://doi.org/10.1111/1365-2435.12897
Schleuning M, Fründ J, Klein A-M, 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-C, 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. https://doi.org/10.1016/j.cub.2012.08.015
Smart SM, Thompson K, Marrs RH, Le Duc MG, Maskell LC, Firbank LG (2006) Biotic homogenization and changes in species diversity across human-modified ecosystems. Proc Biol Sci 273:2659–2665. https://doi.org/10.1098/rspb.2006.3630
Stouffer DB, Cirtwill AR, Bascompte J (2014) How exotic plants integrate into pollination networks. J Ecol 102:1442–1450. https://doi.org/10.1111/1365-2745.12310
Thebault E, Fontaine C (2010) Stability of ecological communities and the architecture of mutualistic and trophic networks. Science 329:853–856. https://doi.org/10.1126/science.1188321
Traveset A, Richardson DM (2006) Biological invasions as disruptors of plant reproductive mutualisms. Trends Ecol Evol 21:208–216. https://doi.org/10.1016/J.TREE.2006.01.006
Traveset A, Heleno R, Chamorro S, Vargas P, McMullen CK, Castro-Urgal R, Nogales M, Herrera HW, Olesen JM (2013) Invaders of pollination networks in the Galapagos Islands: emergence of novel communities. Proc R Soc B Biol Sci 280:20123040. https://doi.org/10.1098/rspb.2012.3040
Traveset A, Tur C, Trøjelsgaard K, Heleno R, Castro-Urgal R, Olesen JM (2016) Global patterns of mainland and insular pollination networks. Glob Ecol Biogeogr 25:880–890. https://doi.org/10.1111/geb.12362
Tylianakis JM, Morris RJ (2017) Ecological networks across environmental gradients. Annu Rev Ecol Evol Syst 48:25–48. https://doi.org/10.1146/annurev-ecolsys-110316-022821
Tylianakis JM, Tscharntke T, Lewis OT (2007) Habitat modification alters the structure of tropical host–parasitoid food webs. Nature 445:202–205. https://doi.org/10.1038/nature05429
van Kleunen M, Essl F, Pergl J, Brundu G, Carboni M, Dullinger S, Early R, González-Moreno P, Groom QJ, Hulme PE, Kueffer C, Kühn I, Máguas C, Maurel N, Novoa A, Parepa M, Pyšek P, Seebens H, Tanner R, Touza J, Verbrugge L, Weber E, Dawson W, Kreft H, Weigelt P, Winter M, Klonner G, Talluto MV, Dehnen-Schmutz K (2018) The changing role of ornamental horticulture in alien plant invasions. Biol Rev 93:1421–1437. https://doi.org/10.1111/brv.12402
Vander Zanden MJ (2005) The success of animal invaders. Proc Natl Acad Sci 102:7055–7056. https://doi.org/10.1073/pnas.0502549102
Vilà M, Bartomeus I, Dietzsch AC, Petanidou T, Steffan-Dewenter I, Stout JC, Tscheulin T (2009) Invasive plant integration into native plant–pollinator networks across Europe. Proc Biol Sci 276:3887–3893. https://doi.org/10.1098/rspb.2009.1076
Vilà M, Basnou C, Pyšek P, Josefsson M, Genovesi P, Gollasch S, Nentwig W, Olenin S, Roques A, Roy D, Hulme PE, Andriopoulos P, Arianoutsou M, Bazos I, Kokkoris I, Yannitsaros A, Zikos A, Augustin S, Cochard PO, Lopez-Vaamonde C, Sauvard D, Yart A, Bacher S, Bretagnolle F, Gasquez J, Chiron F, Kark S, Shirley S, Clergeau P, Cocquempot C, Coeur d’Acier A, Dorkeld F, Migeon A, Navajas M, David M, Delipetrou P, Georghiou K, Desprez-Loustau ML, Didziulis V, Essl F, Galil BS, Hedja M, Jarosik V, Pergl J, Perglová I, Kühn I, Winter M, Kühn PW, Marcer A, Pino J, McLoughlin M, Minchin D, Panov VE, Pascal M, Poboljsaj K, Scalera R, Sedlácek O, Zagatti P (2010) How well do we understand the impacts of alien species on ecosystem services? A pan-European, cross-taxa assessment. Front Ecol Environ 8:135–144. https://doi.org/10.1890/080083
von Humboldt A (1816) Sur les lois que l’on observe dans la distribution des formes vegetales. Ann Chim Phys 1:225–239
WCSP (2017) World checklist of selected plant families. Facilitated by the Royal Botanic Gardens, Kew. http://wcsp.science.kew.org/. Accessed 28 Dec 2017
Williamson M (1993) Invaders, weeds and the risk from genetically manipulated organisms. Experientia 49:219–224. https://doi.org/10.1007/BF01923529
Acknowledgements
We would like to thank Carine Azevedo, Arménio Matos, Filipe Covelo and Kathryn Dix for their valuable assistance with pollination sampling and plant identifications. This work was financed by Fundação para Ciência e Tecnologia/Ministério da Educação e Ciência through national funds and co-funded by the European Regional Development Fund—FEDER, within the Portugal 2020 Partnership Agreement, and the Operational Thematic Program for Competitiveness and Internationalization—COMPETE 2020, namely through project UID/BIA/04004/2013, and grants SFRH/BD/130942/2017 (FLN), SFRH/BD/96292/2013 (JMC), and IF/00441/2013 (RHH). The Botanic Garden of the University of Coimbra is part of PRISC—Portuguese Research Infrastructure of Scientific Collections (POCI-01-0145-FEDER-022168).
Author information
Authors and Affiliations
Contributions
RHH and AG designed the study. CO, FL-N and JMC collected the data. ST and CO performed the analysis and lead the writing with substantial contributions of all authors to discussions and revisions.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Communicated by Monica Geber.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Timóteo, S., O’Connor, C.J., López-Núñez, F.A. et al. Pollination networks from natural and anthropogenic-novel communities show high structural similarity. Oecologia 188, 1155–1165 (2018). https://doi.org/10.1007/s00442-018-4281-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00442-018-4281-5