Skip to main content
SpringerLink
Log in

Invasive Asteraceae plants can enhance community stability by changing pollination network structure, yet cause intense pollen disturbance to native plants in an oceanic island community

  • Original Paper
  • Published:
Biological Invasions Aims and scope Submit manuscript

Abstract

Invasive plant species severely threaten natural plant communities around the world, especially for islands. As introduction rates rise, novel species interactions appear within ecosystems. Studies that focus on invasive plant impacts on native plants, especially on native communities, remain rare and their conclusions are mixed. We constructed ten quantitative plant-pollinator interaction networks and calculated five network-level structure metrics (interaction evenness, linkage density, specialization, weighted connectance, and weighted nestedness) along an Asteraceae invasion gradient in the Yongxing Island community. We calculated the species-level nestedness contribution of each plant species in each network, and compared the nestedness contribution differences between invasive Asteraceae and non-Asteraceae species. Stigmas of three native and four invasive Asteraceae species were collected, and their pollen grains were identified. We analyzed invasive Asteraceae species impacts on native pollination network structure and the pollen deposition of native plants. Both weighted nestedness and weighted connectance increased significantly as invasive Asteraceae became increasingly dominant. Invasive Asteraceae plants had higher nestedness contribution compared to native plants in most sites, and this difference increased as the Asteraceae proportion increased. Furthermore, in native plant species, the proportion of conspecific pollen grains on stigmas decreased significantly, while the proportion of Asteraceae pollen grains on stigmas increased significantly as Asteraceae invasion level increased. For the four Asteraceae species, the proportion of conspecific pollen grains was significantly higher than heterospecific and other Asteraceae pollen grains on the stigmas. These results significantly add to our understanding of how the structure of plant-pollinator interaction networks changes concomitantly with plant invasion intensity. Invasive Asteraceae increase community stability and persistence, and increase the heterospecific pollen deposition on stigmas of native plants as invasion level increases. Invasive plants may greatly shape network structure and maintain community stability in oceanic island systems. Heterospecific pollen avoidance may be crucial mechanism facilitating Asteraceae invasion success within native communities, together with their ‘integration’, into plant-pollinator interactions on the Yongxing Island.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Aizen MA, Morales CL, Morales JM (2008) Invasive mutualists erode native pollination webs. PLoS Biol 6(2):e31

    Article  PubMed  PubMed Central  Google Scholar 

  • Albrecht M, Padrón B, Bartomeus I, Traveset A (2014) Consequences of plant invasions on compartmentalization and species’ roles in plant–pollinator networks. Proc R Soc Lond Series B Biol Sci 281(1788):20140773

    Google Scholar 

  • Arceo-Gómez G, Ashman TL (2016) Invasion status and phylogenetic relatedness predict cost of heterospecific pollen receipt: implications for native biodiversity decline. J Ecol 104(4):1003–1008

    Article  Google Scholar 

  • Arceo-Gómez G, Kaczorowski RL, Patel C, Ashman TL (2019) Interactive effects between donor and recipient species mediate fitness costs of heterospecific pollen receipt in a co-flowering community. Oecologia 189(4):1041–1047

    Article  PubMed  Google Scholar 

  • Ashman TL, Arceo-Gómez G (2013) Toward a predictive understanding of the fitness costs of heterospecific pollen receipt and its importance in co-flowering communities. Am J Bot 100(6):1061–1070

    Article  PubMed  Google Scholar 

  • Ashman TL, Alonso C, Parra-Tabla V, Arceo-Gómez G (2020) Pollen on stigmas as proxies of pollinator competition and facilitation: complexities, caveats and future directions. Ann Bot 125(7):1003–1012

    Article  PubMed  PubMed Central  Google Scholar 

  • Bartomeus I, Bosch J, Vilà M (2008) High invasive pollen transfer, yet low deposition on native stigmas in a Carpobrotus-invaded community. Ann Bot 102(3):417–424

    Article  PubMed  PubMed Central  Google Scholar 

  • Bascompte J, Jordano P (2007) Plant-animal mutualistic networks: the architecture of biodiversity. Annu Rev Ecol Evol Syst 38:567–593

    Article  Google Scholar 

  • Bascompte J, Jordano P, Melián CJ, Olesen JM (2003) The nested assembly of plant–animal mutualistic networks. Proc Natl Acad Sci USA 100(16):9383

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Biella P, Ssymank A, Galimberti A, Galli P, Perlík M, Ramazzotti F, Rota A, Tommasi N (2022) Updating the list of flower-visiting bees, hoverflies and wasps in the central atolls of Maldives, with notes on land-use effects. Biodivers Data J. https://doi.org/10.3897/BDJ.10.e85107

    Article  PubMed  PubMed Central  Google Scholar 

  • Bjerknes AL, Totland Ø, Hegland SJ, Nielsen A (2007) Do alien plant invasions really affect pollination success in native plant species? Biol Cons 138(1–2):1–12

    Article  Google Scholar 

  • Campbell C, Russo L, Albert R, Buckling A, Shea K (2022) Whole community invasions and the integration of novel ecosystems. PLoS Comput Biol 18(6):e1010151

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Charlebois JA, Sargent RD (2017) No consistent pollinator-mediated impacts of alien plants on natives. Ecol Lett 20(11):1479–1490

    Article  PubMed  Google Scholar 

  • Corcos D, Cappellari A, Mei M, Paniccia D, Cerretti P, Marini L (2020) Contrasting effects of exotic plant invasions and managed honeybees on plant-flower visitor interactions. Divers Distrib 26(10):1397–1408

    Article  Google Scholar 

  • Daniels JD, Arceo-Gómez G (2020) Effects of invasive Cirsium arvense on pollination in a southern Appalachian floral community vary with spatial scale and floral symmetry. Biol Invasions 22(2):783–797

    Article  Google Scholar 

  • Emer C, Vaughan IP, Hiscock S, Memmott J (2015) The impact of the invasive alien plant, Impatiens glandulifera, on pollen transfer networks. PLoS ONE 10(12):e0143532

    Article  PubMed  PubMed Central  Google Scholar 

  • Fang Q, Huang SQ (2013) A directed network analysis of heterospecific pollen transfer in a biodiverse community. Ecology 94(5):1176–1185

    Article  PubMed  Google Scholar 

  • Fang Q, Gao J, Armbruster WS, Huang SQ (2019) Multi-year stigmatic pollen-load sampling reveals temporal stability in interspecific pollination of flowers in a subalpine meadow. Oikos 128(12):1739–1747

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Hao Q, Ma JS (2023) Invasive alien plants in China: an update. Plant Diversity 45(1):117

    Article  PubMed  Google Scholar 

  • Heleno RH, Ramos JA, Memmott J (2013) Integration of exotic seeds into an Azorean seed dispersal network. Biol Invasions 15:1143–1154

    Article  Google Scholar 

  • Johnson AL, Ashman TL (2019) Consequences of invasion for pollen transfer and pollination revealed in a tropical island ecosystem. New Phytol 221(1):142–154

    Article  PubMed  Google Scholar 

  • Kaiser-Bunbury CN, Traveset A, Hansen DM (2010) Conservation and restoration of plant–animal mutualisms on oceanic islands. Perspect Plant Ecol, Evol Syst 12(2):131–143

    Article  Google Scholar 

  • 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(1):202–213

    Article  Google Scholar 

  • 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(7640):223–227

    Article  CAS  PubMed  Google Scholar 

  • Kueffer C, Daehler CC, Torres-Santana CW, Lavergne C, Meyer J-Y, Otto R, Silva L (2010) A global comparison of plant invasions on oceanic islands. Perspect Plant Ecol, Evol Syst 12:145–161

    Article  Google Scholar 

  • Lambertini M, Leape J, Marton-Lefevre J, Mittermeier RA, Rose M, Robinson JG, Genovesi P (2011) Invasives: a major conservation threat. Science 333(6041):404–405

    Article  CAS  PubMed  Google Scholar 

  • Lopes SA, Bergamo PJ, Queiroz SNP, Ollerton J, Santos T, Rech AR (2022) Heterospecific pollen deposition is positively associated with reproductive success in a diverse hummingbird‐pollinated plant community. Oikos. https://doi.org/10.1111/oik.08714

    Article  Google Scholar 

  • Memmott J, Waser NM (2002) Integration of alien plants into a native flower–pollinator visitation web. Proc R Soc Lond Series B Biol Sci 269(1508):2395–2399

    Article  Google Scholar 

  • Memmott J, Waser NM, Price MV (2004) Tolerance of pollination networks to species extinctions. Proc R Soc Lond Series B Biol Sci 271(1557):2605–2611

    Article  Google Scholar 

  • Montero-Castaño A, Vilà M (2017) Influence of the honeybee and trait similarity on the effect of a non-native plant on pollination and network rewiring. Funct Ecol 31(1):142–152

    Article  Google Scholar 

  • Montero-Castaño A, Vilà M, Ortiz-Sánchez FJ (2014) Pollination ecology of a plant in its native and introduced areas. Acta Oecologica 56:1–9

    Article  Google Scholar 

  • Morales CL, Traveset A (2009) A meta-analysis of impacts of alien vs. native plants on pollinator visitation and reproductive success of co-flowering native plants. Ecol Lett 12(7):716–728

    Article  PubMed  Google Scholar 

  • Olesen JM, Eskildsen LI, Venkatasamy S (2002) Invasion of pollination networks on oceanic islands: importance of invader complexes and endemic super generalists. Divers Distrib 8(3):181–192

    Article  Google Scholar 

  • 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 4(7):e6275

    Article  PubMed  PubMed Central  Google Scholar 

  • Parra-Tabla V, Arceo-Gómez G (2021) Impacts of plant invasions in native plant–pollinator networks. New Phytol 230(6):2117–2128

    Article  PubMed  Google Scholar 

  • Parra-Tabla V, Angulo-Pérez D, Albor C, Campos-Navarrete MJ, Tun-Garrido J, Sosenski P, Arceo-Gómez G (2019) The role of alien species on plant-floral visitor network structure in invaded communities. PLoS ONE 14(11):e0218227

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Parra-Tabla V, Alonso C, Ashman TL, Raguso RA, Albor C, Sosenski P, Arceo-Gómez G (2021) Pollen transfer networks reveal alien species as main heterospecific pollen donors with fitness consequences for natives. J Ecol 109(2):939–951

    Article  Google Scholar 

  • Petanidou T, Kallimanis AS, Tzanopoulos J, Sgardelis SP, Pantis JD (2008) Long-term observation of a pollination network: fluctuation in species and interactions, relative invariance of network structure and implications for estimates of specialization. Ecol Lett 11(6):564–575

    Article  PubMed  Google Scholar 

  • Russo L, Albert R, Campbell C, Shea K (2019) Experimental species introduction shapes network interactions in a plant-pollinator community. Biol Invasions 21(12):3505–3519

    Article  Google Scholar 

  • Saavedra S, Stouffer DB (2013) “Disentangling nestedness” disentangled. Nature 500:E1–E3

    Article  CAS  PubMed  Google Scholar 

  • Saavedra S, Stouffer DB, Uzzi B, Bascompte J (2011) Strong contributors to network persistence are the most vulnerable to extinction. Nature 478(7368):233–235

    Article  CAS  PubMed  Google Scholar 

  • Stouffer DB, Cirtwill AR, Bascompte J (2014) How exotic plants integrate into pollination networks. J Ecol 102(6):1442–1450

    Article  PubMed  PubMed Central  Google Scholar 

  • Stout JC, Casey LM (2014) Relative abundance of an invasive alien plant affects insect-flower interaction networks in Ireland. Acta Oecologica 55:78–85

    Article  Google Scholar 

  • Stout JC, Tiedeken EJ (2017) Direct interactions between invasive plants and native pollinators: evidence, impacts and approaches. Funct Ecol 31(1):38–46

    Article  Google Scholar 

  • Suárez-Mariño A, Arceo-Gómez G, Sosenski P, Parra-Tabla V (2019) Patterns and effects of heterospecific pollen transfer between an invasive and two native plant species: the importance of pollen arrival time to the stigma. Am J Bot 106(10):1308–1315

    Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Tiedeken EJ, Stout JC (2015) Insect-flower interaction network structure is resilient to a temporary pulse of floral resources from invasive Rhododendron ponticum. PLoS ONE 10(3):e0119733

    Article  PubMed  PubMed Central  Google Scholar 

  • Tommasi N, Biella P, Maggioni D, Fallati L, Agostinetto G, Labra M, Galimberti A (2022) DNA metabarcoding unveils the effects of habitat fragmentation on pollinator diversity, plant-pollinator interactions, and pollination efficiency in Maldive islands. Molecular Ecol 2022:1–11

    Google Scholar 

  • Traveset A, Richardson DM (2006) Biological invasions as disruptors of plant reproductive mutualisms. Trends Ecol Evol 21(4):208–216

    Article  PubMed  Google Scholar 

  • Traveset A, Richardson DM (2014) Mutualistic interactions and biological invasions. Annu Rev Ecol Evol Syst 45:89–113

    Article  Google Scholar 

  • Traveset A, Heleno R, Chamorro S, Vargas P, McMullen CK, Castro-Urgal R, Olesen JM (2013) Invaders of pollination networks in the Galápagos Islands: emergence of novel communities. Proc R Soci B Biol Sci 280(1758):20123040

    Article  Google Scholar 

  • Traveset A, Chamorro S, Olesen JM, Heleno R (2015) Space, time and aliens: charting the dynamic structure of Galápagos pollination networks. AoB Plants 7:plv068

    Article  PubMed  PubMed Central  Google Scholar 

  • Tylianakis JM, Morris RJ (2017) Ecological networks across environmental gradients. Annu Rev Ecol Evol Syst 48:25–48

    Article  Google Scholar 

  • Valdovinos FS (2019) Mutualistic networks: moving closer to a predictive theory. Ecol Lett 22(9):1517–1534

    Article  PubMed  Google Scholar 

  • Valdovinos FS, Ramos-Jiliberto R, Flores JD, Espinoza C, López G (2009) Structure and dynamics of pollination networks: the role of alien plants. Oikos 118(8):1190–1200

    Article  Google Scholar 

  • Vaughan IP, Gotelli NJ, Memmott J, Pearson CE, Woodward G, Symondson WO (2018) Econullnetr: an R package using null models to analyse the structure of ecological networks and identify resource selection. Methods Ecol Evol 9:728–733

    Article  Google Scholar 

  • 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 R Soci b: Biol Sci 276(1674):3887–3893

    Article  Google Scholar 

  • Vilà M, Espinar JL, Hejda M, Hulme PE, Jarošík V, Maron JL, Pyšek P (2011) Ecological impacts of invasive alien plants: a meta-analysis of their effects on species, communities and ecosystems. Ecol Lett 14(7):702–708

    Article  PubMed  Google Scholar 

  • Vizentin-Bugoni J, Sperry JH, Kelley JP, Gleditsch JM, Foster JT, Drake DR, Tarwater CE (2021) Ecological correlates of species’ roles in highly invaded seed dispersal networks. Proc Nat Acad Sci 118(4):e2009532118

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang X, Wen M, Qian X, Pei N, Zhang D (2020a) Plants are visited by more pollinator species than pollination syndromes predicted in an oceanic island community. Sci Rep 10(1):1–12

    CAS  Google Scholar 

  • Wang X, Zeng T, Wu M, Zhang D (2020b) Seasonal dynamic variation of pollination network is associated with the number of species in flower in an oceanic island community. J Plant Ecol 13(5):657–666

    Article  Google Scholar 

  • Wang X, Wen M, Wu M, Xu Y, Zhang K, Zhang D (2020c) Gynodioecy or leaky dioecy? The unusual sexual system of a coral dune-habitant Tournefortia argentea (Boraginaceae). Plant Syst Evol 306(4):1–11

    Article  Google Scholar 

  • Wang X, Wen M, Wu M, Zhang D (2020d) Cordia subcordata (Boraginaceae), a distylous species on oceanic coral islands, is self-compatible and pollinated by a passerine bird. Plant Ecol Evol 153(3):361–372

    Article  Google Scholar 

  • Wang X, Zeng T, Wu M, Zhang D (2021) A half-day flowering pattern helps plants sharing pollinators in an oceanic island community. J Trop Ecol 37(1):16–25

    Article  Google Scholar 

  • Zaninotto V, Thébault E, Dajoz I (2023) Native and exotic plants play different roles in urban pollination networks across seasons. Oecologia 201(2):525–536

    Article  PubMed  PubMed Central  Google Scholar 

  • Dormann CF, Fruend J, Gruber B, Dormann MC, LazyData TR, ByteCompile TR (2014) Package ‘bipartite’. Visualizing bipartite networks and calculating some (ecological) indices (Version 2.04). (R Foundation for Statistical Computing.) Available at https://cran.r-project.org/web/packages/bipartite/index.html [Verified 28 July 2015].

Download references

Acknowledgements

We thank Tong Zeng and Mingsong Wu for their worthy help in the field. We thank the logistical support on the Yongxing Island from Xisha Ocean observation and research station, South China Sea Institute of Oceanology, Chinese Academy of Sciences, Guangzhou, China. We also thank the Reviewers for their valuable suggestions. This study was supported by the National Key Research and Development Program of China (Grant number 2021YFC3100404, 2021YFC3100405), the National Natural Science Foundation of China (Grant number 32271613, 32170232), the Natural Science Foundation of Guangzhou (Grant number 202201010218) and the Science and Technology Basic Works Program of Ministry of Science and Technology of China (Grant number 2019FY202100).

Author information

Authors and Affiliations

  1. Key Laboratory of Plant Resources Conservation and Sustainable Utilization, South China Botanical Garden, The Chinese Academy of Sciences, Guangzhou, China

    Xiang-Ping Wang, Miao-Miao Shi, Zhong-Tao Zhao, Shi-Jin Li & Tie-Yao Tu

  2. South China National Botanical Garden, Guangzhou, China

    Xiang-Ping Wang, Miao-Miao Shi, Zhong-Tao Zhao, Shi-Jin Li & Tie-Yao Tu

  3. Ningxia Yunwu Mountain National Natural Reserve, Guyuan, China

    Xiao Fu

Authors
  1. Xiang-Ping Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Xiao Fu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Miao-Miao Shi
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Zhong-Tao Zhao
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Shi-Jin Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Tie-Yao Tu
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Tie-Yao Tu.

Ethics declarations

Conflict of interest

All authors declare no conflict of interest and gave final approval for publication.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wang, XP., Fu, X., Shi, MM. et al. Invasive Asteraceae plants can enhance community stability by changing pollination network structure, yet cause intense pollen disturbance to native plants in an oceanic island community. Biol Invasions 25, 3603–3618 (2023). https://doi.org/10.1007/s10530-023-03129-w

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10530-023-03129-w

Keywords

Search

Navigation