Skip to main content
Log in

Ecological integration of alien species into a tree-parasitic fungus network

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

Abstract

The diversification of species and their interactions during the course of evolution has produced ecological networks with a complex topology. This topology influences the current functioning of ecosystems. It is therefore important to investigate whether the species introduced recently by human activities have merged seamlessly into recipient ecological networks by developing interactions quantitatively and qualitatively similar to those of native species, or whether their establishment has altered the topology of the networks. We tackled this issue in the case of a well resolved interaction network between 51 forest tree taxa and 154 pathogenic fungal species. We found that alien and native species with similar phylogenetic histories and life-history strategies had similar types and numbers of interactions. Our results also suggest that the clustered architecture of the network has not been altered by the integration of alien species. It therefore seems that a few centuries have been sufficient for the network to assimilate the newly introduced species. This rapid integration was unexpected for a plant-pathogen network, because selection acts continually on plants, favouring the emergence of defences against new pathogens and impeding the development of new interactions. However, it was recently shown that perturbation of the structure of ecological networks might be overlooked if species interactions are not quantified. The tree-parasitic fungus network considered in this study is binary. We might therefore end up with different results by using quantitative data.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

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

    Article  PubMed  Google Scholar 

  • Antia R, Regoes RR, Koella JC, Bergstrom CT (2003) The role of evolution in the emergence of infectious diseases. Nature 426:658–661

    Article  CAS  PubMed  Google Scholar 

  • Bartomeus I, Vila M, Santamaria L (2008) Contrasting effects of invasive plants in plant-pollinator networks. Oecologia 155:761–770

    Article  PubMed  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 

  • Bertheau C, Brockerhoff EG, Roux-Morabito G, Lieutier F, Jactel H (2010). Novel insect-tree associations resulting from accidental and intentional biological ‘invasions’: a meta-analysis of effects on insect fitness. Ecol Lett (in press)

  • Bluthgen N, Frund J, Vazquez DP et al (2008) What do interaction network metrics tell us about specialization and biological traits? Ecology 89:3387–3399

    Article  PubMed  Google Scholar 

  • Callaway RM, Maron JL (2006) What have exotic plant invasions taught us over the past 20 years? Trends Ecol Evol 21:369–374

    Article  PubMed  Google Scholar 

  • Clavero M, Garcia-Berthou E (2005) Invasive species are a leading cause of animal extinctions. Trends Ecol Evol 20:110

    Article  PubMed  Google Scholar 

  • Colautti RI, Ricciardi A, Grigorovich IA et al (2004) Is invasion success explained by the enemy release hypothesis? Ecol Lett 7:721–733

    Article  Google Scholar 

  • Daudin JJ, Picard F, Robin S (2008) A mixture model for random graphs. Stat Comput 18:173–183

    Article  Google Scholar 

  • Desprez-Loustau ML (2009) The alien fungi of Europe. In: Nentwig W, Hulme P, Pysek P, Vila M (eds) Handbook of alien species in Europe. Springer, Berlin, p 400

    Google Scholar 

  • Desprez-Loustau ML, Robin C, Buee M et al (2007) The fungal dimension of biological invasions. Trends Ecol Evol 22:472–480

    Article  PubMed  Google Scholar 

  • Desprez-Loustau ML, Courtecuisse R, Robin C et al (2010) Species diversity and drivers of spread of alien fungi in Europe with a particular focus on France. Biol Invasions 12:157–172

    Article  Google Scholar 

  • Dobson A, Lafferty KD, Kuris AM et al (2008) Homage to Linnaeus: how many parasites? How many hosts? Proc Natl Acad Sci USA 105:11482–11489

    Article  CAS  PubMed  Google Scholar 

  • Garcia-Guzman G, Morales E (2007) Life-history strategies of plant pathogens: distribution patterns and phylogenetic analysis. Ecology 88:589–596

    Article  PubMed  Google Scholar 

  • Hawksworth DL, Rossman AY (1997) Where are all the undescribed fungi? Phytopathology 87:888–891

    Article  CAS  PubMed  Google Scholar 

  • Heath MC (2000) Nonhost resistance and nonspecific plant defenses. Curr Opin Plant Biol 3:315–319

    Article  CAS  PubMed  Google Scholar 

  • Hulme PE (2006) Beyond control: wider implications for the management of biological invasions. J Appl Ecol 43:835–847

    Article  Google Scholar 

  • Hulme PE (2009) Trade, transport and trouble: managing invasive species pathways in an era of globalization. J Appl Ecol 46:10–18

    Article  Google Scholar 

  • Hulme PE, Bacher S, Kenis M et al (2008) Grasping at the routes of biological invasions: a framework for integrating pathways into policy. J Appl Ecol 45:403–414

    Article  Google Scholar 

  • Ings TC, Montoya JM, Bascompte J et al (2009) Ecological networks—beyond food webs. J Anim Ecol 78:253–269

    Article  PubMed  Google Scholar 

  • Ives AR, Godfray HCJ (2006) Phylogenetic analysis of trophic associations. Am Nat 168:E1–E14

    Article  CAS  PubMed  Google Scholar 

  • Keane RM, Crawley MJ (2002) Exotic plant invasions and the enemy release hypothesis. Trends Ecol Evol 17:164–170

    Article  Google Scholar 

  • Lopezaraiza-Mikel ME, Hayes RB, Whalley MR et al (2007) The impact of an alien plant on a native plant-pollinator network: an experimental approach. Ecol Lett 10:539–550

    Article  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • Memmott J, Craze PG, Waser NM et al (2007) Global warming and the disruption of plant-pollinator interactions. Ecol Lett 10:710–717

    Article  PubMed  Google Scholar 

  • Mielke PW, Berry KJ (2001) Permutation methods: a distance function approach. Springer, New York

    Google Scholar 

  • Mitchell CE, Power AG (2003) Release of invasive plants from fungal and viral pathogens. Nature 421:625–627

    Article  CAS  PubMed  Google Scholar 

  • Montoya JM, Rodriguez MA, Hawkins BA (2003) Food web complexity and higher-level ecosystem services. Ecol Lett 6:587–593

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Nielsen A, Bascompte J (2007) Ecological networks, nestedness and sampling effort. J Ecol 95:1134–1141

    Article  Google Scholar 

  • Oksanen J, Kindt R, Legendre P et al (2006) Vegan: community ecology package version 1.8-3. R package URL http://www.R-project.org

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

    Article  Google Scholar 

  • Parker IM, Gilbert GS (2004) The evolutionary ecology of novel plant-pathogen interactions. Annu Rev Ecol Evol Syst 35:675–700

    Article  Google Scholar 

  • Petit RJ, Bialozyt R, Garnier-Gere P et al (2004) Ecology and genetics of tree invasions: from recent introductions to Quaternary migrations. For Ecol Manag 197:117–137

    Article  Google Scholar 

  • Picard F, Miele V, Daudin JJ, et al (2009) Deciphering the connectivity structure of biological networks using MixNet. BMC Bioinformatics

  • Pimentel D, Lach L, Zuniga R et al (2000) Environmental and economic costs of nonindigenous species in the United States. Bioscience 50:53–65

    Article  Google Scholar 

  • Prado PI, Lewinsohn TM (2004) Compartments in insect-plant associations and their consequences for community structure. J Anim Ecol 73:1168–1178

    Article  Google Scholar 

  • Rezende EL, Lavabre JE, Guimaraes PR et al (2007) Non-random coextinctions in phylogenetically structured mutualistic networks. Nature 448:925–928

    Article  CAS  PubMed  Google Scholar 

  • SAS/STAT (2000) SAS Institute Inc., SAS OnlineDoc, version 8. SAS Institute Inc, Cary

    Google Scholar 

  • Sugiura S, Yamaura Y, Makihara H (2008) Biological invasion into the nested assemblage of tree-beetle associations on the oceanic Ogasawara Islands. Biol Invasions 10:1061–1071

    Article  Google Scholar 

  • Thompson JN (2006) Mutualistic webs of species. Science 312:372–373

    Article  CAS  PubMed  Google Scholar 

  • Thuiller W, Richardson DM, Pysek P et al (2005) Niche-based modelling as a tool for predicting the risk of alien plant invasions at a global scale. Global Change Biol 11:2234–2250

    Article  Google Scholar 

  • Tylianakis JM, Tscharntke T, Lewis OT (2007) Habitat modification alters the structure of host-parasitoid food webs. Nature 445:202–205

    Article  CAS  PubMed  Google Scholar 

  • Vacher C, Piou D, Desprez-Loustau M-L (2008a) Architecture of an antagonistic tree/fungus network: the asymmetric influence of past evolutionary history. PLoS ONE 3:e1740

    Article  PubMed  Google Scholar 

  • Vacher C, Vile D, Helion E et al (2008b) Distribution of parasitic fungal species richness: influence of climate versus host species diversity. Divers Distrib 14:786–798

    Article  Google Scholar 

  • Valéry L, Fritz H, Lefeuvre J-C et al (2008) In search of a real definition of the biological invasion phenomenon itself. Biol Invasions 10:1345–1351

    Article  Google Scholar 

  • Vermeij GJ (1996) An agenda for invasion biology. Biol Conserv 78:3–9

    Article  Google Scholar 

  • Vitousek PM, Dantonio CM, Loope LL et al (1996) Biological invasions as global environmental change. Am Sci 84:468–478

    Google Scholar 

  • Wilson JB, Steel JB, Dodd ME et al (2000) A test of community reassembly using the exotic communities of New Zealand roadsides in comparison to British roadsides. J Ecol 88:757–764

    Article  Google Scholar 

  • Worner SP, Gevrey M (2006) Modelling global insect pest species assemblages to determine risk of invasion. J Appl Ecol 43:858–867

    Article  Google Scholar 

Download references

Acknowledgments

We thank the Département Santé des Forêts (DSF) for allowing us to use their database and the French research consortium Interactions Biotiques dans les communautés (GDR ComEvol) for funding. We also thank Julie Sappa (Alex Edelman & Associates) for language revision.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Corinne Vacher.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 20 kb)

Supplementary material 2 (PDF 34 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Vacher, C., Daudin, JJ., Piou, D. et al. Ecological integration of alien species into a tree-parasitic fungus network. Biol Invasions 12, 3249–3259 (2010). https://doi.org/10.1007/s10530-010-9719-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10530-010-9719-6

Keywords

Navigation