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.
Similar content being viewed by others
References
Aizen MA, Morales CL, Morales JM (2008) Invasive mutualists erode native pollination webs. PLoS Biol 6:e31
Antia R, Regoes RR, Koella JC, Bergstrom CT (2003) The role of evolution in the emergence of infectious diseases. Nature 426:658–661
Bartomeus I, Vila M, Santamaria L (2008) Contrasting effects of invasive plants in plant-pollinator networks. Oecologia 155:761–770
Bascompte J, Jordano P (2007) Plant-animal mutualistic networks: the architecture of biodiversity. Annu Rev Ecol Evol Syst 38:567–593
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
Callaway RM, Maron JL (2006) What have exotic plant invasions taught us over the past 20 years? Trends Ecol Evol 21:369–374
Clavero M, Garcia-Berthou E (2005) Invasive species are a leading cause of animal extinctions. Trends Ecol Evol 20:110
Colautti RI, Ricciardi A, Grigorovich IA et al (2004) Is invasion success explained by the enemy release hypothesis? Ecol Lett 7:721–733
Daudin JJ, Picard F, Robin S (2008) A mixture model for random graphs. Stat Comput 18:173–183
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
Desprez-Loustau ML, Robin C, Buee M et al (2007) The fungal dimension of biological invasions. Trends Ecol Evol 22:472–480
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
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
Garcia-Guzman G, Morales E (2007) Life-history strategies of plant pathogens: distribution patterns and phylogenetic analysis. Ecology 88:589–596
Hawksworth DL, Rossman AY (1997) Where are all the undescribed fungi? Phytopathology 87:888–891
Heath MC (2000) Nonhost resistance and nonspecific plant defenses. Curr Opin Plant Biol 3:315–319
Hulme PE (2006) Beyond control: wider implications for the management of biological invasions. J Appl Ecol 43:835–847
Hulme PE (2009) Trade, transport and trouble: managing invasive species pathways in an era of globalization. J Appl Ecol 46:10–18
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
Ings TC, Montoya JM, Bascompte J et al (2009) Ecological networks—beyond food webs. J Anim Ecol 78:253–269
Ives AR, Godfray HCJ (2006) Phylogenetic analysis of trophic associations. Am Nat 168:E1–E14
Keane RM, Crawley MJ (2002) Exotic plant invasions and the enemy release hypothesis. Trends Ecol Evol 17:164–170
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
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
Memmott J, Craze PG, Waser NM et al (2007) Global warming and the disruption of plant-pollinator interactions. Ecol Lett 10:710–717
Mielke PW, Berry KJ (2001) Permutation methods: a distance function approach. Springer, New York
Mitchell CE, Power AG (2003) Release of invasive plants from fungal and viral pathogens. Nature 421:625–627
Montoya JM, Rodriguez MA, Hawkins BA (2003) Food web complexity and higher-level ecosystem services. Ecol Lett 6:587–593
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
Nielsen A, Bascompte J (2007) Ecological networks, nestedness and sampling effort. J Ecol 95:1134–1141
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
Parker IM, Gilbert GS (2004) The evolutionary ecology of novel plant-pathogen interactions. Annu Rev Ecol Evol Syst 35:675–700
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
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
Prado PI, Lewinsohn TM (2004) Compartments in insect-plant associations and their consequences for community structure. J Anim Ecol 73:1168–1178
Rezende EL, Lavabre JE, Guimaraes PR et al (2007) Non-random coextinctions in phylogenetically structured mutualistic networks. Nature 448:925–928
SAS/STAT (2000) SAS Institute Inc., SAS OnlineDoc, version 8. SAS Institute Inc, Cary
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
Thompson JN (2006) Mutualistic webs of species. Science 312:372–373
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
Tylianakis JM, Tscharntke T, Lewis OT (2007) Habitat modification alters the structure of host-parasitoid food webs. Nature 445:202–205
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
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
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
Vermeij GJ (1996) An agenda for invasion biology. Biol Conserv 78:3–9
Vitousek PM, Dantonio CM, Loope LL et al (1996) Biological invasions as global environmental change. Am Sci 84:468–478
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
Worner SP, Gevrey M (2006) Modelling global insect pest species assemblages to determine risk of invasion. J Appl Ecol 43:858–867
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
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights 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
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10530-010-9719-6