Nestedness in bipartite networks of Thuja plicata, Prunus laurocerasus and Buxus sempervirens and their pathogens

Authors

  • Ecaterina Fodor Forestry Department, Faculty of Environmental Protection, University of Oradea, Romania.
  • Ovidiu Hâruţa Forestry Department, Faculty of Environmental Protection, University of Oradea, Romania.

DOI:

https://doi.org/10.15287/afr.2014.173

Keywords:

bipartite network, invasive species, pathogens, Thuja plicata, Buxus sempervirens, Prunus laurocerasus

Abstract

The trade with cultivated plants is one of the major pathways for the introduction of invasive species, pathogens included. Based on network analysis, the present study aimed the interaction between several species of cultivated woody perennials found in gardening outlets and nurseries trading with ornamental species and their documented pathogens. Focal species of the host list were Thuja plicata, Buxus sempervirens and Prunus laurocerasus, the selection being based on reported bestselling figures. Bipartite, qualitative, undirected networks were constructed to incorporate woody perennials as hosts and their documented pathogens. The tested network properties were: connectance, node degree distribution, web asymmetry and nestedness. Cluster analysis using Euclidian distance and niche overlap index of Pianka were employed as additional pattern description metrics. The main network containing 33 host species and 112 pathogens was characterized by truncated power law distribution fitting the observed degree distribution of hosts and power law distribution fitting the observed degree distribution of pathogens, low connectance (C = 0.12), intermediate web asymmetry (W = 0.54) and high significant nestedness (N = 0.94). The network containing three focal hosts showed significant lower nestedness (N = 0.54), higher asymmetry (W = 0.94) and higher connectance (C = 0.38). Cluster analysis revealed the separation of focal species distinctly, the majority of other hosts merging in one cluster. Due to the prevalence of specialized pathogens the niche breadth was narrow, with small overlap in resources’ partition (Pianka index = 0.31). Our results showed that a random assembly of hosts (woody ornamentals displayed for sale in retail centers and nurseries) could harbor pathogens which attached in a non-random manner, generating a characteristic pathosystem, with distinctive topology. The possible implications of the study consisted in a new insight in invasive spread and the inclusion of new pathogens in local pathogen communities using network analysis as a powerful investigation tool.

References

Agrawal A.F., Lively C.M., 2002. Infection genetics: Gene-for-gene versus matching allele models and all points in between. Evolutionary Ecology Research 4: 79–90. Almeida-Neto M., Guimarães Jr. P.R., Lewinsohn T.M., 2007. On nestedness analyses: rethinking matrix temperature and anti-nestedness. Oikos 116: 716–722. DOI: 10.1111/j.0030-1299.2007.15803.x. Atmar W., Patterson B.D., 1993. The measure of order and disorder in the distribution of species in fragmented habitat. Oecologia 96: 373-382. DOI: 10.1007/BF00317508. Barabási R., Albert R., 1999. Emergence of scaling in random networks. Science 286: 509-512. DOI: 10.1126/science.286.5439.509. Bascompte J., Jordano P., Melian C.J., Olesen J.M., 2003. The nested assembly of plant–animal mutualistic networks. PNAS 100: 9383–9387. DOI: 10.1073/pnas.1633576100. Bastolla U., Fortuna M.A., Pascual-Garcìa A., Ferrera A., Luque B., Bascompte J., 2009. The architecture of mutualistic networks minimizes competition and increases biodiversity. Nature 458: 1018–1020. DOI: 10.1038/nature07950. Blüthgen F., Menzel F., Hoverstadt T., Fiala B., Blüthgen N., 2007. Specialization, constraints and conflicting interests in mutualistic networks. Current Biology 17: 341-346. DOI: 10.1016/j.cub. 2006. 12.039. Blüthgen N., Fründ J., Vásquez D.P., Menzel F., 2008. What do specialization network metrics tell us about specialization and biological traits? Ecology 89(2): 3387-3399. DOI: 10.1890/07-2121.1. Borer E., 2013. Plant sharing pathogens: a recipe for successful invasion. S 2.4. in: Plant interactions with other organisms; molecules, ecology and evolution. 32rd New Phytologist Symposium. Universidad CatólicaArgentina,Buenos Aires20-22 November. Brock G., Pihur V., Datta S., Datta S., 2011. clValid: Validation of Clustering Results. R package version 0.6-4. http://CRAN.R-project.org/package=clValid. Burns K.C., 2007. Network properties of an epiphyte metacommunity. Journal of Ecology 95(5): 1142-1151. DOI: 10.1111/j.1365-2745.2007. 01267.x. Colwell R.K., Futuyma D.J., 1971. On the measurement of niche breadth and overlap. Ecology 52(4): 567-576. DOI: 10.2307/1934144. Csardi G. Nepusz T.,2006. The igraph software package for complex network research, InterJournal, Complex Systems 1695. http://igraph.org. Dale M.R.T., Fortin M.J., 2010. From graphs to spatial graphs. Annual Review of Ecology, Evolution and Systematics 42: 21-38. DOI: 10.1146/annurev-ecolsys-102209-144718. Desprez-Lousteau M.L., Robin C., Buee M., Courtecuisse R., Garbaye J., Suffert F., Sache I., Rizzo D.M., 2007. The fungal dimension of biological invasions. Trends in Ecology and Evolution 22: 472-480. DOI: 10.1016/j.tree.2007.04.005. Dormann C.F., Gruber B., Fruend J., 2008. Introducing the bipartite Package: Analysing Ecological Networks. R news Vol 8/2, 8 - 11. Dunne J.A., Lafferty K.D., Dobson A.P., Hechinger R.F., Kuris A.M., et al., 2013. Parasites Affect Food Web Structure Primarily through Increased Diversity and Complexity. PLOS Biology 11(6): e1001579. doi:10.1371/journal.pbio.1001579. DOI: 10.1371/journal.pbio.1001579. Dunne J.A., Williams R.J., MartinezN.D., 2002. Network structure and biodiversity loss in food webs: robustness increases with connectance. Ecology Letters 5:558-567. DOI: 10.1046/j.1461-0248.2002.00354.x. Epps M.J., Arnold A.E., 2010. Diversity, abundance and community network structure in sporocarp associated beetle communities in Appalachian Mountains. Mycologia 102(4): 785-802. DOI: 10.3852/09-161. Fenner A.L., Godfrey S.S., Bull M.C., 2011. Using social networks to deduce whether residents or dispersers spread parasites in a lizard population. Journal of Animal Ecology 80: 835-843. DOI: 10.1111/ j. 1365-2656.2011.01825.x. FloresC.O., Meyer J.R., Valverde S., Farr L., Weitz J.S., 2011. Statistical structure of host-phage interaction. PNAS 108(28): E288-E297. DOI: 10.1073/pnas.1101595108. Garcia-Guzman G., Morales E., 2007. Life-history of plant pathogens. Distribution patterns and phylogenetic analysis. Ecology 88: 589- 596. DOI: 10.1890/05-1174. GotelliN.J., 2001. Research frontiers in null model analysis. Global Ecology and Biogeography 10(4): 337-343. DOI: 10.1046/j.1466-822X.2001.00249.x. Gotelli N.J., Entsminger G.L., 2004. EcoSim: Null models software for ecology. Version 7.0. Acquired Intelligence Inc. & Kesey-Bear. Jericho,VT05465. Available online at: http: //garyentsminger.com /ecosim/index.htm. GotelliN.J.,GravesG.R., 1996. Null models in ecology. Smithsonian Institution Press,Washington,D.C., U.S A. Graham S.P., Hassan H.K., Burkett-CadenaN.D., Guyer C., Unnasch T.R., 2009. Nestedness of ectoparasite-vertebrate host networks. PLOS ONE 4(1): e7873. DOI: 10.1371/journal.pone.0007873. GriffithE.C., Pedersen A.B., Fenton A., Petchey O.L., 2014. Analysis of a summary network of co-infection in humans reveals that parasites interact most via shared resources. Proceedings of the Royal Society B. 281: 20132286. DOI: 10.1098/rspb.2013.2286. Guimarães P.R. Jr., Sazima C., Furtado dos Reis S., SazimaI., 2006. The nested structure of marine cleaning symbioses: is it like fl owers and bees? Biology Letters 3(1): 51-54. DOI: 10.1098/rsbl.2006.0562. Hall G., Cook R.T.H., Bradshaw W.J., 1992. First record of Peronospora sparsa on Prunus laurocerasus. Plant Pathology 4(2): 224/227. Harris M.O., Stuart J.J., Mohan M., Nair S., Lamb R.J., Rohfritsch O., 2003. Grasses and gall midges: plant defense and insect adaptation. Annual Review of Entomology 48: 549–577. DOI: 10.1146/ annurev. ento.48.091801.112559. Hespenheide H.A., 1991. Bionomics of leaf-mining insects. Annual Review of Entomology 36: 535–560. DOI: 10.1146/annurev.en.36. 010191.002535. Jordano P., Bascompte J., Olesen J.M., 2003. Invariant properties in co-evolutionary networks of plant-animal interactions. Ecology Letters 6: 69-81. DOI: 10.1046/j.1461-0248.2003.00403.x. Jordano P., Bascompte J., Olesen J.M., 2006. The ecological consequences of complex topology and nested structure in pollination webs. In:WaserNM, Ollerton J (Eds.), Plant–Pollinator Interactions: From specialization to Generalization. University Presses Marketing,Bristol, (Chapter 8): 173–199. Keller R.P., Geist J., Jeschke J.M., KühnI., 2011. Invasive species in Europe: ecology, status and policy. Environmental Sciences Europe23:23. DOI: 10.1186/2190-4715-23-23. Kondoh M., Kato S., Sakato Y., 2010. Food webs are built up with nested subwebs. Ecology 91: 3123–3130. DOI: 10.1890/09-2219.1. La Porta N., Capretti P., Thomsen I.M., Kasanene R., Hietala A.M., von Weissenberg K., 2008. Forest pathogens with higher damage potential due to climate change in Europe. Canadian Journal of Plant Pathology 30: 177-195. DOI: 10.1080/07060661.2008.10540534. Lafferty K.D., Dobson A.P., Kuris A.M., 2006. Parasites dominate food web links. PNAS 103 (3): 11311-11216. May R.M., 1972. Stability and complexity in model ecosystems. Princeton University Press. 292pp. Memmott J., 1999. The structure of a plant-pollinator food web. Ecology Letters 2: 276–280. DOI: 10.1046/j.1461-0248.1999.00087.x. Montoya J.M., Pimm S.L., Solé R.V., 2006. Ecological networks and their fragility. Nature 442: 259–264. DOI: 10.1038/nature04927. Nielsen A., Bascompte J., 2007. Ecological networks nestedness and sampling effort. Journal of Ecology 95: 1134-1141. DOI: 10.1111/j. 1365-2745.2007.01271.x. Oksanen J., Blanchet F.G., Kindt R., Legendre P., Peter R., Minchin R., O'Hara B., Simpson G.L., Solymos P., Henry M., Stevens H., Wagner H., 2013. vegan: Community Ecology Package. R package version 2.0-10. http://CRAN.R-project.org/package=vegan. Pautasso M., Moslonka-Lefebvre M., Jeger M.J., 2010. The number of links to and from the starting node as a predictor of epidemic size in small-size directed networks. Ecological Complexity 7: 424-432. DOI: 10.1016/j.ecocom.2009.10.003. Pianka E.R., 1974. Niche overlap and diffuse competition. PNAS 71(5): 2141-2145. DOI: 10.1073/pnas.71.5.2141. Piazzon M., Larrinaga A.R., Santamaria L., 2011. Are nested networks more robust to disturbance? A test using epiphyte-tree commensalistic networks. PLOS ONE 6(5); e19637. DOI: 10.1371/journal.pone. 0019637. Podani J., 2000. Introduction to the exploration of multivariate biological data. Backhuys Publishers,Leiden, TheNetherlands. 407 pp. Poisot T., Stanko M., Miklisova D., Morand S., 2013. Facultative and obligate parasite communities exhibit different network properties. Parasitology 140(11): 1340/1345. Poulin R., 1997. Parasite faunas of freshwater fish: the relationship between richness and the specificity of parasites. International Journal for Parasitology 27(9): 1091–1098. DOI: 10.1016/S0020-7519(97) 00070-2. Poulin R., 2010. Network analysis shining light on parasite ecology and diversity. Trends in Parasitology 26(10): 492-498. DOI: 10.1016/j.pt. 2010.05.008 R Development Core Team, 2013. R: A language and environment for statistical computing. R Foundation for Statistical Computing,Vienna,Austria. URL http://www.R-project.org/. Rodríguez-Gironés M.A., Santamaría L., 2006. Anew algorithm to calculate the nestedness temperature of presence-absence matrices. Journal of Biogeography 33: 924-935. DOI: 10.1111/j.1365-2699. 2006.01444.x. Romanuk T.N., Zhou Y., Brose U., Berlow E.L., Williams R.D., MartinezN.D., 2009. Predicting invasion success in complex ecological networks. Philosophical Transactions of the Royal Society B 364: 1743-1754. DOI: 10.1098/rstb.2008.0286. Sachs J.L., Essenberg C.J., Turcotte M.M., 2011. New paradigms for the evolution of beneficial infections. Trends in Ecology & Evolution 26: 202–209. DOI: 10.1016/j.tree.2011.01.010. Santini A., Ghelardini L., De Pace C., Desprez-Loustau M.L., Capretti P., Chandelier A., Cech T., Chira D., Diamandis S., Gaitniekis T., et al. 2013. Biogeographical patterns and determinants of invasion by forest pathogens in Europe. New Phytologist. 197: 238-250. DOI: 10.1111/j. 1469-8137.2012.04364.x. Thompson J.N., 1994. The coevolutionary process. Universityof ChicagoPress, Chicago. 383 pp. DOI: 10.7208/chicago/978022679 7670.001.0001. Tjou-Sin N.N.A., van de Bilt J.L.J., Bergsma-Vlami M., 2012. First report of Xanthomonas arboricola pv. pruni in ornamental Prunus laurocerasus. Plant Disease 96(5): 779. Ulrich W., GotelliN.J., 2007. Null model analysis of species nestedness patterns. Ecology 88: 1824–1831. DOI: 10.1890/06-1208.1. Vacher C., Piou D., Desprez-Loustau M.L., 2008. Architecture of an Antagonistic Tree/Fungus Network: The Asymmetric Influence of Past Evolutionary History. PLOS ONE 3(3): e1740. doi:10.1371/journal. pone.0001740. DOI: 10.1371/journal.pone.0001740. Vasas V., Jordán F., 2006. Topological keystone species in ecological interaction networks: Considering link quality and non-trophic effects. Ecological Modelling 25(3-4): 365-378. DOI: 10.1016/j.ecolmodel. 2006.02.024. Vásquez D.P., 2005. Degree distribution in plant-animal mutualistic networks: forbidden links or random interactions? Oikos 108(2): 421- 426. DOI: 10.1111/j.0030-1299.2005.13619.x Vásquez D.P., Poulin R., Krasnov B.R., Shenbrot G.I., 2005. Species abundance patterns and the distribution of specialization in host-parasite interaction networks. Journal of Animal Ecology 7(5): 946-955. DOI: 10.1111/j.1365-2656.2005.00992.x. Wallace A.R., 1878. Tropical Nature, and Other Essays. Macmillan & Co.,LondonandNew York. i-(xvi), 1-356 pp. Williams R.J., 2011. Biology, Methodology or Chance? The Degree Distributions of Bipartite Ecological Networks. PLOS ONE 6(3): e17645. DOI: 10.1371/journal.pone.0017645.

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2014-04-30

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Research article