, Volume 180, Issue 1, pp 181–191 | Cite as

Interaction type influences ecological network structure more than local abiotic conditions: evidence from endophytic and endolichenic fungi at a continental scale

  • Pierre-Luc ChagnonEmail author
  • Jana M. U’Ren
  • Jolanta Miadlikowska
  • François Lutzoni
  • A. Elizabeth Arnold
Plant-microbe-animal interactions - Original research


Understanding the factors that shape community assembly remains one of the most enduring and important questions in modern ecology. Network theory can reveal rules of community assembly within and across study systems and suggest novel hypotheses regarding the formation and stability of communities. However, such studies generally face the challenge of disentangling the relative influence of factors such as interaction type and environmental conditions on shaping communities and associated networks. Endophytic and endolichenic symbioses, characterized by microbial species that occur within healthy plants and lichen thalli, represent some of the most ubiquitous interactions in nature. Fungi that engage in these symbioses are hyperdiverse, often horizontally transmitted, and functionally beneficial in many cases, and they represent the diversification of multiple phylogenetic groups. We evaluated six measures of ecological network structure for >4100 isolates of endophytic and endolichenic fungi collected systematically from five sites across North America. Our comparison of these co-occurring interactions in biomes ranging from tundra to subtropical forest showed that the type of interactions (i.e., endophytic vs. endolichenic) had a much more pronounced influence on network structure than did environmental conditions. In particular, endophytic networks were less nested, less connected, and more modular than endolichenic networks in all sites. The consistency of the network structure within each interaction type, independent of site, is encouraging for current efforts devoted to gathering metadata on ecological network structure at a global scale. We discuss several mechanisms potentially responsible for such patterns and draw attention to knowledge gaps in our understanding of networks for diverse interaction types.


Biogeography Ecological networks Endolichenic fungi Endophytic fungi Symbiosis 



For financial support we thank the National Science Foundation (DEB-0640996 and DEB-1045766 to AEA; DEB-0640956 and DEB-1046065 to FL), and the College of Agriculture and Life Sciences and School of Plant Sciences at The University of Arizona. PLC was funded by a Vanier Canada PhD scholarship.

Author contribution statement

JMU, AEA, JM, and FL designed and performed the sampling; PLC designed and performed numerical analyses; PLC wrote a first draft of the manuscript; all authors contributed to revisions.

Supplementary material

442_2015_3457_MOESM1_ESM.pptx (47 kb)
Supplementary material 1 (PPTX 47 kb)
442_2015_3457_MOESM2_ESM.xlsx (63 kb)
Supplementary material 2 (XLSX 63 kb)
442_2015_3457_MOESM3_ESM.xlsx (60 kb)
Supplementary material 3 (XLSX 59 kb)
442_2015_3457_MOESM4_ESM.pptx (99 kb)
Supplementary material 4 (PPTX 99 kb)
442_2015_3457_MOESM5_ESM.pptx (346 kb)
Supplementary material 5 (PPTX 346 kb)
442_2015_3457_MOESM6_ESM.xlsx (13 kb)
Supplementary material 6 (XLSX 12 kb)
442_2015_3457_MOESM7_ESM.xlsx (14 kb)
Supplementary material 7 (XLSX 13 kb)
442_2015_3457_MOESM8_ESM.xlsx (42 kb)
Supplementary material 8 (XLSX 42 kb)


  1. Albrecht M, Riesen M, Schmid B (2010) Plant-pollinator network assembly along the chronosequence of a glacier foreland. Oikos 119:1610–1624. doi: 10.1111/j.1600-0706.2010.18376.x CrossRefGoogle Scholar
  2. Allen TR, Millar T, Berch SA, Berbee ML (2003) Culturing and direct DNA extraction find different fungi from the same ericoid mycorrhizal roots. New Phytol 160:255–272. doi: 10.1046/j.1469-8137.2003.00885.x CrossRefGoogle Scholar
  3. Almeida-Neto M, Guimarães P, Guimarães PR Jr, Loyola RD, Ulrich W (2008) A consistent metric for nestedness analysis in ecological systems: reconciling concept and measurement. Oikos 117:1227–1239. doi: 10.1111/j.0030-1299.2008.16644.x CrossRefGoogle Scholar
  4. Arnold AE, Herre EA (2003) Canopy cover and leaf age affect colonization by tropical fungal endophytes: ecological pattern and process in Theobroma cacao (Malvaceae). Mycologia 95:388–398CrossRefPubMedGoogle Scholar
  5. Arnold AE, Lutzoni F (2007) Diversity and host range of foliar fungal endophytes: are tropical leaves biodiversity hotspots? Ecology 88:541–549. doi: 10.1890/05-1459 CrossRefPubMedGoogle Scholar
  6. Arnold AE, Henk DA, Eells RL, Lutzoni F, Vilgalys R (2007) Diversity and phylogenetic affinities of foliar fungal endophytes in loblolly pine inferred by culturing and environmental PCR. Mycologia 99:185–206. doi: 10.3852/mycologia.99.2.185 CrossRefPubMedGoogle Scholar
  7. Arnold AE, Miadlikowska J, Higgins KL, Sarvate SD, Gugger P, Way A, Hofstetter V, Kauff F, Lutzoni F (2009) A phylogenetic estimation of trophic transition networks for ascomycetous fungi: are lichens cradles of symbiotrophic fungal diversification? Syst Biol 58:283–297. doi: 10.1093/sysbio/syp001 CrossRefPubMedGoogle Scholar
  8. Atmar W, Patterson B (1993) The measure of order and disorder in the distribution of species in fragmented habitat. Oecologia 96:373–382. doi: 10.1007/BF00317508 CrossRefGoogle Scholar
  9. Barber M (2007) Modularity and community detection in bipartite networks. Phys Rev E 76:066102. doi: 10.1103/PhysRevE.76.066102 CrossRefGoogle Scholar
  10. Bascompte J, Jordano P, Melián CJ, Olesen JM (2003) The nested assembly of plant-animal mutualistic networks. Proc Natl Acad Sci USA 100:9383–9387. doi: 10.1073/pnas.1633576100 CrossRefPubMedPubMedCentralGoogle Scholar
  11. Bascompte J, Jordano P, Olesen JM (2006) Asymmetric coevolutionary networks facilitate biodiversity maintenance. Science 312:431–433. doi: 10.1126/science.1123412 CrossRefPubMedGoogle Scholar
  12. Beiler KJ, Durall DM, Simard SW, Maxwell SA, Kretzer AM (2010) Architecture of the wood-wide web: Rhizopogon spp. genets link multiple Douglas-fir cohorts. New Phytol 185:543–553. doi: 10.1111/j.1469-8137.2009.03069.x CrossRefPubMedGoogle Scholar
  13. Blüthgen N, Fründ J, Vázquez DP, Menzel F (2008) What do interaction network metrics tell us about specialization and biological traits. Ecology 89:3387–3399. doi: 10.1890/07-2121.1 CrossRefPubMedGoogle Scholar
  14. Bougoure DS, Cairney JW (2005) Fungi associated with hair roots of Rhododendron lochiae (Ericaceae) in an Australian tropical cloud forest revealed by culturing and culture-independent molecular methods. Environ Microbiol 7:1743–1754. doi: 10.1111/j.1462-2920.2005.00919.x CrossRefPubMedGoogle Scholar
  15. Chagnon P, Bradley R, Klironomos J (2012) Using ecological network theory to evaluate the causes and consequences of arbuscular mycorrhizal community structure. New Phytol 194:307–312. doi: 10.1111/j.1469-8137.2011.04044.x CrossRefPubMedGoogle Scholar
  16. Chagnon PL, Bradley RL, Maherali H, Klironomos JN (2013) A trait-based framework to understand life history of mycorrhizal fungi. Trends Plant Sci 18:484–491. doi: 10.1016/j.tplants.2013.05.001 CrossRefPubMedGoogle Scholar
  17. Cohen JE (1978) Food webs and niche space. Princeton University Press, PrincetonGoogle Scholar
  18. Connor E, Collins M, Simberloff D (2013) The checkered history of checkerboard distributions. Ecology 94:2403–2414. doi: 10.1890/12-1471.1 CrossRefPubMedGoogle Scholar
  19. Diamond JM (1975) Assembly of species communities. In: Cody ML, Diamon JM (eds) Ecology and evolution of communities. Belknap Press, Cambridge, pp 342–444Google Scholar
  20. Dormann C, Fründ J, Blüthgen N, Gruber B (2009) Indices, graphs and null models: analyzing bipartite ecological networks. Open Ecol J 2:7–24. doi: 10.2174/1874213000902010007 CrossRefGoogle Scholar
  21. Elias M, Fontaine C, van Veen FJF (2013) Evolutionary history and ecological processes shape a local multilevel antagonistic network. Curr Biol 23:1355–1359. doi: 10.1016/j.cub.2013.05.066 CrossRefPubMedGoogle Scholar
  22. Epps MJ, Arnold AE (2010) Diversity, abundance and community network structure in sporocarp-associated beetle communities of the central Appalachian Mountains. Mycologia 102:785–802. doi: 10.3852/09-161 CrossRefPubMedGoogle Scholar
  23. Fontaine C, Guimarães P, Kéfi S, Loeuille N, Memmott J, van der Putten WH, van Veen FJF, Thébault E (2011) The ecological and evolutionary implications of merging different types of networks. Ecol Lett 14:1170–1181. doi: 10.1111/j.1461-0248.2011.01688.x CrossRefPubMedGoogle Scholar
  24. Freeman LC (1977) A set of measures of centrality based on betweenness. Sociometry 40:35–41. doi: 10.2307/3033543 CrossRefGoogle Scholar
  25. Friesen ML, Porter SS, Stark SC, von Wettberg EJ, Sachs JL, Martinez-Romero E (2011) Microbially mediated plant functional traits. Annu Rev Evol Evol Syst 42:23–46. doi: 10.1146/annurev-ecolsys-102710-145039 CrossRefGoogle Scholar
  26. Gilbert G, Webb C (2007) Phylogenetic signal in plant pathogen–host range. Proc Natl Acad Sci USA 104:4979–4983. doi: 10.1073/pnas.0607968104 CrossRefPubMedPubMedCentralGoogle Scholar
  27. Gotelli N, Rohde K (2002) Co-occurrence of ectoparasites of marine fishes: a null model analysis. Ecol Lett 5:86–94. doi: 10.1046/j.1461-0248.2002.00288.x CrossRefGoogle Scholar
  28. Guimarães P, Rico-Gray V, dos Reis S, Thompson JN (2006) Asymmetries in specialization in ant–plant mutualistic networks. Proc R Soc B 273:2041–2047. doi: 10.1098/rspb.2006.3548 CrossRefPubMedPubMedCentralGoogle Scholar
  29. Guimarães P Jr, Rico-Gray V, Oliveira P, Izzo TJ, dos Reis SF, Thompson JN (2007) Interaction intimacy affects structure and coevolutionary dynamics in mutualistic networks. Curr Biol 17:1797–1803. doi: 10.1016/j.cub.2007.09.059 CrossRefPubMedGoogle Scholar
  30. Higgins KL, Coley PD, Kursar TA, Arnold AE (2011) Culturing and direct PCR suggest prevalent host generalism among diverse fungal endophytes of tropical forest grasses. Mycologia 103:247–260. doi: 10.3852/09-158 CrossRefPubMedGoogle Scholar
  31. Johnson NC, Wilson GW, Bowker MA, Wilson JA, Miller RM (2010) Resource limitation is a driver of local adaptation in mycorrhizal symbioses. Proc Natl Acad Sci USA 107:2093–2098. doi: 10.1073/pnas.0906710107 CrossRefPubMedPubMedCentralGoogle Scholar
  32. Jordano P (1987) Patterns of mutualistic interactions in pollination and seed dispersal: connectance, dependence asymmetries, and coevolution. Am Nat 129:657–677. doi: 10.1086/284665 CrossRefGoogle Scholar
  33. Jordano P, Bascompte J, Olesen J (2003) Invariant properties in coevolutionary networks of plant–animal interactions. Ecol Lett 6:69–81. doi: 10.1046/j.1461-0248.2003.00403.x CrossRefGoogle Scholar
  34. Lewinsohn T, Prado PI, Jordano P, Bascompte J, Olesen JM (2006) Structure in plant–animal interaction assemblages. Oikos 113:174–184. doi: 10.1111/j.0030-1299.2006.14583.x CrossRefGoogle Scholar
  35. Marquitti FMD, Guimarães PR, Pires MM, Bittencourt LF (2014) MODULAR: software for the autonomous computation of modularity in large network sets. Ecography 37:221–224. doi: 10.1111/j.1600-0587.2013.00506.x CrossRefGoogle Scholar
  36. Martos F, Munoz F, Pailler T, Kottke I, Gonneau C, Selosse MA (2012) The role of epiphytism in architecture and evolutionary constraint within mycorrhizal networks of tropical orchids. Mol Ecol 21:5098–5109. doi: 10.1111/j.1365-294X.2012.05692.x CrossRefPubMedGoogle Scholar
  37. McGill B, Etienne RS, Gray JS, Alonso D, Anderson MJ, Benetcha HK, Dornelas M, Enquist BJ, Green JL, He F, Hurlbert AH, Magurran AE, Marquet PA, Maurer BA, Ostling A, Soykan CU, Ugland KI, White EP (2007) Species abundance distributions : moving beyond single prediction theories to integration within an ecological framework. Ecol Lett 10:995–1015. doi: 10.1111/j.1461-0248.2007.01094.x CrossRefPubMedGoogle Scholar
  38. Miadlikowska J, Kauff F, Hofstetter V, Fraker E, Grube M, Hafellner J (2006) New insights from nuclear ribosomal and protein coding genes into classification and evolution of the Lecanoromycetes (Pezizomycotina, Ascomycota). Mycologia 98:1088–1103. doi: 10.3852/mycologia.98.6.1088 CrossRefPubMedGoogle Scholar
  39. Oksanen J, Blanchet G, Kindt R et al (2013) Vegan: Community Ecology Package. R package version 2.0–8. Available at: Accessed Aug 2013
  40. Olesen J, Jordano P (2002) Geographic patterns in plant-pollinator mutualistic networks. Ecology 83:2416–2424. doi: 10.2307/3071803 Google Scholar
  41. Patterson BD, Atmar W (1986) Nested subsets and the structure of insular mammalian faunas and archipelagos. In: Heaney LR, Patterson BD (eds) Island biogeography of mammals. Academic Press, Waltham, pp 65–82Google Scholar
  42. Pimm SL, Lawton JH, Cohen JE (1991) Food web patterns and their consequences. Nature 350:669–674. doi: 10.1038/350669a0 CrossRefGoogle Scholar
  43. Platt J (1964) Strong inference. Science 146:347–353. doi: 10.1126/science.146.3642.347 CrossRefPubMedGoogle Scholar
  44. Podani J, Schmera D (2012) A comparative evaluation of pairwise nestedness measures. Ecography 35:889–900. doi: 10.1111/j.1600-0587.2011.07319.x CrossRefGoogle Scholar
  45. Ramos-Jiliberto R, Domínguez D, Espinoza C, Lopez G, Valdovinos FS, Bustamante RO, Medel R (2010) Topological change of Andean plant–pollinator networks along an altitudinal gradient. Ecol Complex 7:86–90. doi: 10.1016/j.ecocom.2009.06.001 CrossRefGoogle Scholar
  46. Rodriguez RJ, White JF Jr, Arnold AE, Redman RS (2009) Fungal endophytes: diversity and functional roles. New Phytol 182:314–330. doi: 10.1111/j.1469-8137.2009.02773.x CrossRefPubMedGoogle Scholar
  47. Stone L, Roberts A (1990) The checkerboard score and species distributions. Oecologia 85:74–79. doi: 10.1007/BF00317345 CrossRefGoogle Scholar
  48. Tedersoo L, Bahram M, Põlme S et al (2014) Global diversity and geography of soil fungi. Science 346:1256688. doi: 10.1126/science.1256688 CrossRefPubMedGoogle Scholar
  49. Thébault E, Fontaine C (2010) Stability of ecological communities and the architecture of mutualistic and trophic networks. Science 329:853–856. doi: 10.1126/science.1188321 CrossRefPubMedGoogle Scholar
  50. Thompson JN (2005) The geographic mosaic of coevolution. The University of Chicago Press, ChicagoGoogle Scholar
  51. U’Ren JM (2011) Host-, geographic-, and ecological specificity of endophytic and endolichenic fungal communities. PhD thesis. The University of Arizona, TucsonGoogle Scholar
  52. U’Ren JM, Dalling JW, Gallery R et al (2009) Diversity and evolutionary origins of fungi associated with seeds of a neotropical pioneer tree: a case study for analyzing fungal environmental samples. Mycol Res 113:432–449. doi: 10.1016/j.mycres.2008.11.015 CrossRefPubMedGoogle Scholar
  53. U’Ren JM, Lutzoni F, Miadlikowska J, Arnold AE (2010) Community analysis reveals close affinities between endophytic and endolichenic fungi in mosses and lichens. Microb Ecol 60:340–353. doi: 10.1007/s00248-010-9698-2 CrossRefPubMedGoogle Scholar
  54. U’Ren JM, Lutzoni F, Miadlikowska J, Laetsh A, Arnold AE (2012) Host and geographic structure of endophytic and endolichenic fungi at a continental scale. Am J Bot 99:898–914. doi: 10.3732/ajb.1100459 CrossRefPubMedGoogle Scholar
  55. U’Ren JM, Riddle JM, Monacell JT, Carbone I, Miadlikowska J, Arnold AE (2014) Tissue storage and primer selection influence pyrosequencing-based inferences of diversity and community composition of endolichenic and endophytic fungi. Mol Ecol Res 14:1032–1048. doi: 10.1111/1755-0998.12252 Google Scholar
  56. Ulrich W, Almeida-Neto M (2012) On the meanings of nestedness: back to the basics. Ecography 35:865–871. doi: 10.1111/j.1600-0587.2012.07671.x CrossRefGoogle Scholar
  57. Ulrich W, Gotelli NJ (2013) Pattern detection in null model analysis. Oikos 122:2–18. doi: 10.1111/j.1600-0706.2012.20325.x CrossRefGoogle Scholar
  58. Ulrich W, Almeida-Neto M, Gotelli N (2009) A consumer’s guide to nestedness analysis. Oikos 118:3–17. doi: 10.1111/j.1600-0706.2008.17053.x CrossRefGoogle Scholar
  59. Vázquez D, Melián C, Williams N, Blüthgen N, Krasnov BR, Poulin R (2007) Species abundance and asymmetric interaction strength in ecological networks. Oikos 116:1120–1127. doi: 10.1111/j.0030-1299.2007.15828.x CrossRefGoogle Scholar
  60. Vázquez D, Chacoff N, Cagnolo L (2009) Evaluating multiple determinants of the structure of plant–animal mutualistic networks. Ecology 90:2039–2046. doi: 10.1890/08-1837.1 CrossRefPubMedGoogle Scholar
  61. Verbruggen E, Van Der Heijden MGA, Weedon JT, Kowalchuk GA, Röling WFM (2012) Community assembly, species richness and nestedness of arbuscular mycorrhizal fungi in agricultural soils. Mol Ecol 21:2341–2353. doi: 10.1111/j.1365-294X.2012.05534.x CrossRefPubMedGoogle Scholar
  62. Wardhaugh CW, Edwards W, Stork NE (2015) The specialization and structure of antagonistic and mutualist networks of beetles on rainforest canopy trees. Biol J Linn Soc 114:287–295. doi: 10.1111/bij.12430 CrossRefGoogle Scholar
  63. Wehner J, Powell JR, Muller LAH, Caruso T, Veresoglou SD, Hempel S, Rillig MC (2014) Determinants of root-associated fungal communities within Asteraceae in a semi-arid grassland. J Ecol 102:425–436. doi: 10.1111/1365-2745.12197 CrossRefGoogle Scholar
  64. Wilson AWG, Morris WF, Bronstein JL (2003) Coexistence of mutualists and exploiters on spatial landscapes. Ecol Monogr 73:397–413. doi: 10.1890/02-0297 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • Pierre-Luc Chagnon
    • 1
    Email author
  • Jana M. U’Ren
    • 2
  • Jolanta Miadlikowska
    • 3
  • François Lutzoni
    • 3
  • A. Elizabeth Arnold
    • 2
    • 4
  1. 1.Université de SherbrookeSherbrookeCanada
  2. 2.School of Plant SciencesThe University of ArizonaTucsonUSA
  3. 3.Department of BiologyDuke UniversityDurhamUSA
  4. 4.Department of Ecology and Evolutionary BiologyThe University of ArizonaTucsonUSA

Personalised recommendations