Biological Invasions

, Volume 12, Issue 4, pp 943–957 | Cite as

Comparing the influences of ecological and evolutionary factors on the successful invasion of a fungal forest pathogen

  • Matteo Garbelotto
  • Rachel Linzer
  • Giovanni Nicolotti
  • Paolo GonthierEmail author
Original Paper


The fungal forest pathogen Heterobasidion annosum has been introduced from North America into Italy and is now associated with high mortality of Italian stone pines. Due to the presence of a closely related native H. annosum taxon, this pathosystem presents an unusual opportunity to test specific ecological and evolutionary factors influencing fungal invasions. Comparative inoculation experiments on Scots pine cuttings and on seedlings of European and North American pines failed to identify significant increased pathogenicity of North American genotypes on European hosts congruent with lack of host-pathogen co-evolution. However, spore trappings indicate that while reproductive potential of native H. annosum was significantly reduced in the dry season, that of the invasive taxon was consistently high regardless of season. Ecological differences between the native and exotic taxon may therefore facilitate this invasion. Understanding which factors enhance this emerging forest disease is important both for biotic invasion theory and for disease control.


Co-evolution Emerging infectious disease Fungi Heterobasidion Propagule pressure Pathogenicity 



We gratefully acknowledge Sergio Zerunian and the staff of the Circeo National Park. Thanks to Lydia Baker, Enrico Bonuso, Tami Harnik, Katy Hayden, Daniel Hüberli, Drew Linzer, Heather Rickard, Noah Rosenzweig, Amy Smith and Bret Voss for technical assistance with Experiment 2, and to Simona Ricca for technical assistance with Experiment 3. We also thank the anonymous reviewers for their constructive comments which greatly improved the manuscript. The research was partially supported by a grant of the University of Torino (60%).


  1. Asiegbu FO, Adomas A, Stenlid J (2005) Conifer root and butt rot caused by Heterobasidion annosum (Fr.) Bref. s.l. Mol Plant Pathol 6:395–409CrossRefPubMedGoogle Scholar
  2. Baker HG (1965) Characteristics and modes of origins of weeds. In: Baker HG, Stebbins GL (eds) The genetics of colonizing species. Academic Press, London, pp 141–172Google Scholar
  3. Balci Y, Balci S, MacDonald WL, Gottschalk KW (2008) Relative susceptibility of oaks to seven species of Phytophthora isolated from oak forest soils. For Pathol 38:397–409Google Scholar
  4. Blumenthal DM (2006) Interactions between resource availability and enemy release in plant invasion. Ecol Lett 9:887–895CrossRefPubMedGoogle Scholar
  5. Bodles WJA, Beckett E, Woodward S (2007) Responses of Sitka spruce of different genetic origins to inoculation with Heterobasidion annosum: lesion lengths, fungal growth and development of the lignosuberized boundary zone. For Pathol 37:174–186Google Scholar
  6. Bonello P, Capretti P, Luchi N, Martini V, Michelozzi M (2008) Systemic effects of Heterobasidion annosum s.s. infection on severity of Diplodia pinea tip blight and terpenoid metabolism in Italian stone pine (Pinus pinea). Tree Physiol 28:1653–1660PubMedGoogle Scholar
  7. Boyce JS Jr (1963) Colonization of pine stem sections by Fomes annosus and other fungi in two slash pine stands. Plant Dis Report 47:320–324Google Scholar
  8. Boyce JS Jr (1966) Sporulation by Peniophora gigantea with reference to control of Annosus root rot. For Sci 12:2–7Google Scholar
  9. Colautti RI, Ricciardi A, Grigorovich IA, MacIsaac HJ (2004) Is invasion success explained by the enemy release hypothesis? Ecol Lett 7:721–733CrossRefGoogle Scholar
  10. Čufar K, De Luis M, Eckstein D, Kajfež-Bogata L (2008) Reconstructing dry and wet summers in SE Slovenia from oak tree-ring series. Int J Biometeorol 52:607–615CrossRefPubMedGoogle Scholar
  11. D’Amico L, Motta E, Annesi T, Scirè M, Luchi N, Hantula J, Korhonen K, Capretti P (2007) The North American P group of Heterobasidion annosum s.l. is widely distributed in Pinus pinea forests of the western coast of central Italy. For Pathol 37:303–320Google Scholar
  12. Davis MA, Grime JP, Thompson K (2000) Fluctuating resources in plant communities: a general theory of invasibility. J Ecol 88:528–534CrossRefGoogle Scholar
  13. De Martonne E (1926) Une nouvelle fonction climatologique: l’indice d’aridité. La Metéorologie 2:449–458Google Scholar
  14. Despommier D, Ellis BR, Wilcox BA (2007) The role of ecotones in emerging infectious diseases. EcoHealth 3:281–289CrossRefGoogle Scholar
  15. Desprez-Loustau ML, Robin C, Buee M, Courtecuisse R, Garbaye J, Suffert F, Sache I, Rizzo DM (2007) The fungal dimension of biological invasions. Trends Ecol Evol 22:472–480CrossRefPubMedGoogle Scholar
  16. Dodd RS, Hüberli D, Douhovnikoff V, Harnik TY, Afzal-Rafii Z, Garbelotto M (2004) Is variation in susceptibility to Phytophthora ramorum correlated with population genetic structure in coast live oak (Quercus agrifolia)? New Phytol 165:203–214CrossRefGoogle Scholar
  17. Driver CH, Ginns JH Jr (1964) The effects of climate on occurrence of Annosus root-rot in thinned slash pine plantations. Plant Dis Report 48:509–511Google Scholar
  18. Duncan RP, Blackburn TM, Sol D (2003) The ecology of bird introductions. Annu Rev Ecol Syst 34:71–98CrossRefGoogle Scholar
  19. Ebert D, Bull JJ (2008) The evolution and expression of virulence. In: Stearns SC, Koella JC (eds) Evolution in health and disease, 2nd edn. Oxford University Press, Oxford, pp 153–167Google Scholar
  20. Elton CS (1958) The ecology of invasions by animals and plants. Methuen, LondonGoogle Scholar
  21. Facon B, Pointier JP, Glaubrecht M, Poux C, Jarne P, David P (2003) A molecular phylogeography approach to biological invasions of the New World by parthenogenetic Thiarid snails. Mol Ecol 12:3027–3039CrossRefPubMedGoogle Scholar
  22. Facon B, Genton BJ, Shykoff JA, Jarne P, Estoup A, David P (2006) A general eco-evolutionary framework for understanding bioinvasions. Trends Ecol Evol 21:130–135CrossRefPubMedGoogle Scholar
  23. Fausch KD (2008) A paradox of trout invasions in North America. Biol Invasions 10:685–701CrossRefGoogle Scholar
  24. Filip GM, Morrison DJ (1998) North America. In: Woodward S, Stenlid J, Karjalainen R, Hüttermann R (eds) Heterobasidion annosum, biology, ecology, impact and control. CAB International, New York, pp 405–427Google Scholar
  25. Fitt DBL, McCartney HA, Walkalate PJ (1989) The role of rain in dispersal of pathogen inoculum. Annu Rev Phytopathol 27:241–270CrossRefGoogle Scholar
  26. Garbelotto M (2004) Root and butt rot diseases. In: Burley J, Evans J, Youngquist JA (eds) The encyclopedia of forest sciences, vol 2. Elsevier, Oxford, pp 750–758Google Scholar
  27. Garbelotto M, Schmidt D (2009) Phosphonate controls sudden oak death pathogen for up to 2 years. Calif Agric 63:10–17CrossRefGoogle Scholar
  28. Garbelotto M, Cobb FW, Bruns TD, Otrosina WJ, Popenuck T, Slaughter G (1999) Genetic structure of Heterobasidion annosum in white fir mortality centers in California. Phytopathology 89:546–554CrossRefPubMedGoogle Scholar
  29. Garbelotto M, Gonthier P, Nicolotti G (2007) Ecological constraints limit the fitness of fungal hybrids in the Heterobasidion annosum species complex. Appl Environ Microbiol 73:6106–6111CrossRefPubMedGoogle Scholar
  30. Gernandt DS, Lopez GG, Garcia SO, Liston A (2005) Phylogeny and classification of Pinus. Taxon 54:29–42CrossRefGoogle Scholar
  31. Gilbert GS (2002) Evolutionary ecology of plant diseases in natural ecosystems. Annu Rev Phytopathol 40:13–43CrossRefPubMedGoogle Scholar
  32. Gonthier P, Warner R, Nicolotti G, Mazzaglia A, Garbelotto MM (2004) Pathogen introduction as a collateral effect of military activity. Mycol Res 108:468–470CrossRefPubMedGoogle Scholar
  33. Gonthier P, Garbelotto M, Nicolotti G (2005) Seasonal patterns of spore deposition of Heterobasidion species in four forests of the western Alps. Phytopathology 95:759–767CrossRefPubMedGoogle Scholar
  34. Gonthier P, Nicolotti G, Linzer R, Guglielmo F, Garbelotto M (2007) Invasion of European pine stands by a North American forest pathogen and its hybridization with a native interfertile taxon. Mol Ecol 16:1389–1400CrossRefPubMedGoogle Scholar
  35. Green S, MacAskill GA (2007) Pathogenicity of Marssonina betulae and other fungi on birch. Plant Pathol 56:242–250CrossRefGoogle Scholar
  36. Hawkes CV (2007) Are invaders moving targets? The generality and persistence of advantages in size, reproduction, and enemy release in invasive plant species with time since introduction. Am Nat 170:832–843CrossRefPubMedGoogle Scholar
  37. Hufbauer RA, Torchin ME (2007) Integrating ecological and evolutionary theory of biological invasions. In: Nentwig W (ed) Biological invasions. Springer, Berlin, pp 79–96CrossRefGoogle Scholar
  38. James RL, Cobb FW Jr (1984) Spore deposition by Heterobasidion annosum in forests of California. Plant Dis 68:246–248CrossRefGoogle Scholar
  39. Juliano SA, Lounibos LP (2005) Ecology of invasive mosquitoes: effects on resident species and on human health. Ecol Lett 8:558–574CrossRefPubMedGoogle Scholar
  40. Keane RM, Crawley MJ (2002) Exotic plant invasions and the enemy release hypothesis. Trends Ecol Evol 17:164–170CrossRefGoogle Scholar
  41. Korhonen K, Stenlid J (1998) Biology of Heterobasidion annosum. In: Woodward S, Stenlid J, Karjalainen R, Hüttermann R (eds) Heterobasidion annosum, biology, ecology, impact and control. CAB International, New York, pp 43–70Google Scholar
  42. Korhonen K, Capretti P, Karjalainen R, Stenlid J (1998) Distribution of Heterobasidion annosum intersterility groups in Europe. In: Woodward S, Stenlid J, Karjalainen R, Hüttermann R (eds) Heterobasidion annosum biology, ecology, impact and control. CAB International, New York, pp 93–104Google Scholar
  43. Lambrinos JG (2004) How interactions between ecology and evolution influence contemporary invasion dynamics. Ecology 85:2061–2070CrossRefGoogle Scholar
  44. Linzer RE, Otrosina W, Gonthier P, Bruhn J, Laflamme G, Bussières G, Garbelotto M (2008) Inferences on the phylogeography of the fungal pathogen Heterobasidion annosum, including evidence of interspecific horizontal genetic transfer and of human-mediated, long-range dispersal. Mol Phylogenet Evol 46:844–862CrossRefPubMedGoogle Scholar
  45. Mack RN, Simberloff D, Lonsdale WM, Evans H, Clout M, Bazzaz FA (2000) Biotic invasions: causes, epidemiology, global consequences, and control. Ecol Appl 10:689–710CrossRefGoogle Scholar
  46. Malmstrom CM, McCullough AJ, Johnson HA, Newton LA, Borer ET (2005) Invasive annual grasses indirectly increase virus incidence in California native perennial bunchgrasses. Oecologia 145:153–164CrossRefPubMedGoogle Scholar
  47. Mayr E (1965) The nature of colonizations in birds. In: Baker HG, Stebbins GL (eds) The genetics of colonizing species. Academic Press, London, pp 29–43Google Scholar
  48. Morales J, Gonzáles-Minero FJ, Carrasco M, Ogalla VM, Candau P (2006) Airborne basidiospores in the atmosphere of Seville. Aerobiologia 22:127–134CrossRefGoogle Scholar
  49. Moykkynen T, Kontiokari J (2000) Spore deposition of Heterobasidion annosum coll. in Picea abies stands of North Karelia, eastern Finland. For Pathol 31:107–114Google Scholar
  50. Olson A, Stenlid J (2001) Mitochondrial control of fungal hybrid virulence. Nature 411:438CrossRefPubMedGoogle Scholar
  51. Parker IM, Gilbert GS (2004) The evolutionary ecology of novel plant-pathogen interactions. Annu Rev Ecol Syst 35:675–700CrossRefGoogle Scholar
  52. Parker IM, Rodriguez J, Loik ME (2003) An evolutionary approach to understanding the biology of invasions: local adaptation and general-purpose genotypes in the weed Verbascum thapsus. Conserv Biol 17:59–72CrossRefGoogle Scholar
  53. Prinzing A, Durka W, Klotz S, Brandl R (2002) Which species become alien? Evol Ecol 4:385–405Google Scholar
  54. R Development Core Team (2007) R: a language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  55. Redfern DB, Stenlid J (1998) Spore dispersal and infection. In: Woodward S, Stenlid J, Karjalainen R, Hüttermann R (eds) Heterobasidion annosum, biology, ecology, impact and control. CAB International, New York, pp 105–124Google Scholar
  56. Rishbeth J (1951) Observations on the biology of Fomes annosus, with particular reference to East Anglian pine plantations. (III) Natural and experimental infection of pines, and some factors affecting severity of the disease. Ann Bot 15:221–246Google Scholar
  57. Sakai AK, Allendorf FW, Holt JS, Lodge DM, Molofsky J, With KA, Baughman S, Cabin RJ, Cohen JE, Ellstrand NC, McCauley DE, O’Neill P, Parker IM, Thompson JN, Weller SG (2001) The population biology of invasive species. Annu Rev Ecol Syst 32:305–332CrossRefGoogle Scholar
  58. Sax DF, Brown JH (2000) The paradox of invasion. Glob Ecol Biogeogr 9:363–371CrossRefGoogle Scholar
  59. Schwartz MW, Hoeksema JD, Gehring CA, Johnson NC, Klironomos JN, Abbott LK, Pringle A (2006) The promise and the potential consequences of the global transport of mycorrhizal fungal inoculum. Ecol Lett 9:501–515CrossRefPubMedGoogle Scholar
  60. Scirè M, D’Amico L, Motta E, Annesi T (2008) North American P type of Heterobasidion annosum shows pathogenicity towards Pinus halepensis in Italy. For Pathol 38:299–301Google Scholar
  61. Swedjemark G, Karlsson B (2006) Mycelial growth and exclusion of Heterobasidion parviporum inoculated in branches of 15-year-old Picea abies clones. For Pathol 36:209–214Google Scholar
  62. Tatem AJ, Rogers DJ, Hay SI (2006) Global transport networks and infectious disease spread. Adv Parasitol 62:293–343CrossRefPubMedGoogle Scholar
  63. Thoungchaleun V, Kim KW, Lee DK, Kim CS, Park EW (2008) Pre-infection behavior of the pitch canker fungus Fusarium circinatum on pine stems. Plant Pathol J 24:112–117Google Scholar
  64. Togashi D, Shigesada N (2006) Spread of the pinewood nematode vectored by the Japanese pine sawyer: modeling and analytical approaches. Pop Ecol 48:271–283CrossRefGoogle Scholar
  65. Torchin ME, Lafferty KD, Dobson AP, McKenzie VJ, Kuris AM (2003) Introduced species and their missing parasites. Nature 421:628–630CrossRefPubMedGoogle Scholar
  66. Werner A, Łakomy P (2002a) Host specialization of IS-group isolates of Heterobasidion annosum to Scots pine, Norway spruce and common fir in field inoculation experiments. Dendrobiology 47:59–68Google Scholar
  67. Werner A, Łakomy P (2002b) Intraspecific variation in Heterobasidion annosum for mortality rate on Pinus sylvestris and Picea abies seedlings growth in pure culture. Mycologia 94:856–861CrossRefGoogle Scholar
  68. Williamson MH, Fitter A (1996) The characters of successful invaders. Biol Conserv 78:163–170CrossRefGoogle Scholar
  69. Wingfield MJ, Slippers B, Roux J, Wingfield BD (2001) Worldwide movement of exotic forest fungi, especially in the tropics and the southern hemisphere. Bioscience 51:134–140CrossRefGoogle Scholar
  70. Woodward S, Stenlid J, Karjalainen R, Hüttermann A (eds) (1998) Heterobasidion annosum: biology, ecology, impact and control. CAB International, WallingfordGoogle Scholar
  71. Woolhouse MEJ, Haydon DT, Antia R (2005) Emerging pathogens: the epidemiology and evolution of species jumps. Trends Ecol Evol 20:238–244CrossRefPubMedGoogle Scholar
  72. Worrall JJ, Parmeter JR, Cobb FW (1983) Host specialization of Heterobasidion annosum. Phytopathology 73:304–307CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2009

Authors and Affiliations

  • Matteo Garbelotto
    • 1
  • Rachel Linzer
    • 1
  • Giovanni Nicolotti
    • 2
  • Paolo Gonthier
    • 2
    Email author
  1. 1.Department of Environmental Science, Policy and Management, Ecosystem Sciences DivisionUniversity of California at BerkeleyBerkeleyUSA
  2. 2.Department of Exploitation and Protection of the Agricultural and Forestry Resources (DIVAPRA), Plant PathologyUniversity of TorinoGrugliascoItaly

Personalised recommendations